Lignocellulosic Materials Into Biohydrogen and Biomethane: Impact of Structural Features and...

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Lignocellulosic Materials IntoBiohydrogen and Biomethane: Impact ofStructural Features and PretreatmentFlorian Monlau a , Abdellatif Barakat a , Eric Trably a , Claire Dumas a

, Jean-Philippe Steyer a & Hélène Carrère aa INRA, UR0050, Laboratoire de Biotechnologie de l’Environnement,Narbonne, FranceAccepted author version posted online: 21 Oct 2011.Publishedonline: 05 Feb 2013.

To cite this article: Florian Monlau , Abdellatif Barakat , Eric Trably , Claire Dumas , Jean-PhilippeSteyer & Hélène Carrère (2013): Lignocellulosic Materials Into Biohydrogen and Biomethane: Impactof Structural Features and Pretreatment, Critical Reviews in Environmental Science and Technology,43:3, 260-322

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Critical Reviews in Environmental Science and Technology, 43:260–322, 2013Copyright © Taylor & Francis Group, LLCISSN: 1064-3389 print / 1547-6537 onlineDOI: 10.1080/10643389.2011.604258

Lignocellulosic Materials Into Biohydrogenand Biomethane: Impact of Structural Features

and Pretreatment

FLORIAN MONLAU, ABDELLATIF BARAKAT, ERIC TRABLY,CLAIRE DUMAS, JEAN-PHILIPPE STEYER, and HELENE CARRERE

INRA, UR0050, Laboratoire de Biotechnologie de l’Environnement, Narbonne, France

Production of energy from lignocellulosic biomass or residues isreceiving ever-increasing interest. Among the different processes,dark fermentation for producing biohydrogen and anaerobic di-gestion for producing biomethane present considerable advantages.However, they are limited by the accessibility of holocelluloses thatare embedded in the lignin network. The authors propose a re-view of works on the conversion of biomass into biohydrogen andbiomethane with the comprehensive description of (a) biomass com-position and features that may impact on its anaerobic conversionand (b) the impact of different kinds of pretreatment on these fea-tures and on the performance of biohydrogen and methane pro-duction.

KEY WORDS: anaerobic digestion, biogas, dark fermentation, hy-drogen, lignocellulosic biomass, methane, physicochemical prop-erties, pretreatments

1. INTRODUCTION

The development of renewable sources of bioenergy has recently generatedconsiderable interest due to the energy crisis and global warming.

The use of lignocellulosic biomass as a source of bioenergy is partic-ularly interesting on account of its abundance, its renewability and the fact

Address correspondence to Abdellatif Barakat, INRA, UR0050, Laboratoire de Biotech-nologie de l’Environnement, Avenue des Etangs, F-11100 Narbonne, France. E-mail:[email protected]

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Lignocellulosic Materials Into Biohydrogen and Biomethane 261

that it does not create competition for land used for food or feed produc-tion (Kleinert and Barth, 2008; Ohman et al., 2006). The use of lignocellu-losic biomass for the production of the so-called second-generation biofuelshas recently been widely investigated for the production of liquid biofuels(Gnansounou, 2010; Hromadko et al., 2010; Sims et al., 2010; Sivakumaret al., 2010). The production of biomethane (Frigon and Guiot, 2010) andbiohydrogen (Guo et al., 2010a) from lignocellulosic biomass also needsto be considered. In fact, biomethane is a versatile energy source becauseit can be used to produce heat, electricity combined with heat (cogenera-tion), or biofuel. Compared to most liquid biofuels, biomethane has beenshown to have a far better performance with regard to both agricultural landarea efficiency and life cycle emissions (Borjesson and Mattiasson, 2008).Biohydrogen can be used in fuel cells to produce electricity or in inter-nal combustion engines. The main advantages to the use of hydrogen asa biofuel are the absence of CO2 emission, its high energy content, andits combustion kinetics (Koroneos et al., 2004). An alternative utilization ofhydrogen is as hythane gas, a mixture of hydrogen and methane. As a fuelin internal combustion engines, hythane offers several advantages comparedwith pure methane. Hydrogen has a flame speed eight times higher thanthat of methane and the addition of hydrogen to methane decreases theair/fuel ratio, resulting in a more stable combustion than with methanewhile at the same time-lowering emissions levels (Sierens and Rosseel,2000).

Biohydrogen and biomethane can be produced by dark fermentationand anaerobic digestion respectively (Figure 1). Anaerobic digestion is a bi-ological conversion process in which biomass is transformed into biogas, amixture of methane and carbon dioxide. The process can also be orientedtoward dark fermentation, H2 producing instead of CH4, by controlling suchoperational parameters in the reactor as pH and retention time and by in-hibiting methanogenesis (Hawkes et al., 2007; Nath and Das, 2004). Theresidue of an anaerobic digestion process is known as the digestate, madeup of stabilized organic materials that are enriched in nitrogen and phos-phorus (Frigon and Guiot, 2010). The digestate can thus be used as anenvironmentally friendly fertilizer for growing biomass (Figure 1).

Lignocellulosic biomass consists of holocelluloses (cellulose, hemicellu-loses) and lignin fractions (Figure 1), which quantitatively and qualitativelyvary according to the plant material (Aman, 1993). Holocelluloses, which arethe major component of most lignocellulosic materials, have been shownto be anaerobically biodegradable in their pure form. But hemicellulosesand lignin are covalently bonded through lignin–carbohydrate complexes,as demonstrated several decades ago by Bjorkmann (1957). These covalentlinks are important in the biological roles of plant cell walls (mechanicalresistance, protection against pathogens) and in the ability of lignocellulosic

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262 F. Monlau et al.

FIGURE 1. Strategy of biohydrogen and biomethane production from lignocellulosic materi-als in integrated lignocellulosic biomass production (Color figure available online).

materials to be transformed in practical application (i.e., production of pulpor chemicals, biodegradation, bioethanol, biohydrogen, biogas). Hemicel-luloses serve as connections between the lignin and the cellulose fibersand give rigidity to the whole cellulose–hemicellulose–lignin network (Atallaet al., 1993; Laureano-Perez et al., 2005; Salmen and Olsson, 1998). However,lignin content and the lignin-carbohydrate matrix limit the digestibility of lig-nocellulosic biomass because lignin is a cross-linked network hydrophobicpolymer that remains insoluble in all solvents and is fairly resistant to anaer-obic degradation (Monties and Fukushima, 2001; Watanabe et al., 2003).The presence of lignin is apparently the most important factor affecting thebiodegradability of lignocellulosic materials although others factors such asthe crystallinity of cellulose and accessible surface area may also play animportant role (Chang and Holtzapple, 2000; Koullas et al., 1992; Laureano-Perez et al., 2005; Puri, 1984).

Hence, both yields and rates of biohydrogen and biomethane produc-tion from biomass can be enhanced by the pretreatment of lignocellulosic

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materials. Such pretreatment should make hollocelluloses more accessibleto the microorganisms involved in the biological process. The objectives ofsuch pretreatments are thus to dissolve lignin structure (delignification), re-duce the degree of polymerization of cellulose and hemicelluloses, decreasethe crystallinity of cellulose and increase the available surface area. Manytypes of pretreatment have been widely investigated for the production ofsecond-generation bioethanol and several review papers published (Demir-bas, 2005; Galbe and Zacchi, 2007; Galbe and Zacchi, 2002; Kumar et al.,2009a; Mosier et al., 2005; Sun and Cheng, 2002). These pretreatments aregenerally divided into four categories: physical (milling, irradiation), chem-ical (alkali, acid, oxidizing agents, and organic solvents), thermal (steamexplosion; ammonia fiber explosion [AFEX], wet oxidation), biological andenzymatic, or a combination of two of them. However, the choice of thepretreatment is closely related to the final product. Bioethanol productionuses only cellulose and the objective of pretreatment is to separate ligninand hemicelluloses from cellulose in order to enhance enzymatic cellulosehydrolysis, whereas biohydrogen and biomethane production may use bothcellulose and hemicelluloses. The application of pretreatments to improvethe anaerobic digestion or dark fermentation of lignocellulosic biomass hasbeen less well investigated than their use in bioethanol production. However,the anaerobic digestion of lignocellulosic materials has been shown to be lim-ited by the biological hydrolysis step and the accessibility of biodegradablecompounds (cellulose and hemicelluloses) (Pavlostathis and Giraldogomez,1991). Thus, to achieve high biodegradation yields, lignocellulose must firstbe pretreated.

The objective of this article is to review previous work dealing with theproduction of biohydrogen and biomethane from lignocellulosic biomass,with special attention paid to the impact and mechanisms of pretreatmentprocesses. First, the composition of lignocellulosic material is described. In asecond part, properties that can impact the biological conversion of biomass(degree of polymerization, crystallinity, accessible surface area, lignin con-tents) are mentioned. Then, lignocellulosic pretreatments are detailed andtheir influences on the previously mentioned parameters are discussed. Fi-nally, the association of biohydrogen and biomethane processes is presented,along with the effect of pretreatments on biohydrogen and biomethane pro-duction.

2. COMPOSITION OF LIGNOCELLULOSIC MATERIALS

The composition of biomass depends essentially on the nature of the feed-stock (Mosier et al., 2005). Cellulose is most abundant, representing 30–70%of lignocellulosic biomass while hemicelluloses and lignin represent 15–30%and 10–25% of the biomass, respectively (Table 1).

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TA

BLE

1.

Bio

chem

ical

com

posi

tion

ofdiffe

rentlig

noce

llulo

sic

bio

mas

sG

rass

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getic

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Softw

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Lign

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pla

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nst

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canth

us

Popla

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lyptu

sSp

ruce

Pin

e

Cel

lulo

ses

(%)

39.6

42.5

36.8

32.0

37.5

41.7

39.8

38.0

37.7

44.5

54.1

45.5

43.3

Mw

(g/m

ol)

250.

720

——

272.

130

337.

820

382.

210

—24

1.83

0—

171.

950

——

—D

P15

47—

7050

1680

2085

2360

—14

39—

1091

——

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rI50.3

—50.3

51.7

——

——

—49.9

54.3

38.4

—H

emic

ellu

lose

s(%

)26.6

21.2

30.6

18.0

25.3

18.9

29.7

36.9

37.3

22.5

18.4

22.9

21.5

Xyl

ose

(Xyl

)24

.315

.422

.214

.321

.711

.8—

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.819

.415

.06.

65.

3Ara

bin

ose

(Ara

)2.

13.

15.

52.

32.

51.

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—2.

80.

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51.

21.

6

Gal

acto

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nose

——

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10.

61.

513

.510

.7A

ra/X

yl0.0

90.2

00.2

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60.1

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—0.0

80.0

25

0.0

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80.3

Lign

in(%

)21.0

3.4

23.1

11.2

16.0

26.1

2.6

17.6

25.1

19.5

21.5

27.9

28.3

FA/p

CA

1.2/

0.64

0.44

/0.0

1—

1.22

/0.6

11.

27/1

.28

0.82

/0.3

2—

1.42

/0.4

5—

——

——

G/S

/H49/4

6/0

5—

35/6

1/4

45/6

0/1

5—

——

44/5

4/2

—41/5

9/n

d38/6

2/n

d98/t

r/2

82/t

r/18

β-O

-4(μ

mol/

gof

lignin

)1040

—610

630

——

—1610

—2390

2780

1230

1140

Mw

(g/m

ol)

2800

——

3600

3200

3600

—30

00—

5500

≥50

00≥

6000

≥80

00O

ther

s(%

)5.

5—

9.5

14.2

6.4

3.1

7.3

6.3

——

3.0

4.2

7.9

Ref

eren

ces

(Akp

inar

etal

.,20

09;

Lapie

rre,

1993

;Le

quar

tet

al.,

1999

;Su

net

al.,

2005

;Su

net

al.,

2002

a)

(Leq

uar

tet

al.,

1999

)

(Lap

ierr

e,19

93;Su

net

al.,

2005

;Su

net

al.,

2001

;Ter

amoto

etal

.,20

09)

(Per

sson

etal

.,20

09;Su

net

al.,

2005

;Su

net

al.,

2002

a;Ter

amoto

etal

.,20

09)

(Akp

inar

etal

.,20

09;

Gullo

net

al.,

2009

;Su

net

al.,

2005

)

(Kiv

aisi

and

Elia

-pen

da,

1994

)

(Lap

ierr

e,19

93;Su

net

al.,

2005

)

(Agu

ilar

etal

.,20

02)

(Bro

sse

etal

.,20

09)

(Guer

raet

al.,

2006

;La

pie

rre,

1993

;Popes

cuet

al.,

2009

;Sa

ntia

goan

dN

eto,

2008

;Su

net

al.,

2005

)

(Gal

be

and

Zac

chi,

2007

;G

uer

raet

al.,

2006

;La

pie

rre,

1993

;Sa

ntia

goan

dN

eto,

2008

)

(Gal

be

and

Zac

chi,

2007

;La

pie

rre,

1993

;Pal

man

dZac

chi,

2004

;Popes

cuet

al.,

2009

)

(Gal

be

and

Zac

chi,

2007

;La

pie

rre,

1993

;Tej

ado

etal

.,20

07)

Not

e.pCA

=p-c

oum

aric

acid

;FA

=fe

rulic

acid

;G

=gu

aiac

ylunits

inlig

nin

;S

=sy

ringy

lunits

;H

=p-h

ydro

xyphen

yl;

Mw

=m

ole

cula

rm

ass;

DP

=deg

ree

of

poly

mer

izat

ion;CrI

=cr

ysta

llinity

index

;nd

=notdet

ecte

d;tr

=trac

es.

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2.1 Cellulose

Cellulose consists of D-glucose subunits, linked by β-(1→4) glycosidicbonds (Fengel, 1992; Fengel and Wegener, 1984). The cellulose in aplant consists of parts with an organized crystalline structure and partswith a poorly organized amorphous structure. The cellulose strains arebundled together and form so-called cellulose fibrils or cellulose bundles.These cellulose fibrils are mostly independent and weakly bound throughhydrogen binding (Atalla and Vanderhart, 1984; Liang and Marchessault,1959; Vanderhart and Atalla, 1984). Cellulose, insoluble in water and mostorganic solvents, is chiral and biodegradable. It can be broken downchemically into its glucose units by treating it with concentrated acids athigh temperature. Many properties of cellulose depend on its chain length,crystallinity, or degree of polymerization.

2.2 Hemicelluloses

Hemicelluloses can be any of the heteropolymers (matrix polysaccha-rides) present in almost all plant cell walls along with cellulose (Figure 2;Aman, 1993). While cellulose is crystalline, strong and resistant to hy-drolysis, hemicelluloses have a random, amorphous structure with littlestrength. Hemicelluloses have a lower molecular weight than cellulose.It has branches with short lateral chains that consist of different sugarmonomers and can include xylose, mannose, galactose, rhamnose, and ara-binose, which are polymers that can be easily hydrolyzed (Ebringerovaand Heinze, 2000; Fengel and Wegener, 1984; Kacurakova et al., 1999)by both dilute acid or a base as well as by numerous hemicellulase en-zymes. Xylose is always the sugar monomer present in the largest amount,though uronic and ferulic acids also tend to be present (Table 1). Thedominant component of hemicelluloses from hardwood and agriculturalplants such as grasses and straw is xylan, while in softwoods glucoman-nan is dominant (Ebringerova and Heinze, 2000; Ebringerova et al., 1994;Fengel and Wegener, 1984; Sun et al., 1996). Hemicelluloses are embed-ded in the cell walls of plants, sometimes in chains that form a ground:they bind to cellulose with pectin to form a network of cross-linked fibersmade up of hemicelluloses and lignin which are covalently linked throughlignin–carbohydrate complexes (LCCs) and, as such, represent a limitingfactor in the biodegradation of lignocellulosic materials (Watanabe et al.,2003). The hemicelluloses are the most thermal-chemically sensitive of lig-nocellulosic components (Levan and Winandy, 1990; Sweet and Winandy,1999; Winandy et al., 1991). During thermal–chemical pretreatment, theside groups of hemicelluloses react first, followed by the hemicellulosesbackbone.

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2.3 Lignin

Lignin is the third most abundant polymer in nature, after cellulose andhemicelluloses, and is present in cell walls. It is an amorphous heteropoly-mer consisting of three different phenylpropane alcohols: p-coumaryl (H),coniferyl (G), and sinapyl (S) (Figure 2). The nature and the quantity of ligninmonomers (H, G, S) vary according to species, maturity, and the space local-ization in the cell (Yoshizawa et al., 1993). For instance, an increase in lignincontent from 3% to 7% was observed during the maturing of grass (Nizamiet al., 2009). The biosynthesis process consists, in the main, of the couplingof radicals and creates a unique lignin polymer in each plant species (Fig-ure 2; Boerjan et al., 2003; Vanholme et al., 2010). There are three maingroups of lignins: the lignins from softwoods (gymnosperms) contain mainly

FIGURE 2. Simplified scheme of the lignification, supramolecular organization, and composi-tion of plant cell walls in a lignocellulosic matrix. Monolignols oxidized by a peroxydase/H2O2

system form radicals. The coupling and oxidation of these radicals result in lignin polymer(Color figure available online).

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guaıacyl units, those from hardwoods (angiosperms) mainly guaıacyl andsyringyl units, whereas the lignins from herbaceous plants (non-woody orgramineae) contain all three units (H, G, S) in significant amounts with dif-ferent ratios (Billa and Monties, 1995; Boerjan et al., 2003; Lapierre et al.,1986; Nimz et al., 1981; Vanholme et al., 2010). They are held together bydifferent kinds of linkage (Adler, 1977; Akiyama et al., 2002; Sarkanen, 1971;Sarkanen and Hergert, 1971). These are classified as either carbon-carbonbonds (5–5, β-1, β-5, β-β) or diaryl-ether (4-O-5), both of which are con-densed. They are resistant to usual chemical degradation. Other connectionsdescribed as noncondensed or unstable are of the type aryl-ether (α-O-4,β-O-4), the β-O-4 bonds being the most frequent in natural lignins. Themain purpose of lignin is to give the plant structural rigidity, impermeability,and resistance against microbial attack and oxidative stress. The amorphousheteropolymer is also insoluble in water and optically inactive, which makesthe degradation of lignin very difficult (Akin, 2008; Fengel and Wegener,1984; Grabber, 2005). Like hemicelluloses, lignin normally starts to dissolvein water at around 180◦C under neutral conditions (Kubikova et al., 1996).The solubility of lignin in acidic, neutral, or alkaline environments depends,however, on the precursor of the lignin (p-coumaryl, coniferyl, sinapyl alco-hols or combinations of them) (Grabber, 2005).

3. FACTORS AFFECTING ACCESSIBILITY ANDBIODEGRADABILITY OF LIGNOCELLULOSIC MATERIALS

The mechanical, physical, chemical, and biological properties of lignocellu-losic materials are dependent not only on the chemical composition of thematrix but also on the organization of their constituents and the interactionbetween them (Salmen and Olsson, 1998). The cell wall may be schematicallyviewed as cellulose microfibril bundles arranged in parallel in a matrix ofamorphous hemicelluloses and lignin, as shown in Figure 2. A considerableamount of work has been carried out to try to determine the substrate charac-teristics that lead to a decrease in the rate of cellulose hydrolysis and, in manycases, incomplete hydrolysis of the lignocellulosic substrates (Hendriks andZeeman, 2009; Koullas et al., 1992; Tarantili et al., 1996; Yoshida et al., 2008;Zhu et al., 2008). Most of this work has concerned bioethanol productionand focused on the separation of cellulose from lignin and hemicellulosesin order to enhance enzymatic cellulose hydrolysis. However, some studiesprovide insight useful in assessing or understanding the anaerobic biodegrad-ability of lignocellulosic materials. Indeed, the anaerobic digestion of suchmaterials has been shown to be limited by the biological hydrolysis stepas well as by the accessibility of biodegradable compounds (cellulose andhemicelluloses; Pavlostathis and Giraldogomez, 1991). Thus, to achieve highbiodegradation yields or high yields of polysaccharide monomers (glucose

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and xylose), lignocellulose must first be pretreated. Moreover, biologicaldegradation (anaerobic digestion or enzymatic hydrolysis) can be affectedby factors such as the degree of polymerization and crystallinity of the cellu-lose, the structure of hemicelluloses, structural surface area and pore volume,lignin composition and content and cross-linking Lignin Carbohydrate Com-plex (LCCs).

3.1 Crystallinity and Degree of Polymerization of Cellulose

It has been suggested that during the enzymatic hydrolysis of cellulosethe readily accessible regions (amorphous regions) are more efficiently hy-drolyzed, resulting in an accumulation of crystalline cellulose (Hayashi et al.,2005). Other authors have suggested that the decreasing rate of cellulosedegradation occurs as a result of structural transformations during the initialstages of hydrolysis with the result that the more resistant fraction remainsunhydrolyzed (Gupta and Lee, 2009; Jeoh et al., 2007; Mansfield and Meder,2003; Mooney et al., 1999) and as a consequence, cellulase digestibility of thetreated biomass is limited by cellulose accessibility. Many properties of cel-lulose depend on its crystallinity (CrI), molecular weight (Mw), particle size,degree of polymerization, surface area, and solubility, all of which dependon the species, plant part, and plant maturity (Table 1). All these parametershave been shown to influence the enzymatic hydrolysis of cellulose. Somework has shown a good correlation between crystallinity and the rate of en-zymatic hydrolysis of pure cellulose. However, with lignocellulosic materialsthis relationship is not so clear-cut, due to the more heterogeneous natureof this material and the contribution of other components such as lignin andhemicelluloses (Chang and Holtzapple, 2000; Ciolacu et al., 2008; Gupta andLee, 2009; Koullas et al., 1992; Lee et al., 2010).

3.2 Physicochemical Properties of Hemicelluloses

In contrast to cellulose, the effect of the physicochemical properties ofhemicelluloses on the accessibility of lignocellulosic substrates and theirbiodegradability into biogas and bioethanol has not been studied. Yet, of thetotal mass in the residues of annual plants, which can be fermented to biogas,hemicelluloses (C5-sugars) represent about 15–30%. Hemicelluloses serve asa connection between the lignin and the cellulose fibers and give rigidityto the whole cellulose–hemicellulose–lignin network (Salmen and Olsson,1998; Watanabe et al., 2003). In general, the dominant hemicelluloses fromall plant cell walls are xylans (Table 1). Xylans display significant variabilityin their structural characteristics. The structure of xylan is more complex thanthat of cellulose and has been fully described in several reviews on hemi-celluloses in wood (Puls, 1997) and grass (Izydorczyk and Dexter, 2008;Izydorczyk and MacGregor, 2000; Puls, 1997; Roubroeks et al., 2000; Saake

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et al., 2001). Xylan structure depends on the degree of substitution of the xy-lose linear chains by arabinose, hydroxycinnamic, and uronic acids and themolar mass. All these parameters depend on the species, plant part, and plantmaturity as shown in Table 1 (Aman, 1993; Dervilly et al., 2000; Ebringerovaet al., 1994; Izydorczyk, 2009; Saulnier et al., 1997; Saulnier et al., 1999). Thetype and the distribution of substitution determine the degree of solubilityas well as the capacity to bind to the components of the plant cell wall.Ferulic and p-coumaric acids (Figure 3C) represent the major cross-linkingphenolic acids in the cell walls of grasses (Russel et al., 2000; Russell et al.,1999; Tuyet Lam et al., 1992; Wallace and Fry, 1994). The presence of ferulicand p-coumaric acids further increases the chemical and structural complex-ity of xylans and, as a consequence, impacts the enzymatic accessibilityand biodegradability of hemicelluloses (Beaugrand et al., 2004a; Beaugrandet al., 2004b; Benamrouche et al., 2002; Bernard Vailhe et al., 2000; Fauldset al., 2006; Grabber, 2005). Considering the chemical and structural com-plexity of grass hemicelluloses, it is not surprising that nature has developeda complete arsenal of hemicellulose-hydrolyzing enzymes that, through theirconcerted action, bring about complete degradation of these polymers. Themain depolymerizing enzyme is xylanase whose action is complementedby that of arabino-hydrolyzing enzymes such as α-L-arabinofuranosidase,β-D-xylosidase, α-D-glucuronidase, and β-feruloyl esterases. Generally, xy-lanase action is most efficient on β-(1,4) bonds linking nonbranching xylose

FIGURE 3. (A) Chemical structure of ferulic acid and p-coumaric acid and chemical structureof lignin-carbohydrate complex (LCC), (B) via glucuronic acid and arabinose (woody plantcell walls), and (C) via phenolic acids and arabinose non-wood (grass cell walls) (Color figureavailable online).

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residues. Therefore, the specific structural features of xylan, such as thedegree of branching and the oxidative coupling of xylan-xylan chains (feru-late dimers) or xylan-lignin via hydroxycinnamic acid, form a cohesive wallnetwork that may limit enzyme access (Figure 3).

3.3 Surface Area and Pore Volume

Others parameters such as pore volume and surface area have been shown toaffect the biodegradability of lignocellulosic materials. Several groups showgood correlation between pore volume, surface area, and the enzymatic di-gestibility of lignocellulosic materials (Chang and Holtzapple, 2000; Koullaset al., 1992; Laureano-Perez et al., 2005; Park et al., 2007; Puri, 1984). Increas-ing the surface area of a substrate enhances its digestibility. But this may beinfluenced by the lignin content and distribution. Indeed, alkali washing ofa steam-exploded substrate resulted in decreased hydrolysis rates, despitean increase in pore volume and the reduced lignin content of the substrate(Mooney et al., 1998).

3.4 Lignin Content and Composition

One of the major roles of lignin is to maintain fiber integrity and the struc-tural rigidity of the plant. Lignin is a polymer of phenylpropane units thatform a three-dimensional network inside the cell wall. The major inter-unitlinkage is an aryl-ether type β-O-4 link. The macromolecular structure of thelignin polymer depends on the β-O-4 linkage, monomer distribution (G, S,and H), and molecular weight, all of which depend on the species, plantpart, and plant maturity (Fukushima and Terashima, 1991; Vanholme et al.,2010). These different parameters modify the architecture and supramolecu-lar organization of the cell wall and influence its accessibility and digestibil-ity (Akin et al., 1995; Chang and Holtzapple, 2000; Jung and Engels, 2002;Laureano-Perez et al., 2005; Tian et al., 2010). The enzymatic degradabil-ity of cell walls in leaves and particularly in the stems of plants declinesduring maturing because of accumulation and progressive lignification ofthe primary and secondary cell walls of vascular and sclerenchyma tissues.Such reduced biodegradability is partly related to the increased lignin con-tent of cell walls. However, variations in three-dimensional structure, thecomposition of lignin and its hydrophobicity, encrustation, supramolecularorganization, and cross-linking to other matrix components have also beenimplicated (Boukari et al., 2009).

The distribution and composition of lignin are also very important forenzyme accessibility and the digestibility of biomass (Adler, 1977; Clark et al.,2009; Guo et al., 2010b; Ntaikou et al., 2010; Yuan et al., 2008). For example,these factors have been cited as being responsible for the higher recalci-trance of softwood-derived substrates (Mooney et al., 1999; Mooney et al.,

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1998). It has also been suggested that guaıacyl lignin restricts fiber swellingand, hence, enzyme accessibility more than syringyl lignin. G-type units areable to form C–C bonds, but this is not possible in S-type units as theyhave a C5 position substituted by a methoxy group (Figure 2). This struc-tural variability of the lignin polymer can influence the reactivity of ligninmolecules, for example in the course of depolymerization and repolymer-ization reactions during pretreatment. Depolymerization/repolymerization oflignin molecules is a very important parameter that impacts on the accessibil-ity and biodegradability of lignocellulosic biomass. The original C–C bondsand C–C bonds formed by repolymerization are not cleaved during pretreat-ment of the lignocellulosic biomass (for example, in pulping wood) due totheir higher stability. As a consequence, lignins whose composition is strictlyof G and G-H units are expected to show higher molecular weight than thosepresenting a high level of S units. Under highly alkaline conditions, someα-hydroxyl groups form quinone methide (Figure 2) that reacts easily withother lignin fragments, giving alkali-stable methylene linkages (Ralph andYoung, 1983; Sipila, 1990; Sipila and Brunow, 1991). This reaction, occurringespecially during the Kraft process due to the more severe conditions used,causes the formation of species with a high molecular weight.

In an attempt to correlate substrate accessibility with the efficiency ofenzymatic hydrolysis, various studies measured the initial enzyme adsorptioncapacity of different substrates and correlated this with the initial rates ofhydrolysis. It was found that substrates containing little or no lignin showedgood correlation between initial hydrolysis rates and adsorption capacity,while substrates with higher lignin content demonstrated a poor correlation(Chang and Holtzapple, 2000; Koullas et al., 1992).

3.5 Lignin-Carbohydrates Complex: LCC

Lignin is associated with other cell wall polysaccharides to form an LCC.The first two components are hydrophilic whereas the latter is hydropho-bic (Barakat et al., 2008; Monties and Fukushima, 2001). LCCs are insolublein water and partially soluble in organic solvents (Wong et al., 1996; Yakuet al., 1981). Such a complex structure makes lignocellulosic materials hard tobiodegrade and difficult to use by microorganisms, resulting in low hydroly-sis rates. Lignin does not exist in plant tissue as an independent polymer butis always associated with hemicelluloses, not only as physical mixtures, butthrough covalent bonds (LCC). The mechanism of formation of LCC can bedivided into two main processes. The first is based on the oxidative couplingof phenolic compounds in plant cell walls (Figure 3C). This process is re-stricted to herbaceous species. The second process, ubiquitous in all lignifiedcell walls (Terashima, 2001; Xi et al., 2000), involves the attack of nucleophilicgroups (i.e., hydroxyl or carboxylic groups of hemicelluloses, phenols, wa-ter) generally on the α-carbon of transient quinone methide intermediate

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generated during the oxidative polymerization of lignin (Freudenberg andNeish, 1968; Tanaka et al., 1979; Toikka and Brunow, 1999; Watanabe et al.,1986; Figure 2).

The cleaving of LCC bonds and the removal of lignin remain the majorobstacles to the biodegradability of lignocellulosic biomass. If LCC bonds arecleaved, the cellulose/hemicelluloses become more accessible for enzymatichydrolysis and fermentation. In herbaceous plants, hydroxycynamic acids(p-coumaric and ferulic acids; Figure 3A) are attached to lignin and hemicel-luloses via ester and ether bonds as bridges between lignin and hemicellu-loses forming lignin/phenolics–carbohydrate complexes (Figure 3C) (Barakatet al., 2007; Barakat et al., 2008; Sun et al., 2002a; Wallace and Fry, 1994).However, lignin and carbohydrates in wood are attached to each other viabenzyl-ether and benzyl-ester bonds (Figure 3B). The direct evidence for theexistence of these LCC is obtained with the oxidative cleavage of benzyl-etherand benzyl-ester bonds, reduction, methylation analysis, chromatography,spectroscopy and electron microscopy. More detailed information on recentdevelopments related to LCC in wood has been published by Koshijima andWatanabe (Watanabe et al., 2003).

The LCCs from grasses are structurally different from those in woodand contain ferulic bridges between lignin and carbohydrates (xylans)via ester-linked ferulic acids (Grabber and Lu, 2007; Wallace and Fry,1994; Wallace et al., 1995). Therefore, they are often referred to aslignin/phenolic–carbohydrate complexes (Figure 3C). Ferulic acid is attachedto lignin with ether bonds and to carbohydrates with ester bonds (DasNath et al., 1981; Quideau and Ralph, 1997; Takahashi and Koshijima, 1988;Wallace and Fry, 1994; Wallace et al., 1995). Ferulate dimers, already cross-linking polysaccharide chains, can also be incorporated into lignins via anoxidative mechanism (Figure 3C). It is generally accepted that the associationof phenolic components with carbohydrates presents the greatest barrier tothe utilization of carbohydrates. Whether this barrier is caused primarily bypolyphenols (i.e., lignin), oligomeric phenols or monophenols is debatableand it may depend on the species, plant part, and plant maturity. Therefore,specific fractionation technology must be designed for each herbaceous crop,depending on its lignin structure.

4. EFFECTS OF PRETREATMENT ON STRUCTURAL FEATURES

Lignin in plant cell walls combines with holocelluloses to form carbohydratecomplexes (LCC). These LCCs make the plant cell wall resistant to micro-bial attack. Therefore, prior to anaerobic digestion, a pretreatment processthat alters the structure and composition of the substrate may be usefulto break up the lignocellulosic feedstock. The main objective of pretreat-ment in biohydrogen and biomethane production is delignification so as

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to make the holocelluloses more accessible to microbial attack. The crys-tallinity of cellulose is another important factor governing anaerobic di-gestion. Indeed, during pretreatment it is important to reduce the crys-tallinity of cellulose because the crystalline structure prevents penetrationby microorganisms. But effective pretreatment may also increase porosity,reduce the degree of polymerization of holocelluloses and be environmen-tally friendly. Finally, pretreatment has to be as cost-effective as possiblebecause several economic models show that pretreatment is an essential op-eration requiring a dedicated unit in a lignocellulosic biorefinery, account-ing for 16–19% of total cost equipment (Aden et al., 2002). In order tofacilitate the production of methane and hydrogen from lignocellulosic sub-strates, several types of pretreatment can be carried out to accelerate thehydrolysis phase and to increase the availability of compounds. Pretreat-ment methods can be divided into different categories: mechanical, chem-ical, thermal, thermo-chemical and biological or various combinations ofthese.

4.1 Mechanical Pretreatment4.1.1 MECHANICAL COMMINUTION

Mechanical pretreatment methods include chipping, grinding, milling (e.g.,two-roll, hammer, colloid, vibro ball). Such mechanical pretreatment leadsto a reduction in the particulate size, usually to 10–30 mm after chipping and0.2–2 mm after milling or grinding. Mechanical pretreatment transforms thebiomass into a fine powder, thus increasing the surface area of the celluloseand reducing the degree of crystallinity of celluloses as well as decreasingthe degree of polymerization of celluloses and hemicelluloses (Galbe andZacchi, 2007; Palmowski and Muller, 2000; Taherzadeh and Karimi, 2008).

Gharpuray et al. (1983) investigated the effects of ball milling, fitzmilling, and roller milling on the structural features (crystallinity, surface area,and lignin content) of wheat straw. Ball milling pretreatment was found tobe effective in increasing the specific surface area (2.3 m2/g compared with0.64 m2/g for the raw wheat straw) and decreasing the crystallinity index(23.7 compared with 69.6 for the raw wheat straw; Gharpuray et al., 1983).Palmowski et al. (2003) have also studied the effect of comminution ondifferent organic samples (apples, rice, sunflower seeds, hay, and mapleleaves). After comminution of these substrates, a release of soluble organiccompounds occurred for two reasons: cells were destroyed through com-minution; and/or the dissolution of organic components through newly gen-erated accessible surfaces (Palmowski and Muller, 2003). However, Bridge-man et al. (2007) showed that a big reduction in the size of switchgrass isundesirable as it causes significant carbohydrate losses that ultimately resultin a small amount of reducing sugars. Moreover, this process is not cost-effective because it requires too much energy and it has been shown that

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greater amounts of energy are needed to reduce size when biomass has ahigher moisture content (Yu et al., 2006).

4.1.2 OTHER TYPES OF MECHANICAL PRETREATMENT

Digestibility of lignocellulosic biomass can also be enhanced by use of high-energy radiation using γ -rays, electron beam, or microwaves. Kumakura andKaetsu (1983) investigated the effect of irradiation pretreatment on bagasse:after enzymatic hydrolysis, a double yield of glucose was observed for thepretreated sample. Cleavage of β-(1,4)-glycosidic bonds leading to an in-crease in surface area and a reduction in crystallinity was observed afterapplying γ -rays to cellulose (Takacs et al., 2000).

Microwave pretreatment combined with acid pretreatment (HCl) wasused on wheat straw and wheat bran (Fan et al., 2005; Pan et al., 2008). Thetotal soluble sugar in the microwave-assisted acid-pretreated wheat bran in-creased from 0.086 g/gTS to 0.461 g/gTS at 9 min hydrolysis time. Generally,microwave irradiation can change the ultrastructure of cellulose, degradehemicelluloses, and increase the accessibility of the substrate (Zhu et al.,2005). However, microwave pretreatment has several disadvantages, includ-ing high energy consumption, complicated operation procedures, and strictmonitoring of equipment (Pan et al., 2008).

4.2 Thermal Pretreatment4.2.1 LIQUID HOT WATER

During liquid hot water (LHW) treatment, the lignocellulosic substrate isheated to a high-temperature (200–230◦C) for a few minutes. Water underhigh pressure can penetrate into the biomass, increasing surface area andhence the removal of hemicelluloses and lignin. Generally, all the hemicellu-loses, 35–60% of the lignin, and 4–22% of the cellulose are dissolved (Mosieret al., 2005; Wyman et al., 2005).

Three types of reactor can be used for liquid hot water pretreatment:cocurrent (biomass and water are heated together for a certain residencetime), countercurrent (water and lignocelluloses move in opposite direc-tions), and flow-through (hot water passes over a stationary bed of lignocel-luloses) (Liu and Wyman, 2005).

4.2.2 STEAM EXPLOSION

During steam explosion, lignocellulosic biomass is heated rapidly to a hightemperature (160–260◦C) with sufficient pressure (7–50 bar) to enable watermolecules to penetrate the substrate structure for a few minutes. The pressureis then suddenly released to allow the water molecules to escape in anexplosive manner. This pretreatment opens up the plant cells, increasessurface area, and enhances the digestibility of biomass (Ballesteros et al.,2000). According to Ramos (2003), lignin is primarily degraded through the

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homolytic cleavage of β-O-4 ether and other acid-labile linkages, producinga series of cinnamyl alcohol derivatives and by-products of condensation.

One limitation of steam explosion is the incomplete disruption of thelignin-carbohydrate matrix (Kumar et al., 2009a). Consequently, steam pre-treatment can be improved by using an acid catalyst, such as H2SO4 or SO2

(1–2% w/w), which increases the recovery of hemicelluloses sugars (Galbeand Zacchi, 2007). SO2 steam explosion at 190◦C for 2 min was applied towheat straw and spruce: solubilization of hemicelluloses was observed at,respectively, 46% and 85% (Li and Chen, 2007).

4.2.3 AFEX (AMMONIA FIBER EXPLOSION)

AFEX is a physicochemical pretreatment in which the biomass is exposed toliquid ammonia at a relatively high temperature (90–120◦C) for a period of30 min, followed by the suddently reduction of pressure. AFEX pretreatmentreduces lignin content, increases surface area, and cellulose and hemicellu-loses are well preserved, showing little or no degradation (Moniruzzamanet al., 1997). AFEX was shown to be insufficiently effective for substrates withhigh lignin content such as aspen in the form of chips or wood (McMillan,1994).

For example, Gupta and Lee (2010) applied AFEX to switchgrass and ob-served 68%, 45%, and 1% of solubilization of lignin, hemicelluloses, and cel-lulose, respectively. On the other hand, Kumar and Wyman (2009) observedno solubilization (of lignin, hemicelluloses, or cellulose) after treatment ofpoplar. However, the crystallinity index of corn stover was significantly re-duced (from 50.3 to 36.3) whereas the crystallinity index of poplar did notchange.

4.2.4 CO2 EXPLOSION

In CO2 explosion, the biomass is exposed to CO2 at low temperatures(30–50◦C) and high pressure (140–180 bar) for a short period of time, fol-lowed by a sudden drop in pressure. CO2 explosion is similar to steamexplosion and AFEX: carbon dioxide molecules are comparable in size tothose of water and ammonia and are able to penetrate small pores accessibleto water and ammonia molecules. With the explosive release of carbon diox-ide pressure, disruption of the cellulosic structure increases the accessiblesurface area (Zheng et al., 1998). Moreover, an increase in pressure facili-tates the faster penetration of carbon dioxide molecules into the crystallinestructures and more glucose is produced in further biological hydrolyzateof biomass. Once dissolved in water, carbon dioxide forms carbonic acid.Even though it is a weak acid, it should be helpful in hydrolyzing hemi-celluloses as well as cellulose (Zheng et al., 1998). CO2 explosion is morecost-effective than steam explosion because the temperature required in theprocess is lower. It was also shown to be more cost-effective than ammoniaexplosion (Zheng et al., 1998). A further advantage of using CO2 explosion

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and AFEX rather than steam explosion is that they both avoid xylose de-composition that produces furfural, an inhibitor of the biological processinvolved in bioethanol production (Dale and Moreira, 1982).

4.2.5 WET OXIDATION

Wet oxidation pretreatment involves the treatment of the biomass with airor oxygen at temperatures above 120◦C. It was presented in the early 1980sas an alternative to steam explosion. This process is an effective method forseparating the cellulosic fraction from lignin and hemicelluloses. The hemi-celluloses are cleaved to monomeric sugars, lignins undergo both cleavageand oxidation and cellulose is partly degraded (Saha, 2003; Schultz et al.,1984). Wet oxidation at 195◦C for 15 min led to the solubilization of 95%of hemicelluloses and 40–50% of lignin of sugarcane bagasse (Martin et al.,2007). Alkaline wet oxidation at 185◦C for 5 min on the same substrate sol-ubilized only 30% of hemicelluloses and 20% of lignin (Martin et al., 2007).The combination of wet oxidation with alkaline pretreatment permitted thereduction of temperature in the process and, consequently, avoided the for-mation of soluble compounds such as furfural (Ahring et al., 1996; Martinet al., 2007).

4.3 Chemical Pretreatment4.3.1 ACID PRETREATMENT

Acid pretreatment is used for efficiently removing hemicelluloses by breakingether bonds in lignin/phenolics-carbohydrates complexes without dissolvinglignin (Knappert et al., 1981).

Concentrated acids (typically 72% H2SO4 or 42% HCl at low tempera-ture) usually lead to the conversion of at least 90% of the potential glucan inthe biomass into glucose (Xiao and Clarkson, 1997). However, concentratedacids are corrosive and toxic and to make the process economically feasible,need to be recovered after pretreatment (Sun and Cheng, 2002). Conse-quently, dilute acid pretreatment appears to be a more promising processand has been widely studied. Concentrations of 0.4–2% H2SO4 at temper-atures between 160 and 220◦C for a few minutes are typically employed(Willfor et al., 2005). Dilute sulfuric acid treatment has been used success-fully to hydrolyze hemicelluloses to sugars with high yields, to change thestructure of the lignin and to increase the cellulosic surface area (Mosieret al., 2005; Wyman et al., 2005).

Sulfuric acid is the most widely used but other acids have been used,including hydrochloric, phosphoric, nitric and acetic acid associated at timeswith nitric acid (Xiao and Clarkson, 1997). Peracetic acid, which is also anoxidant (oxidation potential: 1.81 eV), was shown to lead to a drastic reduc-tion in the crystallinity index; this was attributed to structural swelling and

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dissolution of the crystalline cellulose component (Gharpuray et al., 1983).The disadvantages of acid pretreatment are that it implies a corrosive reagent,with corresponding downstream neutralization, and special materials for re-actor construction.

4.3.2 ALKALINE PRETREATMENT

Alkaline pretretament is used mainly for the cleavage of ester bonds inlignin/phenolics-carbohydrates complexes (Buranov and Mazza, 2008). Itleads to the saponification of esters of the uronic bonds between hemicel-luloses and lignin, swells the fibers and increases pore size, facilitating thediffusion of the hydrolytic enzymes (Datta, 1981).

Aqueous lime or soda pretreatment was shown to be effective at a lowertemperature than that used in acid treatment but the time required is of theorder of hours or days rather than the minutes or seconds needed for acidpretreatment. For example, the degradation of lignin, the cleavage of linksbetween lignin and carbohydrates, the solubilization of lignin (14%) andthe increase in the accessibility of holocelluloses were observed after limepretreatment was applied to wheat straw at 85◦C for 3 hr (Chang et al., 1998).The destruction of the ester bond in LCCs was observed during the NaOHpretreatment of rice straw. Pretreatment of miscanthus with 12% NaOH at70◦C for 4 hr led to 77% of delignification of the raw material and to 44%hydrolysis of hemicelluloses (de Vrije et al., 2002).

Ammonia can also be used in the ammonia recycle percolation (ARP)pretreatment. Aqueous ammonia passes through the biomass in a percolationreactor (packed-bed, flow-through type) at high temperatures (150–170◦C).Under these conditions, ammonia reacts with lignin and not with cellulose.ARP is effective for the delignification of hardwood and agricultural residuesbut less effective for softwood (Mosier et al., 2005). For example, in cornstover, ARP removed 75–85% of the total lignin and solubilized 50–60% ofhemicelluloses, but retained more than 92% of the cellulose content (Kim andLee, 2005). In the case of herbaceous biomass, Iyer et al. (1996) observed60–80% delignification of a mixture of corn cobs and stover and 65–85%delignification of switchgrass. Moreover, a pretreatment of switchgrass with15% NH3 at 120◦C was shown to be efficient in LCC solubilization whereasLCC were not solubilized by a 5% NaOH pretreatment at 85◦C (Gupta andLee, 2010).

4.3.3 OXIDATIVE PRETREATMENT

Oxidative pretreatment (H2O2, O3, FeCl3) can also be used to solubilize ligninand hemicelluloses and to increase the surface area of cellulose.

Hydrogen peroxide is usually used in association with alkali (pH = 11.5;Rabelo et al., 2008). For example, 50% lignin and most of the hemicelluloseswere solubilized by 2% H2O2 at pH = 11.5 and 30◦C for 8 hr on sugarcanebagasse (Azzam, 1989). By applying 1% H2O2 at pH = 11.5 and 65◦C for 3 hr

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on corn stover, 66% delignification was observed compared with untreatedcorn stover (Selig et al., 2009). Gupta and Le (2010) assessed the impactof alkali pretreatment of switchgrass with 5% H2O2. Whereas 5% NaOH at85◦C and 15% NH3 at 120◦C led to comparable levels of lignin and hemicel-luloses removal from solid fractions, the use of ammonia led to significantdegradation of xylan, galactan, arabinan and mannan originating from hemi-celluloses. A 5% H2O2, 5% NaOH, 85◦C pretreatment was also shown to beeffective in LCC solubilization.

Ozone can be applied to degrade lignin, though hemicelluloses isslightly affected and cellulose not at all (Kumar et al., 2009a). For example,a reduction in lignin content from 29% to 8% was observed after ozonolysispretreatment of poplar sawdust (Vidal and Molinier, 1988). Ben-Ghedalia andMiron (1981) showed 60% removal of lignin by applying ozone pretreatmentto wheat straw. Although the process is carried out at room temperature andnormal pressure, this pretreatment requires a large amount of ozone, makingthe process expensive.

Inorganic salts (NaCl, KCl, FeCl3) have also been tested as catalysts forthe degradation of hemicelluloses in corn stover. FeCl3 pretreatment was themost effective on corn stover, removing almost all the hemicelluloses; thispretreatment can disrupt almost all the ether linkages and some ester link-ages between lignin and carbohydrates but had no effect on delignification.FeCl3 significantly increased the degradation of hemicelluloses in aqueoussolutions heated to between 140–200◦C, with 90% xylose solubilization andonly 10% cellulose removal (Liu et al., 2009a; Liu et al., 2009b).

4.3.4 ORGANOSOLV PRETREATMENT

In the organosolv process, an organic or aqueous organic solvent mixturewith inorganic acid catalysts is used to break the internal lignin and hemicel-luloses bonds. The solvents generally used are methanol, ethanol, acetone,ethylene glycol, triethylene glycol, and tetrahydrofurfuryl alcohol; the acidsused are HCl or H2SO4 (Kumar et al., 2009a). For most organosolv processesat high temperatures (185–210◦C), there is no need for the addition of acidbecause organic acids released from the biomass at this temperature act ascatalysts for the breakdown of the LCC (Duff and Murray, 1996). Most hemi-celluloses and lignin are solubilized, but the cellulose remains solid, makingthis process competitive for the bioethanol process (Zhao et al., 2009). Dur-ing the organosolv process with poplar using aqueous ethanol; the recoveryof lignin and hemicelluloses were 74% and 72%, respectively. (Pan et al.,2006). In the case of an ethylene glycol pretreatment of wheat straw, sol-ubilization was observed at a level of 95% for hemicelluloses and 64% fordelignification (Gharpuray et al., 1983). However, at the end of organosolvpretreatment, the solvents used in the process must be removed from thereactor because they may inhibit the growth of microorganisms and theyneed to be recycled in order to reduce costs (Kumar et al., 2009a).

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4.3.5 IONIC LIQUIDS

Ionic liquids have also been investigated as an aid to dissolving lignocellu-losic biomass (Dadi et al., 2007; Nguyen et al., 2010; Samayam and Schall,2010). Ionic liquids offer several advantages: they have minimal environmen-tal impact due to their low volatility and can be reused after pretreatment(Dadi et al., 2007). Ionic liquid pretreatment of lignocellulosic biomass pro-duces amorphous cellulose with little residual crystallinity (Samayam andSchall, 2010). Poplar and switchgrass were pretreated with (Emin)OAc (1-ethyl 3-methyl imidazolium acetate) for 30 min at 120◦C. For poplar andswitchgrass, the crystallinity dropped from 38% to 8% (wt%) and from 21% to6%, respectively (Samayam and Schall, 2010). Besides reducing crystallinity,ionic liquids can efficiently remove lignin. Wood flour was pretreated with(Emin)OAc for 90 min at temperatures ranging from 50 to 130◦C. At 110◦C,44% of the lignin was removed and the crystallinity reduced from 63% to 30%(Lee et al., 2009). At the present time, however, this process is too expensivefor application as a lignocellulosic pretreatment due, mainly, to the high costof ionic liquids (Nguyen et al., 2010).

4.4 Biological Pretreatment

During biological pretreatment, industrial enzymes such as cellulase and xy-lanase or lignolytic enzymes (laccase, lignin, and manganese peroxidase) areused to break down all components of lignocelluloses, including lignin, thepolymer most refractory to microbial attack (Lopez et al., 2007). These en-zymes can also be produced by microorganisms such as brown-, white-,and soft-rot fungi that secrete extracellular enzymes (Galbe and Zacchi,2007). White-rot fungi are the most effective in the biological pretreatmentof lignocellulosic biomass (Fan et al., 1982). Lignin degradation by white-rot fungi occurs through the action of lignin-degrading enzymes such asperoxidases (lignin peroxidase, manganese peroxidase, versatile peroxidase,and laccase; Lee et al., 2007). To oxidize lignin, laccases, with low redoxpotential, need the presence of small compounds forming stable radicalsthat act as redox mediators. A mediating role is also played by the Mn3+ ionformed during the manganese peroxidase and versatile peroxidase oxidationof Mn2+ (which acts as an oxidizer of phenolic structures and a starter of lipidperoxidation reactions), as well as by some aromatic radicals required forlignin peroxidase oxidation of lignin, while versatile peroxidase can oxidizelignin directly (Martinez et al., 2009).

For example, white-rot fungi (Ceriporiopsis subvermispora and Cyathusstercoreus) were found effective in delignification of bermuda grass: afterincubation with Ceriporiopsis subvermispora and Cyathus stercoreus, about23% and 41% of total aromatics were removed respectively (Akin et al.,1995). Lopez et al. (2007) used Coniochaet ligniaria fungus to pretreat pep-per plant residues. This microorganism produced cellulase, xylanase, and

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two lignolytic enzymes (manganese peroxidase and lignin peroxidase). After20 days of culture, reductions of about 75%, 50%, and 40% were obtainedfor hemicelluloses, cellulose, and lignin, respectively.

The various types of biological pretreatment are considered environ-mentally friendly and energy-saving as they are performed at low temper-ature and do not need any chemicals. However, biological pretreatment,because of its very low treatment rates, must be combined with other kindsof pretreatment (Sun and Cheng, 2002).

4.5 General Remarks

Table 2 showsthe results of the main types of pretreatment on the solubi-lization of cellulose, hemicelluloses and lignin and on the crystallinity index,the surface area and digestibility of some selected biomass. Wheat straw isone of the most widely studied substrates. Measurements revealed high di-gestibility using (Emim)OAc ionic liquid (92%; Fu et al., 2010), organosolvprocess (85%; Sun and Chen, 2008), and SO2 steam explosion (up to 70%;Piccolo et al., 2010). Where gramineae were involved, a high level of solubi-lization of hemicelluloses was obtained by organosolv (Demirbas, 1998; Sunand Chen, 2008), wet oxidation (Bjerre et al., 1996), SO2 steam explosion(Piccolo et al., 2010), and dilute acid (Kumar et al., 2009b). A high levelof solubilization of lignin was obtained with peracetic acid pretreatment,organosolv (Demirbas, 1998; Gharpuray et al., 1983; Sun and Chen, 2008),and ARP for corn stover (Kumar et al., 2009b). A significant decrease in thecrystallinity index was observed after milling, peracetic acid pretreatment,and pretreatment involving ammonia (Gharpuray et al., 1983; Kumar et al.,2009b; Kumar and Wyman, 2009). However, several studies have shown anincrease in the crystallinity index after ammonia treatment of wheat straw andafter low-pH treatment of poplar (Kumar et al., 2009b; Kumar and Wyman,2009; Remond et al., 2010). These results were explained by the greaterbreakdown of amorphous cellulose in comparison to crystalline cellulose.

Where woody plants are concerned, the same trends are observed ex-cept for AFEX and ARP, which are more effective on gramineae, notably indecreasing the crystallinity index (Kumar et al., 2009b). Also noteworthy isthat (Emim)OAc ionic liquid is highly effective in reducing the crystallinityindex and that a high level of solubilization of hemicelluloses and lignin isobtained by pretreatment involving soda.

General trends for the effects of pretreatment on the lignocellulosicstructure are summarized in Table 3. The majority of these studies werecarried out with a view to bioethanol production. Thus the objective ofpretreatment was to remove or dissolve hemicelluloses and lignin from thecellulose, which has to be retained in the solid fraction of the biomass.However, hemicelluloses solubilization is a key feature in the bioethanol

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Dilu

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ross

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al.,

2009

)O

rgan

oso

lv:1.

2%H

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2009

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281

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TA

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(Bje

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team

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sion

190◦

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2009

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2009

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sion

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——

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um

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——

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iet

al.,

2009

)

282

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Org

anoso

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sion

200◦ C

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al.,

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a with

outpre

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conditi

ons.

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TABLE 3. General trends for the effects of pretreatment on lignocellulosic structure andcharacteristics and its impact on biohydrogen/biomethane and bioethanol processes

Impact on Impact on Results ifCH4/H2 bioethanol conditions

production production Achieved by too severe

Mechanical treatmentIrradiationLiquid hot waterSteam explosionCO2 explosion

Increase of surface area + + AcidAlkaliAFEXOxidationOrganosolvLignolytic enzymes

Ionic liquidsReduction of cellulose

cristallinity + + Mechanical treatmentAFEXOxidation

AlkaliAFEX

Alteration of ligninstructure (Cleavage oflignin-carbohydratecomplex)

Oxidation+ + CO2 explosion

Lignolytic enzymesRot fungiAcid

AcidLiquid hot waterSteam explosion

Solubilisation ofhemicelluloses

+ + CO2 explosion oxidation O3Oxidation FeCl3OrganosolvXylanase

Acid/thermal MechanicaltreatmentSolubilisation of cellulose + −∗

Ionic liquid Acid/thermal

AFEXalkalioxidation O3

Solubilisation of lignin + + OrganosolvIonic liquidLignolytic enzymesRot fungi

Formation of furfural/HMF No/low impactfor methane

—Acid/thermal

Not clear forhydrogen

OrganosolvLiquid hot water

Mineralisation of hexoses — — oxidation

Mineralisation of pentoses — No impact oxidation

+: positive impact, -: negative impact.∗Effect of pretreatment before enzymatic hydrolysis of cellulose.

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process though it is not indispensible to improve anaerobic digestion inso-far as hemicelluloses can be converted into biomethane. But solubilizationof hemicelluloses and cellulose are expected to improve anaerobic diges-tion rates. The shared aims of pretreatment for improving ethanol produc-tion and anaerobic digestion are the alteration of lignin structure (i.e., LCCcleavage and lignin solubilization) and an increase in the surface area, bothof which should improve the extent and the rate of anaerobic digestion.Reduction of cellulose crystallinity, which is important for bioethanol pro-duction, may also impact on anaerobic digestion rates, though to a lesserextent.

When pretreatment conditions are too severe, especially in the case ofthermal pretreatment at high temperature (LHW, steam explosion) and ther-mochemical pretreatment that requires high temperatures (acid or organo-solv), by-products such as furfural, hydroxymethylfurfural, and soluble lignincompounds can be formed (Palmqvist and Hahn-Hagerdal, 2000). Such com-pounds become a problem during the fermentation stage of bioethanol pro-duction because they inhibit, or even stop, fermentation (Laser et al., 2002).In contrast to the bioethanol process, anaerobic digestion can convert thesecompounds. However, the methanogen microorganisms require a period ofadaptation that decreases the hydrogen or methane production rate (Ben-jamin et al., 1984; Fox et al., 2003). Furthermore, the overly severe conditionsof some forms of pretreatment such as oxidation may lead to the partialdegradation or mineralization of sugars. Whereas in bioethanol production itis the degradation of glucose that must be avoided, in any pretreatment foranaerobic digestion degradation of sugars originating from either celluloseor hemicelluloses should be avoided because this results in the partial lossof biohydrogen or biomethane potential.

5. CONVERSION OF LIGNOCELLULOSIC MATERIALS TO BIOH2

AND BIOCH4 IN ONE- AND TWO-STAGE PROCESSES

Hydrogen (H2) and methane (CH4) are both valuable energy sources thatcan be used for the production of heat and electricity or as vehicle fuel.Hydrogen is regarded as an ideal type of renewable energy for the futurebecause it can be converted either to electrical energy in fuel cells or burntand converted to mechanical energy without producing CO2 (Momirlan andVeziroglu, 2005). Over the past 10 years, several studies have focused on theproduction of biohydrogen and biomethane using lignocellulosic residueswhich constitute a sustainable source thanks to their abundance and lowcost (de Vrije et al., 2002; Koullas et al., 1992; Mosier et al., 2005; Pana-giotopoulos et al., 2009). Methane can be produced from organic matterby a biological process known as anaerobic digestion while biohydrogencan be obtained by dark fermentation as a part of an anaerobic process.

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FIGURE 4. Principle of the conversion of lignocellulosic biomass to biohydrogen andbiomethane (Color figure available online).

Indeed, the dark fermentation process is defined as an intermediate stagealong the anaerobic digestion pathway when the last step (methanogene-sis) does not occur or is inhibited (Figure 4). One of the major advantagesof dark fermentation and anaerobic digestion processes is that all the or-ganic compounds can be transformed into biofuel except lignin, contraryto only simple sugars for bioethanol and lipids for biodiesel (Frigon et al.,2008; Xiao et al., 2010). Consequently, hydrogen or methane productionin a one-stage process or combined hydrogen and methane productionin a two-stage process appears to be very promising (Pakarinen et al.,2009).

5.1 Dark Fermentation5.1.1 PRINCIPLES

Biohydrogen can be biologically produced by bacterial fermentation (darkfermentation and photo-fermentation) or by a photosynthetic process car-ried out by microalgae (direct or indirect biophotolysis). One of the advan-tages in the use of the fermentation process rather photo-fermentation isthat it performs concomitantly waste treatment and H2 production (Sarataleet al., 2008). In addition, dark fermention requires less space and is around

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340 times cheaper than photosynthetic production because anaerobic fer-mentative bacteria produce hydrogen without photoenergy (Atif et al.,2005).

Dark H2 fermentation is a simple process that requires low energy andcan use various kinds of organic waste (Wang et al., 2008). Monosaccharides(i.e., glucose, xylose, arabinose) and also polymers such as starch, cellulose,or hemicelluloses can be used as hydrogen feedstocks. There are two com-mon pathways in the production of hydrogen by dark H2 fermentation: oneproducing acetate and the second butyrate. These acidification processesare described by the following reactions (Equations 1–4), using glucose andxylose as models.

The theoretical metabolic pathways of acetic acid (Equation 1) andbutyric acid (Equation 2) from glucose are the following (Antonopoulouet al., 2006):

C6H12O6 + H2O → 2CH3COOH + 2CO2 + 4H2 (1)

C6H12O6 → CH3CH2CH2COOH + 2CO2 + 2H2 (2)

The theoretical metabolic pathways of acetic acid (Equation 3) andbutyric acid (Equation 4) from xylose are the following (Kongjan et al.,2009):

C5H10O5 + 1.67H2O → 1.67CH3COOH + 1.67CO2 + 3.33H2 (3)

C5H10O5 → 0.83CH3CH2CH2COOH + 1.67CO2 + 1.67H2 (4)

Theoretically, using pure cultures, 4 mol of hydrogen can be producedfrom glucose by the acetate pathway and 2 mol by the butyrate pathway,3.33 mol of hydrogen can be produced from xylose by the acetate pathway,and 1.67 mol by the butyrate pathway (Antonopoulou et al., 2006; Kongjanet al., 2009). Therefore, the butyrate/acetate ratio might be a quantitativeindicator of substrate metabolism such that more hydrogen production isto be expected if more acetate and less butyrate are found in the system(Hawkes et al., 2007).

Of the heterotrophic bacteria that can be used for dark H2 fermentation,anaerobic (Clostridium), or facultative (Enterobacter and Bacillus) bacteriaare the most efficient microorganisms. They can be found in pure, mixed,or cocultures. Pure cultures of selected hydrogen species that include strictanaerobes (Clostridia, rumen bacteria, archaea) or facultative anaerobes(E. coli, Enterobacter, Citrobacter) are often used to produce hydrogen(Ntaikou et al., 2010). Among the hydrogen-producing bacteria, Clostrid-ium sp., and Enterobacter sp. are the most widely studied bacterial species.

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Hydrogen production is about 2 mol H2/mol glucose by Clostridium sp. com-pared with 1 mol H2/mol glucose by Enterobacter sp. (Girbal et al., 1995;Yokoi et al., 1995). Hydrogen production using Clostridium thermocellum onlignocellulosic substrates was investigated by Levin et al. (2006). A hydrogenyield of 1.6 mol H2/mol glucose was observed from wood fibers (Levin et al.,2006). Thermophilic biohydrogen production from energy crops by Caldicel-lulosiruptor saccharolyticus was also studied by Ivanova et al. (2009). Wheatstraw was found to be the best, with a H2 production capacity of 2.09 molH2/kgDM (Ivanova et al., 2009). Cocultures can be a promising alternative(Yokoi et al., 2001). Wang et al. (2008) investigated biohydrogen produc-tion from microcrystalline cellulose using Clostridium acetobutylicum in acomparison with cocultures (Clostridium acetobutylicum and Ethanoigenensharbinense). A hydrogen yield of 3.6 mmol H2/g cellulose was observedusing the pure culture and 8.1 mmol H2/g cellulose using the coculture.Ethanoigenens harbinense rapidly removed the reduced sugars producedby Clostridium acetobutylicum through cellulose hydrolysis, resulting inimproved cellulose hydrolysis and subsequent hydrogen production rates(Wang et al., 2008). However, pure cultures need to be isolated and re-quire aseptic conditions, which significantly increases the overall cost of theprocess (Ntaikou et al., 2010).

Most studies have used mixed cultures originating from natural envi-ronments such as soils and anaerobic sludge to produce hydrogen (Ntaikouet al., 2010). Mixed cultures are easier to use because they are simpler tooperate and a large range of feedstock can be transformed (Li and Chen,2007). Moreover, unlike pure cultures they do not require aseptic condi-tions (Ntaikou et al., 2010). However, the use of mixed cultures has thedisadvantage that non-hydrogen-producing species such as methanogens,homoacetogens, and lactic acid bacteria are present, leading to either thegeneration of by-products such as propionate, ethanol, and lactate that in-volve the consumption of hydrogen; or to no hydrogen production (Guoet al., 2010a; Ntaikou et al., 2010). Methanogens that are considered as themain hydrogen-consuming microorganisms can be inhibited by using pre-treatment such as heat shock and pH control. Heat-shock treatment methodsutilize the capacity of some acidogenesic bacteria (Bacillus and Clostridium)to sporulate at high temperatures. In general, a heat-shock treatment of 110◦Cfor 15 min to 2 hr is applied to eradicate non-spore-forming microorganisms(e.g., methanogenic archaebacteria) and to select spores of acidogenic bac-teria that germinate when conditions become favorable again (Argun et al.,2008; Fang et al., 2006; Lay et al., 2003). Similarly, an acid/base pretreatmentis an alternative to heat pretreatment. It consists in maintaining the seedmicroorganisms in acidic or basic conditions over a prolonged period toeradicate the methanogens that cannot survive in conditions of extreme pH(Ntaikou et al., 2010). Chemical inhibitiors such as bromoethanesulfonate,acetylene, and chloroform can also be used (Guo et al., 2010a).

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5.1.2 DARK FERMENTATION OF LIGNOCELLULOSIC BIOMASS

While carbohydrates and proteins are both basic components of organic ma-terials, in terms of hydrogen yield during dark fermentation, carbohydratesare known to be a better substrate than proteins (Bai et al., 2004). The maxi-mum hydrogen yields are about 6.25 mmol H2/g glucose and 3.43 mmol H2/gprotein at initial neutral pH (Xiao et al., 2010). However, proteins content canimprove the cell growth of hydrogen-producing bacteria and consequentlyincrease hydrogen productivity (Brosseau et al., 1986). By way of example,substrates containing 60% glucose and 40% peptone were tested and pro-vided better conditions for cell growth and biohydrogen production than asubstrate containing only glucose (Bai et al., 2004). Consequently, lignocel-lulosic materials that contain holocelluloses (hemicelluloses and cellulose)represent interesting substrates for hydrogen production, as has been shownin extensive reviews of biohydrogen production involving a large range ofsubstrates (Demirel et al., 2010; Guo et al., 2010a).

Some studies using lignocellulosic feedstocks to produce biohydrogenare mentioned in Table 4. For lignocellulosic biomasses, Table 4 reportsvalues ranging from 3.16 L H2/kgVS (corn stalk) to 73 L H2/kgVS (ryegrass).Better results for hydrogen potential were observed for starchy substratessuch as fodder turnip and maize starch, 188 L H2/kgDM and 190L H2/kgDM,respectively.

5.2 Anaerobic Digestion5.2.1 PRINCIPLES

Anaerobic digestion of lignocellulosic residues consists of a complex se-ries of metabolic interactions involving different anaerobic microorganismsin an oxygen-free environment. Anaerobic digestion is made up of fourmain steps: hydrolysis, acidogenesis, acetogenesis, and methanogenesis (Fig-ure 4). Each stage requires the activity of its own specific group of microor-ganisms. Hydrolysis is the conversion of carbohydrates into soluble sugarmonomers (glucose, xylose, arabinose, mannose). Acidogenesis is the trans-formation of soluble sugar monomers into volatile fatty acids (VFA). Thesetwo first steps correspond to dark H2 fermentation during which the activ-ity of hydrogen-consuming bacteria is not inhibited. During acetogenesis,VFA are transformed into acetate, CO2, and H2. Homoacetogenesis is of par-ticular interest since it produces acetate from the mixture CO2/H2. Finally,methanogenesis is the conversion of acetate, CO2, and H2 to methane byarchae bacteria. The mixture CO2/H2 is transformed into methane by hy-drogenophilic methanogens while acetate is transformed into methane byacetoclastic methanogens. Thus, the final product of anaerobic digestion isbiogas, which consists mainly of methane (55–75%) and CO2 (25–45%). Asanaerobic digestion is a biological process, it is strongly influenced by the

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TA

BLE

4.

Bio

H2

and

Bio

CH

4pro

duct

ion

inone-

and

two-s

tage

pro

cess

es

Hyd

roge

nyi

eld

Met

han

eyi

eld

Ener

gyyi

eld

Bio

Ener

gySu

bst

rate

s(L

H2/k

gV

Sadded

)(L

CH

4/k

gV

Sadded

)(M

J/kg

VS

added

)aRef

eren

ces

Corn

stal

k3.

160.

03(Z

han

get

al.,

2006

)Corn

-cob

13.1

0.14

(Pan

etal

.,20

09)

Popla

rle

aves

150.

16(C

uiet

al.,

2010

)M

aize

leav

es17

0.14

(Iva

nova

etal

.,20

09)

Swee

tso

rghum

30.5

0.33

(Iva

nova

etal

.,20

09)

Whea

tst

raw

460.

50(I

vanova

etal

.,20

09)

Whea

tbra

n51

0.55

(Pan

etal

.,20

08)

Bio

H2

Swee

tso

rghum

stal

k52

.10.

56(S

hiet

al.,

2010

)Fo

dder

mai

ze61

c0.

66(K

yazz

eet

al.,

2008

)Rye

gras

s73

c0.

79(K

yazz

eet

al.,

2008

)B

eer

resi

dues

3.11

b0.

034b

(Cuiet

al.,

2009

)Sw

eetso

rghum

59b

0.63

b(N

taik

ou

etal

.,20

07)

Whea

tflour

60b

0.65

b(H

awke

set

al.,

2008

)Fo

dder

turn

ip18

8b2.

02b

(Rec

hte

nbac

h&

Steg

man

n,20

09)

Mai

zest

arch

190b

2.05

b(R

echte

nbac

h&

Steg

man

n,20

09)

Coco

nutfiber

s66

2.63

(Kiv

aisi

&Elia

pen

da,

1994

)N

ewsp

rint

973.

86(X

iao

&Cla

rkso

n,19

97)

Corn

stove

r11

44.

54(Z

hen

get

al.)

Switc

hgr

ass

125

4.97

(Guio

tet

al.,

2009

)W

hea

tgr

ass

160

6.37

(Rom

ano

etal

.,20

09)

Sisa

lfibre

180

7.16

(Msh

andet

eet

al.,

2006

)Ric

est

raw

190

7.56

(Zhan

g&

Zhan

g,19

99)

Corn

sila

ge19

47.

72(F

rigo

net

al.,

2008

)W

illow

200

7.96

(Uel

lendah

let

al.,

2008

)M

isca

nth

us

200

7.96

(Uel

lendah

let

al.,

2008

)

290

Dow

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ded

by [

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] at

19:

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Pap

ertu

be

resi

dues

222

8.83

(Teg

ham

mar

etal

.,20

09)

Ric

est

raw

224

8.91

(Ghosh

&B

hat

tach

aryy

a,19

99)

Bar

ley

stra

w22

99.

11(D

inucc

ioet

al.,

2010

)B

ioC

H4

Gra

sshay

230

9.15

(Leh

tom

akiet

al.,

2004

)B

agas

se23

79.

43(K

ivai

si&

Elia

pen

da,

1994

)W

hea

tst

raw

276

10.9

8(B

auer

etal

.,20

09)

Whea

tst

raw

297

11.8

2(K

apar

aju

etal

.,20

09)

Suga

rbee

tto

ps

310

12.3

3(L

ehto

mak

iet

al.,

2004

)Red

ban

ana

pee

l32

212

.81

(Gunas

eela

n,20

03)

Pota

toes

328

13.0

5(F

rigo

net

al.,

2008

)Pota

topulp

332

13.2

1(K

ryvo

ruch

koet

al.,

2008

)W

inte

rry

e33

613

.37

(Pet

erss

on

etal

.,20

07)

Offi

cepap

er36

414

.48

(Xia

o&

Cla

rkso

n,19

97)

Mai

zesi

llage

370

14.7

2(B

runiet

al.,

2010

)Corn

kern

els

397b

15.8

b(F

rigo

net

al.,

2008

)Su

mm

ersw

itchgr

ass

403

16.0

4(F

rigo

net

al.,

2008

)G

rass

silla

ge43

117

.15

(Pak

arin

enet

al.,

2009

)Citr

us

pee

ls45

518

.10

(Gunas

eela

n,20

03)

Pota

toes

200.

413

07.

33(X

ieet

al.,

2007

)B

ioH

2+

Gra

sssi

llage

5.6

467

18.3

6(P

akar

inen

etal

.,20

09)

Bio

CH

4Sw

eetso

rghum

10.4

b,c

107b

,c4.

36b,c

(Anto

nopoulo

uet

al.,

2006

)M

aize

108b

426b

18.1

1b(R

echte

nbac

h&

Steg

man

n,20

09)

a Ener

gyyi

eld

1Nm

3CH

4=

3979

0kJ

;1N

m3

H2

=10

780

kJ.

bL

CH

4/k

gD

Mad

ded

or

LH

2/k

gD

Mad

ded

or

MJ/

kgD

Mad

ded

.c a

dap

ted

from

the

liter

ature

.

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following environmental factors: temperature, pH, and toxic compounds.Anaerobic digestion is divided into psychrophilic (10–20◦C), mesophilic(20–40◦C), or thermophilic (50–60◦C) digestion processes. The first stage inanaerobic digestion can occur at a wide range of pH, whereas methanogenicmicroorganisms are efficient only at neutral pH (6.5–7.5).

5.2.2 ANAEROBIC DIGESTION OF LIGNOCELLULOSIC BIOMASS

The advantage to using anaerobic digestion is that not only simple organiccompounds such as pentoses, hexoses, and volatile fatty acids are convertedinto methane but also polymers (cellulose, starch, hemicelluloses). Eveninhibiting compounds from bioethanol fermentation (furfural, HMF, and sol-uble lignin) can be transformed into methane if not highly concentrated(Benjamin et al., 1984; Fox et al., 2003).

Based on the stoechiometric conversion of organic material intomethane and carbon dioxide, the theoretical or maximum methane yield(100% conversion) can be calculated from the elemental composition of thesubstrate CaHbOcNdSe as follows (Frigon and Guiot, 2010; Lubken et al.,2010):

Y TheoreticalC H4

(L /gsubstrate) = 22.4(4a + b − 2c − 3d − 2e

)

8(12a + b + 16c + 14d + 16e

) (5)

According to Equation 5, the theoretical methane yields of carbohy-drates (C10H18O9) and lignocellulosic biomass (C5H9O2.5NS0.025) are 397 LCH4/kgVS and 475 L CH4/kgVS, respectively (Frigon and Guiot, 2010). Basedon measured elemental analysis, Lubken et al. (2010) calculated the theoreti-cal methane yields of various form of lignocellulosic biomass. Results rangedfrom 394 L CH4/kgVS for triticale straw to 490 L CH4/kgVS for rye grass. How-ever, actual methane yields from lignocellulosic biomass can be far lowerthan the theoretical amounts. According to Frigon and Guiot, they do notgenerally exceed 60% of theoretical values due to poorly or nonbiodegrad-able compounds (e.g., lignin, peptidoglycan) and polymers that are difficultto dissolve (cellulose, hemicelluloses, and proteins).

Several extensive reviews of methane production from biomass havebeen published (Frigon and Guiot, 2010; Gunaseelan, 1997; Ward et al.,2008). Some results are presented in Table 4 where values range from 25 LCH4/kgVS (barley straw) to 455 L CH4/kgVS (citrus peel).

It is generally accepted that the higher the crude fiber content, thelower the methane potential of the biomass. This has been confirmed onthree types of paper (newsprint, paper tube residues, and office paper) withdifferent lignin content (30.3%, 23%, and 3.6% respectively), which had amethane potential of 97 L CH4/kgVS added, 222 L CH4/kgVS added, and 364 LCH4/kgVS added, respectively (Teghammar et al., 2009; Xiao et al., 2010). Ac-cording to Kobayashi et al. (2004), a linear regression shows a strong negative

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correlation between the amount of methane produced and the amount ofKlason lignin in bamboo. The lignin content plays a major role in methaneproduction by limiting the access to holocelluloses. Holocelluloses, whichare anaerobically biodegradable compounds in their pure form, appear tobe less biodegradable or even completely refractory when combined withlignin (Jimenez et al., 1990; Tong et al., 1990). Furthermore, Buffiere et al.(2006) showed a link between the methane potential of various lignocellu-losic residues and the sum of their cellulose and lignin content: the higherthe sum of cellulose and lignin, the lower the methane potential (Buffiereet al., 2006). As pure cellulose can be fully converted into biogas, previ-ous results showed that the anaerobic digestion of lignocellulosic biomass isstrongly conditioned by the bioaccessibility of cellulose. However, Klimiuket al. (2010) found that the methane yields of two varieties of micanthushaving comparable lignin concentrations varied by a factor of 2: 100 and190 m3 CH4/kgVS for Miscanthus × giganteus and Miscanthus Sacchariflor-ous, respectively (Klimiuk et al., 2010). Lignin concentration is thus a keyparameter in anaerobic biodegradation, though not the only one.

Various studies have considered the anaerobic digestion of biomasssillage. Ensiling, the natural degradation of organic matter by aerobic lacticbacteria, favours nutrient conservation. Lehtomaki (2006) has shown thatensiling has a positive impact on methane production. He suggested thatthe structural polysaccharides contained in plant material, which are quiteresistant to anaerobic degradation, can be partially degraded by aerobiclactic bacteria during storage (Lehtomaki, 2006). High methane potentialwas observed in sillage such as maize and grass, with methane productionof 370 ml CH4/gVS and 431 ml CH4/gVS, respectively (Bruni et al., 2010;Pakarinen et al., 2009). A 25% increase in methane potential was observedfor maize after four months ensiling. Ensiling can thus be considered as anatural pretreatment (Neureiter et al., 2005).

5.2.3 COMPARISON OF ENERGY PRODUCTION BY ANAEROBIC DIGESTION

WITH COMBUSTION AND BIOETHANOL PRODUCTION

In terms of energy potential (MJ/kgDM), it is interesting to compare methaneproduction from lignocellulosic waste with other energy sources such ascombustion and bioethanol (Table 5). Calorific values that represent potentialenergy produced by combustion were directly taken from Voivontas et al.(2001) and McKendry (2002). Energy potential from bioethanol and methaneproduction were calculated on the basis of yields of 23 200 kJ/L bioethanol and39 790 kJ/Nm3

CH4.Because various energy potentials are considered from different studies,

Table 5 does not provide a comparison of different routes for profitableuse of the same substrate. Knowing that methane or ethanol potentials canvary significantly depending on several factors such as the plant species

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TABLE 5. Comparison of the different profitable uses of energy of lignocellulosic substrates

Lignocellulosicsubstrates

Energy potentialfrom bioethanol

(MJ/kgDM)

Energy potentialfrom methane

(MJ/kgDM)

Calorific valuecombustion(MJ/kgDM)

Wheat straw 6.7(Kim and Dale, 2004)

10.2(Bauer et al., 2009)

17.9(Voivontas et al., 2001)

Barley straw 7.2(Kim and Dale, 2004)

8.6(Dinuccio et al., 2010)


Rice straw 6.5(Kim and Dale, 2004)

7.9(Ghosh &

Bhattacharyya, 1999)


Rye straw — 12.3(Petersson et al., 2007)


Sugarcanebagasse

6.5(Kim and Dale, 2004)

8.8(Kivaisi & Eliapenda,

1994)

19.4(McKendry, 2002)

Miscanthus — 7.64(Uellendahl et al., 2008)


Switchgrass 6.5(Guiot et al., 2009)

5–15(Frigon et al., 2008)


Willow — 7.64(Uellendahl et al., 2008)

20(McKendry, 2002)

Poplar — 11.93a

(Chynoweth et al., 1993)18.5

(McKendry, 2002)

aMJ/kgvs.

and maturity, values for energy potential are considered as rough estimates.Even so, methane production seems to lead to higher energy production thanbioethanol, whatever the biomass. But energy production by combustion isfar higher than by ethanol and methane conversion. These results can beexplained by the high proportion of lignin that can be burnt during heatingbut not converted during bioethanol and biomethane production processes.Even so, apart from the amount of energy produced, the use of energy has tobe considered: in fact biofuel and electricity are considered as more flexibleenergy sources than heat.

5.3 Coupling BioH2 and BioCH4 Two-Stage Processes

Only about 10–20% of the energy potential of an organic substrate is obtainedthrough dark fermentation (Cooney et al., 2007). Dark fermentation residuescontain VFA (mainly acetic and butyric acids) and other compounds, whichwill not be degraded to H2 due to thermodynamic restrictions (Hawkes et al.,2007). There are several routes for using such residues in a second stage,these include converting the by-products to H2 using photosynthetic bacteriaor converting VFA to CH4 during an anaerobic process (Ren et al., 2009).

In the second stage, acetate and butyrate derived from soluble metabo-lites of the dark fermentation can be converted into hydrogen by photo-synthetic bacteria, known for their dominant tendency to convert organic

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acids to hydrogen in the presence of light, and by the action of the nitro-genase enzyme (Claassen et al., 2004). The combination of dark and photofermentation can achieve a theoretical maximum hydrogen yield of 12 molH2/mol hexose. This kind of two-stage bioprocess has been investigated us-ing lignocellulosic substrates such as potato steam peel and cassava starch(Claassen et al., 2004; Su et al., 2009). By a combination of dark and photofermentation, the maximum hydrogen yield from cassava starch increased to18 mmoles H2/g starch from the original 10.7 mmoles H2/g starch in darkfermentation only (Su et al., 2009). However, one of the major drawbacks ofthis process is its costs because photo-heterotrophic bacteria employ light astheir primary energy source and organic compounds as the carbon source(Claassen et al., 2004).

Another promising route is the use of a two-stage H2-CH4 process whichhas shown greatly enhanced hydrolysis and higher energy yields comparedto a one-stage methanogenic process (Hawkes et al., 2007). In the first stage,the operating conditions (acid pH and short retention time) are set to fa-vor fermentation of the substrate to hydrogen by enhancing the growthof acidogenic bacteria. In the second stage, conditions are changed to suitmethanogenesis (neutral pH and longer retention time). This kind of processpresents several advantages because the first stage acts efficiently for solubi-lization and the combined hydrogen-methane mixture (20–30% H2, 80–70%CH4) has been shown to burn cleaner than methane alone (Bauer and Forest,2001; Ueno et al., 2007).

Some studies have been carried out using a two-stage H2 and CH4

process (Table 4). Pakarinen et al. (2009) compared mesophilic CH4 produc-tion from grass sillage in a one-stage process to combined thermophilic H2

and mesophilic CH4 production in a two-stage process. As well as a hydro-gen production of 5.6 ml H2/gVS, an 8% increase in CH4 yields was obtainedfrom grass sillage in the two-stage process compared with the one-stage pro-cess (467 ml CH4/gVS vs. 431 ml CH4/gVS; Pakarinen et al., 2009). In termsof energy, an increase of 7% in MJ/kgVS was observed with the two-stageprocess, in which only 0.4% came from hydrogen production. This highermethane yield in the two-stage process was attributed to the fact that thethermophilic H2 production stage enhanced hydrolysis of the solid substratesand resulted in increased solubilization and VFA production (Pakarinen et al.,2009).

A two-stage process was also applied to potatoes and maize: hydrogenproduction of 271 ml H2/gVS and 158 ml H2/gDM, respectively, was observed,the methane production being 130 ml CH4/gVS and 426 ml CH4/gDM, respec-tively (Rechtenbach and Stegmann, 2009; Xie et al., 2007). Finally, this kind ofprocess was also studied by Antonopoulou et al. (2006) using sweet sorghum(hydrolysate and solid fraction). The two-stage H2-CH4 process was appliedto the hydrolyzed part that was rich in readily fermentable sugars whereasthe one-stage CH4 process was only applied to the solid fraction. Yields of

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10.4 ml H2/gDM and 29 ml CH4/gDM were achieved for the hydrolyzate and 78ml CH4/gDM for the solid fraction. A two-stage process can increase methaneproduction; however, the increase in the CH4 yield has to be considered inthe light of the investment required in the more complex two-stage process(Pakarinen et al., 2009).

6. PRETREATMENT FOR ENHANCING HYDROGENAND METHANE PRODUCTION

Pretreatment of lignocellulosic substrates prior to biohydrogen or bio-methane production favors the accessibility of holocelluloses to anaerobicmicroorganisms. Several kinds of pretreatment were used to enhance theproduction of bioH2 and bioCH4. The main results for bioH2 and bioCH4

potentials and the gain of energy (MJ/kgVS) attributable to pretreatment arepresented in Table 6.

6.1 Mechanical Pretreatment

Mechanical pretreatment, in particular grinding, has been used to enhanceanaerobic digestion. Grinding (0.5 mm) led to a 53% enhancement of theenergy yield from wheat straw (Sharma et al., 1988). The influence of particlesize reduction on different types of organic solid waste was investigated. Itwas observed that such size reduction of a substrate led to an increase inmethane production (≈20%) and a reduction in anaerobic digestion time(≈20%), particularly with substrates having a high fiber content such ashay and leaves (Palmowski and Muller, 2000). According to Palmowski andMuller (2000), comminution not only releases cell compounds usable moreeasily and rapidly but also supports hydrolysis of the solid compounds inthe long term.

6.2 Thermal Pretreatment

Of the kinds of thermal pretreatment used to enhance hydrogen and methaneproduction, steam explosion has been one of the most widely investigated.This pretreatment removes lignin and improves the accessibility of holocel-luloses (Kobayashi et al., 2004). When steam explosion at 180◦C for 25 minwas applied to wheat straw, methane production increased by 31% (Baueret al., 2009). Teghammar et al. (2009) combined chemical pretreatment withsteam explosion. They observed that the combination of steam explosionwith 2% NaOH and 2% H2O2 enhanced the methane yield of paper tuberesidues from 238 ml CH4/gVS to 493 ml CH4/gVS (Teghammar et al., 2009).Steam explosion has also been investigated for hydrogen production withcorn straw, cornstalks and wheat bran, giving hydrogen production of 68 ml

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TA

BLE

6.

Effec

tofpre

trea

tmen

ton

bio

H2

and

bio

CH

4pro

duct

ion

Pre

trea

tmen

tm

ethod

Pro

cess

esLi

gnoce

llulo

sic

mat

eria

lsPre

trea

tmen

tco

nditi

ons

Bio

H2

pro

duct

ion

(LH

2/k

g VSa

dded

)

Bio

CH

4

pro

duct

ion

(LCH

4/k

g VSa

dded

)

Ener

gyfrom

pre

trea

ted

bio

mas

s(M

J/kg

VSa

dded

)

Ener

gyfrom

raw

bio

mas

s(M

J/kg

VSa

dded

)Ener

gyga

in(%

)Ref

eren

ces

Whea

tst

raw

0.4

mm

248

9.87

6.45

53(S

har

ma

etal

.,19

88)

Ber

muda

gras

s0.

4m

m22

89.

075.

4566

(Shar

ma

etal

.,19

88)

Phys

ical

Grindin

gG

rass

5m

m32

012

.73

——

(Kap

araj

uet

al.,

2009

)Si

salfibre

2m

m22

08.

757.

1622

(Msh

andet

eet

al.,

2006

)M

aize

silla

ge2-

8m

m41

016

.31

14.7

211

(Bru

niet

al.,

2010

)

Corn

stra

w1.

5M

Pa,

10m

in,

+ce

llula

se(2

5FP

U/g

)

68b

0.73

b—

—(L

i&

Chen

,20

07)

Whea

tbra

n0.

27M

Pa,

60m

in,0.

01M

HCl

860.

930.

5569

(Pan

etal

.,20

08)

Bam

boo

5m

in/2

43◦ C

215

8.55

——

(Kobay

ashiet

al.,

2004

)St

eam

explo

sion

Pota

topulp

15m

in/1

07◦ C

373

14.8

413

.21

12(K

ryvo

ruch

koet

al.,

2008

)W

hea

tst

raw

10m

in/1

70◦ C

361

14.3

610

.98

31(B

auer

etal

.,20

09)

Ther

mo-

chem

ical

Pap

ertu

be

resi

dues

10m

in/2

20◦ C

/4%

H2O

2(w

/w)

+4%

NaO

H(w

/w)

493

19.6

28.

8312

2(T

egham

mar

etal

.,20

09)

Corn

stal

ks5

min

/1.6

MPa

63.7

b11

4.6b

5.25

b—

—(L

uet

al.,

2009

)

Mis

canth

us

—36

014

.32

7.96

80(U

elle

ndah

let

al.,

2008

)W

etoxi

dat

ion

Will

ow

—36

014

.32

7.96

80(U

elle

ndah

let

al.,

2008

)W

inte

rry

e2g

/LN

a 2CO

3/1

95◦ C

/15

min

/12

bar

O2

447

17.7

913

.37

33(P

eter

sson

etal

.,20

07)

(Con

tin

ued

onn

ext

page

)

297

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TA

BLE

6.

Effec

tofpre

trea

tmen

ton

bio

H2

and

bio

CH

4pro

duct

ion

(Con

tin

ued

)

Pre

trea

tmen

tm

ethod

Pro

cess

esLi

gnoce

llulo

sic

mat

eria

lsPre

trea

tmen

tco

nditi

ons

Bio

H2

pro

duct

ion

(LH

2/k

g VSa

dded

)

Bio

CH

4

pro

duct

ion

(LCH

4/k

g VSa

dded

)

Ener

gyfrom

pre

trea

ted

bio

mas

s(M

J/kg

VSa

dded

)

Ener

gyfrom

raw

bio

mas

s(M

J/kg

VSa

dded

)Ener

gyga

in(%

)Ref

eren

ces

Whea

tflour

2%H

2O

2(w

/v),

4h,60

◦ C31

b26

4b10

.84b

——

(Haw

kes

etal

.,20

08)

Oxi

dat

ive

Pap

ertu

be

resi

dues

4%H

2O

2

(w/w

)/19

0◦C/3

0m

in

233

9.27

8.83

5(T

egham

mar

etal

.,20

09)

Corn

stal

ks0.

5%N

aOH

570.

620.

0319

66(Z

han

get

al.,

2006

)B

agas

se4%

NaO

H(w

/v),

100◦

C,2h

+Cel

lula

se,20

FPU

/g

300

3.23

——

(Chai

rattan

a-m

anoko

rnet

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page

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299

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TA

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300

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H2/gDM, 63.7 ml H2/gDM and 86 ml H2/gVS, respectively (Li and Chen, 2007;Lu et al., 2009; Pan et al., 2008).

6.3 Thermochemical Pretreatment

Thermochemical pretreatment has also been studied with a view to enhanc-ing hydrogen and methane production. Dilute acid pretreatment has beenmost widely investigated in relation to bioH2 production. The main reasonfor using dilute acid treatment in hydrogen production is the effect of suchpretreatment on the lignocellulosic structure: hydrolysis of hemicelluloses tosugars with high yields, a change in the structure of the lignin, and an in-crease in the cellulosic surface area (Mosier et al., 2005; Wyman et al., 2005).This enhances hydrogen production, which remains very slow or inhibitedwhen hemicelluloses and cellulose are not transformed into monomer sug-ars. A great increase in hydrogen production, varying from 58% (wheat bran)to 5300% (cornstalk) was observed for lignocellulosic substrates subjected toa dilute acid (HCl) pretreatment (Pan et al., 2008; Zhang et al., 2006).

Types of alkaline pretreatment that delignify the lignocellulosic sub-strates and thus favor their degradation by anaerobic microorganisms havebeen widely studied for the enhancement of bioH2 and above all bioCH4

production. The application of a NaOH pretreatment to coconut fibers andcorn stover led to big methane production increases of 50% and 89%, re-spectively (Kivaisi and Eliapenda, 1994; Zheng et al., 2009).

6.4 Biological Pretreatment

Finally, biomethane production can be enhanced by using biological pre-treatment involving microorganisms (e.g., brown-, white-, and soft-rot fungi)or enzymes (cellulases, xylanases, lignin peroxidase, manganese peroxidase;Ghosh and Bhattacharyya, 1999; Lehtomaki et al., 2004). Ghost et al. (1999)studied the effect of white-rot fungi and brown-rot fungi on rice straw. In-creases in methane of 32% and 46%, respectively, were observed for ricestraw pretreated with brown- and white-rot fungi compared with untreatedstraw (Ghosh and Bhattacharyya, 1999). The use of enzymes to increasemethane yield has also been studied (Guiot et al., 2009; Lehtomaki et al.,2004). Lehtomaki et al. (2004) applied enzymatic pretreatment to grass at35◦C for 24 hr using two xylanases (GC 320 and Multifect) and two cel-lulases (IndiAge MAX L and Primafast 200). A slight increase, from 230 mlCH4/gVS to 271 ml CH4/gVS, was observed (Lehtomaki et al., 2004). Finally,Chairattanamanokorn et al. (2009) investigated a combination of alkalineand enzymatic pretreatment. By applying 4% NaOH (w/v) at 100◦C for 2hr followed by the enzymatic pretreatment (cellulase, 20U/g), a hydrogenyield of 300 ml H2/gVS was observed versus 31.4 ml H2/gVS for the enzymaticpretreatment alone (Chairattanamanokorn et al., 2009).

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6.5 General Remarks

Table 6 also shows the potential energy that can be recovered from pre-treated and raw substrates by biohydrogen and/or biomethane production.If paper tube residues are excluded, as they do not actually belong to classiclignocellulosic biomass, the maximum amount of recovered energy was ob-tained from grass sillage, winter rye, and maize sillage (ranging from 16 to19 MJ/kgVS) after their respective pretreatment by soda, wet oxidation, andgrinding (Bruni et al., 2010; Pakarinen et al., 2009; Petersson et al., 2007).These values approach the calorific value of straw from different types ofbiomass (ranging from 17 to 18 MJ/kgVS, Table 5). Moreover, it is worthnoting that when applied to sillage pretreatment does not lead to a verysignificant increase in the amount of energy recovered (2.8% and 11% inthe case of grass sillage and maize sillage, respectively). In fact, sillage canbe considered as a biological pretreatment and it would be interesting toconsider its impact on biomass features.

On the other hand, in biohydrogen production from substrates whichinitially had a very low hydrogen potential (corn stalks: 0.03 MJ/kgVS, beerlees: 0.03 MJ/kgVS, corn cobs: 0.14 MJ/kgVS, poplar leaves: 0.16 MJ/kgDM,and maize leaves: 0.18 MJ/kgVS), massive gains were observed, from 200to 5,300 times the initial value (Cui et al., 2010; Cui et al., 2009; Ivanovaet al., 2009; Pan et al., 2009; Zhang et al., 2006). Among these examples, thegreatest enhancement was obtained after acid (Cui et al., 2009; Pan et al.,2009; Zhang et al., 2006) or alkali pretreatment (Zhang et al., 2006). More-over, biological (Bacillus amyloliquefaciens) and enzymatic (viscozyme L)pretreatments were shown to be advantageous on maize and poplar leaves,with 333-fold and 206-fold increases, respectively (Cui et al., 2010; Ivanovaet al., 2009).

A very few studies investigated pretreatment prior to two-stage H2-CH4

processes (Hawkes et al., 2008; Lu et al., 2009; Pakarinen et al., 2009; Xieet al., 2007). Among them, some studies concerned very low lignin-contentsubstrates such as potatoes (Xie et al., 2007) or wheat flour industry co-products (Hawkes et al., 2008). Lu et al. (2009) studied steam explosion ofcornstalks prior to two-stage process but they did not indiquate bioH2 andbioCH4 production from the untreated substrate. Only one study comparedthe two-stage bioH2 and bioCH4 production with and without pretreatment(4% NaOH, 20◦C, 24 hr; Pakarinen et al., 2009). A 16% increase in bioH2

production but no significant increase in bioCH4 production was observed(Pakarinen et al., 2009). This poor result on bioCH4 production may be ex-plained by the methane yield increase by solubilization during the first H2

stage, as mentioned previously. On the other hand, this study was carriedout with grass sillage and, as mentioned previously, sillage can be consid-ered as a biological pretreatment and may have lowered the impact of thealkali pretreatment. If the impact of lignocellulosic biomass pretreatment on

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two-stage bioH2 production can be deduced from the results on one-stagebioH2 process, the impact on bioCH4 production is thus still not clear andneeds further studies.

Kaparaju et al. (2009) tested an original three-stage process on wheatstraw, producing bioethanol, biohydrogen, and biomethane. Initially, wheatstraw was hydrothermally pretreated, giving a cellulose-rich solid fractionand a hemicellulose-rich liquid fraction (hydrolysate). After enzymatic hy-drolysis of the solid fraction, an ethanol yield of 0.41 g ethanol/g sugars wasobserved and a biohydrogen yield of 178 ml H2/g sugars from the liquid frac-tion. The effluents from both the bioethanol and biohydrogen processes werefurther used to produce methane, with yields of 324 and 381 ml/gVS added,respectively (Kaparaju et al., 2009).

As well as increasing biodegradability and, thus, biohydrogen andmethane production, pretreatment is effective in increasing the hydrolysisrate of lignocellulosic biomass. For example, Fernandes et al. (2009) havemeasured the first-order hydrolysis rate constant of anaerobic digestion ofhay pretreated with 4% ammonium (w/v). No significant increase in methanepotential was observed but the hydrolysis rate increased from 0.088 to 0.409d−1 (Fernandes et al., 2009).

To sum up, pretreatment can be effective in increasing biodegradabilityand, thus, the biohydrogen and biomethane potential. Pretreatment can bean advantage where it reduces the hydrolysis time. Solid retention time canbe lowered in the digester, making for a higher organic load and a conse-quent increase in methane production in a given digestor. Acid pretreatmenthas been shown to be advantageous for hydrogen production whereas ther-mochemical (steam explosion, wet oxidation) and alkaline pretreatments arebetter for methane production. Over and above its performance-enhancingfunction, pretreatment must be considered for its environmental impact andits cost-effectiveness.

7. CONCLUSION

The profitable use of lignocellulosic biomass via anaerobic digestion or darkfermentation is of great interest for the production of renewable energy. Themain advantage of these two processes compared to bioethanol or biodieselproduction is that they use consortia of microorganisms that accept a largerange of substrates (cellulose, hemicelluloses, lipids, proteins). Moreover,biohydrogen and biomethane production can be combined in a two-stageprocess in which biohydrogen is produced in a first reactor by H2 darkfermentation and methane is produced in a second reactor using the sol-uble metabolites of dark H2 fermentation. The major advantage of using atwo-stage process is an enhancement of solubilization during dark H2 fer-mentation and, consequently, an increase in the methane yield as well asthe production of hydrogen.

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Due to the poor accessibility of biodegradable compounds, pretreatmentcan enhance the performance of the anaerobic digestion or dark fermentationof lignocellulosic materials. However, the complex structure and composi-tion of biomass must be thoroughly understood in order to first decide onand then carry out effective pretreatment. All types of biomass pretreatmentshare common denominator: they must make more accessible biodegrad-able material as well as being cost-effective and environmentally friendly.However, pretreatment must also be adapted to subsequent biological pro-cesses. For example, lignin and hemicelluloses have to be removed fromcellulose for ethanol fermentation whereas delignification is the objectiveof anaerobic digestion or dark fermentation pretreatment. Further progressmay come from a combination of a more highly refined characterization oflignocellulosic materials and the optimization of their pretreatment.

ACKNOWLEDGMENTS

The authors are grateful to ADEME, the French Environment and EnergyManagement Agency, for financial support in the form of F. Monlau’s PhDgrant.

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Lignocellulosic Materials Into Biohydrogen and Biomethane: Impact of Structural Features and...

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