REVIEW Open Access Theoretical constraints of physical and … · 2017. 8. 24. · with seawater in...

Nakamura and Takai Progress in Earth and Planetary Science 2014, 1:5http://www.progearthplanetsci.com/content/1/1/5

REVIEW Open Access

Theoretical constraints of physical and chemicalproperties of hydrothermal fluids on variations inchemolithotrophic microbial communities inseafloor hydrothermal systemsKentaro Nakamura1,2* and Ken Takai1,3

Abstract

In the past few decades, chemosynthetic ecosystems at deep-sea hydrothermal vents have received attention asplausible analogues to the early ecosystems of Earth, as well as to extraterrestrial ecosystems. These ecosystems aresustained by chemical energy obtained from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) inhydrothermal fluids and ambient seawater. The chemical and isotope compositions of the hydrothermal fluid are, inturn, controlled by subseafloor physical and chemical processes, including fluid–rock interactions, phase separationand partitioning of fluids, and precipitation of minerals. We hypothesized that specific physicochemical principlesdescribe the linkages among the living ecosystems, hydrothermal fluids, and geological background in deep-seahydrothermal systems. We estimated the metabolic energy potentially available for productivity by chemolithotrophicmicroorganisms at various hydrothermal vent fields. We used a geochemical model based on hydrothermal fluidchemistry data compiled from 89 globally distributed hydrothermal vent sites. The model estimates were compared tothe observed variability in extant microbial communities in seafloor hydrothermal environments. Our calculations clearlyshow that representative chemolithotrophic metabolisms (e.g., thiotrophic, hydrogenotrophic, and methanotrophic)respond differently to geological and geochemical variations in the hydrothermal systems. Nearly all of the deep-seahydrothermal systems provide abundant energy for organisms with aerobic thiotrophic metabolisms; observedvariations in the H2S concentrations among the hydrothermal fluids had little effect on the energetics of thiotrophicmetabolism. Thus, these organisms form the base of the chemosynthetic microbial community in global deep-seahydrothermal environments. In contrast, variations in H2 concentrations in hydrothermal fluids significantly impactorganisms with aerobic and anaerobic hydrogenotrophic metabolisms. Particularly in H2-rich ultramafic rock-hostedhydrothermal systems, anaerobic and aerobic hydrogenotrophy is more energetically significant than thiotrophy. TheCH4 concentration also has a considerable impact on organisms with aerobic and anaerobic methanotrophicmetabolisms, particularly in sediment-associated hydrothermal systems. Recently clarified patterns and functions ofexisting microbial communities and their metabolisms are generally consistent with the results of our thermodynamicmodeling of the hydrothermal mixing zones. These relationships provide important directions for future researchaddressing the origin and early evolution of life on Earth as well as for the search for extraterrestrial life.

Keywords: Deep-sea hydrothermal systems; Chemosynthetic ecosystems; Hydrothermal fluid chemistry; Host rockgeochemistry; Geochemical modeling; Bioavailable energy yield

* Correspondence: [email protected] Ecosystem Laboratory (PEL), Japan Agency for Marine-EarthScience and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka,Kanagawa 237-0061, Japan2Current address: Department of Systems Innovation, School of Engineering,The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8656, JapanFull list of author information is available at the end of the article

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Nakamura and Takai Progress in Earth and Planetary Science 2014, 1:5 Page 2 of 24http://www.progearthplanetsci.com/content/1/1/5

ReviewIntroductionDeep-sea hydrothermal vents host some of the mostdiverse microbial communities on Earth (Takai andNakamura 2011). Since the first discovery of blacksmoker vents inhabited by dense and unique chemosyn-thetic macrofaunal communities (Spiess et al. 1980),submarine hydrothermal systems and their associatedbiota have attracted great interest (e.g., Humphris et al.1995; Van Dover 2000; Wilcock et al. 2004). Unlike mostbiological communities, in which photosynthetic organ-isms are the base of the food web, deep-sea hydrothermalvent ecosystems are dependent on primary production bysymbiotic and free-living chemolithoautotrophic microor-ganisms that obtain energy from inorganic redox sub-stances (e.g., H2S, CO2, H2, CH4, and O2) in hydrothermalfluids and ambient seawater (Karl, 1995; Kelley et al.2002). Because of the unique features of deep-sea hydro-thermal vent ecosystems, they are considered plausible an-alogues to the early ecosystems of Earth and also toextraterrestrial life on other planets and moons (e.g.,Jannasch and Mottl 1985; Nealson et al. 2005; Takai et al.2006a).To date, more than 300 high-temperature hydrother-

mal vent systems have been identified at mid-oceanridges (MOR), island arcs, and back-arc spreading cen-ters (Hannington et al. 2011). Deep-sea hydrothermalfluids vary greatly in their chemical compositions due tosubseafloor physical and chemical processes such asfluid-rock interactions, magmatic volatile inputs, andphase separation of hydrothermal fluids (Von Damm1995; Butterfield et al. 2003; German and Von Damm2004; Tivey 2007). Compositional variations in hydro-thermal fluids (particularly energy and carbon sources)in turn affect biomass production and the diversity ofhydrothermal vent-endemic communities. Consequently,clarifying the relationships among the geological back-ground of hydrothermal environments, physical andchemical variations in hydrothermal fluids, and the com-positional and functional diversity of chemosyntheticecosystems has provided important information on thediversification and development of extant deep-seahydrothermal ecosystems as well as the generation andsustenance of early ecosystems and possible extraterres-trial life forms.In deep-sea hydrothermal vents, rapid mixing between

hot reduced hydrothermal fluids and cold oxidized sea-water provides chemical energy for microbial activityand biomass production. To quantify the in situ energet-ics of chemolithotrophic microorganisms in hydrother-mal mixing environments, a thermodynamic model wasfirst proposed and applied to a basalt-hosted hydrothermalsystem at 21° N on the East Pacific Rise (EPR) (McCollomand Shock 1997). Using batch-mixing models modified

from this original model, thermodynamic calculationshave been conducted for several hydrothermal vent sys-tems at MOR and arc-backarc (ABA) hydrothermal sys-tems (Shock and Holland 2004; Tivey 2004; McCollom2007; Amend et al. 2011). These studies have demon-strated differing patterns in the potential energy yields ofvarious in situ metabolic reactions in the mixing zones ofthese habitats, providing the theoretical basis for relation-ships between hydrothermal fluid chemistry and thediversity of hydrothermal vent-endemic biological com-munities. However, the hydrothermal systems studiedwere quite limited. In addition, the structures and func-tions of extant chemosynthetic biological communities,which have been characterized in many previous investi-gations, have not yet been integrated into development ofthese theoretical relationships.Many studies have identified high compositional and

functional diversity of chemosynthetic ecosystems ingeographically and geologically diverse hydrothermalsystems (e.g., in reviews by Huber and Holden 2008;Nakagawa and Takai 2008; Takai et al. 2006b). Some ofthese studies have noted possible relationships betweenthe metabolic abundances and compositions of hydro-thermal vent-endemic microbial communities and thechemical characteristics of hydrothermal vent fluids indeep-sea hydrothermal systems (Perner et al. 2007, 2010;Reysenbach and Shock 2002; Takai and Horikoshi 1999;Takai et al. 2001, 2004a). However, most of these studieswere qualitative and focused mainly on the genetic andphylogenetic diversity of microbial communities andtheir constituents. Thus, the relationships between theabundance and composition of chemolithotrophic mi-crobial communities and the geological and geochemicalenvironments of global deep-sea hydrothermal systemsremain unclear.Takai and Nakamura (2010, 2011) first provided clear

evidence of biogeochemical relationships among micro-biological community development, the chemical com-position of hydrothermal fluids, and the geologicalenvironment of deep-sea hydrothermal systems throughboth thermodynamic calculations of the potential energyyields of various in situ metabolic reactions and ob-served compositional and functional diversity of chemo-synthetic ecosystems in the mixing zones of thesehabitats. However, examples of hydrothermal systemsfor this comparison were still scarce; thus, only micro-bial populations in chimney habitats adjacent to high-temperature hydrothermal fluids were characterized byquantitative cultivation techniques and included. In thepresent study, we conducted a more comprehensiveevaluation of the relationships among variations in geol-ogy, geochemistry, and microbial metabolisms and thediversity of communities in global deep-sea hydrother-mal environments, based on compilation of a substantial


hydrothermal fluid chemistry data set and microbialcommunities in the mixing zones of a wide variety ofhabitats.

MethodsWe compiled end-member fluid chemistry data for 89hydrothermal vent sites (Additional file 1). Hydrother-mal vent sites were included only if the data set con-tained complete chemical composition data essential forthe thermodynamic calculations performed in this study,including H2, H2S, CH4, CO2, Na, Cl, Ca, K, Fe, Mn, andSi. In addition, the data set included representative geo-logical settings such as MOR hydrothermal systems inthe Pacific, Atlantic, and Indian Oceans; ABA hydrother-mal systems in the western Pacific region; and thesediment-associated (SED) hydrothermal systems in theeastern Pacific and Okinawa Trough (Figure 1).The amount of metabolic energy available for produc-

tion by chemolithotrophic microorganisms was evalu-ated as in Takai and Nakamura (2010, 2011). Fouraerobic and anaerobic reactions were considered repre-sentative of chemolithotrophic energy metabolisms(Table 1). To simulate mixing of hydrothermal fluidswith seawater in a seafloor hydrothermal system, weemployed a thermodynamic reaction path model, follow-ing McCollom and Shock (1997), Shock and Holland

60°S60°S60°S

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60°W60°W60°W 30°W30°W30°W 0°0°0° 30°E30°E30°E 60°E60°E60°E 90°E90°E90°E 111

TAGTAGTAGSnakePitSnakePitSnakePit

LogatchevLogatchevLogatchev

Menez GwenMenez GwenMenez GwenLucky StrikeLucky StrikeLucky StrikeRainbowRainbowRainbow

Red LionComfortless CoveTurtle Pits



EdmondEdmondEdmondKaireiKaireiKairei

Figure 1 Index map showing mid-ocean ridges and subduction zonesMOR, mid-ocean ridge; SZ, subduction zone; MOR-B, basalt-hosted systema mid-ocean ridge setting; ABA-M, mafic rock-hosted system in an arc-backSED-MOR, sediment-associated system in a mid-ocean ridge setting; SED-A

(2004), and McCollom (2007). The compositions of thehydrothermal solutions in the mixing zones were calcu-lated from those of the end-member vent fluids and sea-water (Additional file 1). The model calculation beganwith 1 kg of vent fluid and continued with addition ofsuccessive increments of seawater until a seawater tovent fluid mixing ratio of 1,000:1 was reached. In themixing calculations, minerals were not allowed to pre-cipitate and all redox reactions were prohibited, whileacid-base reactions were allowed to equilibrate. Inaddition, the temperatures of the calculated mixed solu-tions were assumed to scale linearly with the tempera-tures of the end-members, ignoring conductive coolingand/or heating.The overall Gibbs free energy for the metabolic reac-

tions was calculated using the following equation:

ΔGr ¼ ΔGr˚þ RT lnQr ð1Þ

where ΔGr is the Gibbs free energy of the reaction, ΔGr°is the standard-state Gibbs free energy of the reaction, Ris the universal gas constant, T is the temperature inKelvin, and Qr is the activity quotient of the compoundsinvolved in the reaction. The Qr term takes into accountthe contribution of the fluid composition to the Gibbsfree energy of each reaction, determined based on the

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Middle ValleyMiddle ValleyMiddle Valley

Main EndeavourMain EndeavourMain Endeavour

EscanabaEscanabaEscanaba

Guaymas BasinGuaymas BasinGuaymas Basin

EPR21NEPR21NEPR21N

EPR13NEPR13NEPR13N

EPR9.50NEPR9.50NEPR9.50N

EPR17SEPR17SEPR17SEPR18SEPR18SEPR18S

Minami-enseiIheya NorthIzena



BrotherBrotherBrother

MarinerMarinerMarinerTui MalilaTui MalilaTui Malila

ABEABEABETow CamTow CamTow Cam Kilo MoanaKilo MoanaKilo Moana

PACMANUSPACMANUSPACMANUSVienna WoodsVienna WoodsVienna Woods

MORMORMOR

SZSZSZ

ABA-MABA-MABA-M

SED-MORSED-MORSED-MORSED-ABASED-ABASED-ABA

ABA-FABA-F

MOR-BMOR-BMOR-BMOR-UMOR-UMOR-U

with active hydrothermal vents used in this study. Abbreviations:in a mid-ocean ridge setting; MOR-U, ultramafic rock-hosted system inarc setting; ABA-F, felsic rock-hosted system in an arc-backarc setting;BA, sediment-associated system in an arc-backarc setting.

Table 1 Metabolic reactions for chemolithoautotrophy considered in this study

Energy metabolism Overall chemical reaction Identified (I)/cultured (C) ΔGr°2, 250 (kJ)a

Aerobic reactions

Aerobic methanotrophy CH4 + 2O2 = CO2 + 2H2O I and C −860.7

Hydrogenotrophic O2 reduction H2 + 1/2O2 = H2O I and C −264.4

Thiotrophic (H2S-oxidizing) O2 reduction H2S + 2O2 = SO42− + 2H+ I and C −758.2

Fe(II)-oxidizing O2 reduction Fe2+ + 1/4O2 + H

+ = Fe3+ + 1/2H2O I and C −52.6

Anaerobic reactions

Hydrogenotrophic methanogenesis H2 + 1/4CO2 = 1/4CH4 + 1/2H2O I and C −49.2

Hydrogenotrophic SO4 reduction H2 + 1/4SO42− + 1/2H+ = 1/4H2S + H2O I and C −74.9

Hydrogenotrophic Fe(III) reduction H2 + 2Fe3+ = 2Fe2+ + 2H+ I and C −159.2

Anoxic methanotrophy with SO4 reduction CH4 + SO42− = HCO3

− + HS− + H2O I but not yet C −30.1aStandard-state Gibbs free energy of the metabolic reactions at 2°C, 250 bar.


chemical composition of the mixed fluid estimated fromthe reaction path calculations. The energy available fromthe metabolic reactions as a function of temperature(equivalent to the mixing ratio) was calculated by multi-plying the calculated Gibbs free energy for the reactionat each temperature by the concentrations of the reac-tants in the mixed fluid. This method takes into accountthe stoichiometry of the reaction and the reactants thatare limiting, multiplied by the total amount of mixedfluid at that temperature (McCollom and Shock 1997;McCollom 2007).This calculation yields an estimate of the maximum

energy that is potentially available from the metabolicreactions per kilogram of mixed fluid. We used the aver-age ΔGr values for four temperature ranges:

Figure 2 Major elements versus Cl concentration plots for hydrothermal vent fluids. The composition of seawater is also plotted forcomparison.


(Charlou et al. 1998, 2002). This is attributed to differ-ences in the mineralogy and bulk chemistry of the rocks,resulting in a substantially different alteration reactionknown as serpentinization (Janecky and Seyfried 1986;Wetzel and Shock 2000; Allen and Seyfried 2003). H2concentrations of 12 to 16 mmol/kg (roughly 1 to 2

orders of magnitude higher than in basalt-hosted hydro-thermal fluids) due to serpentinization have been re-ported in ultramafic rock-hosted deep-sea hydrothermalvent fluids (Additional file 1) (Charlou et al. 2002; Kelleyet al. 2005). In addition, enrichment of CH4 in ultra-mafic rock-associated systems is likely associated with

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0 1000 2000 3000 4000 5000

Depth (m)

MOR-BMOR-UABA-MABA-FSED-MORSED-ABA

Tem

per

atu

re (

°C)

Figure 3 Maximum temperature conditions versus water depth forindividual vent areas. Two-phase curve for seawater (dashed line) is alsoplotted with the liquid field to the lower right of the curve and theliquid + vapor field to the upper left of the curve. The star represents thecritical point of seawater at 407°C and 298 bar. The maximum temperatureof nearly all of the vent fluids is limited by the two-phase boundary.


reduction of CO2 to CH4 under highly reducing (highH2) conditions.

ABA hydrothermal systemsAlthough significant global magma production occurs inthe MOR, the second most active volcanic area is the sub-duction zone (Fisher and Schmincke 1984; Schmincke2004), where ABA volcanic systems develop. Some arcvolcanoes are subaerial, particularly in continental arc set-tings, whereas more than 40% of volcanic arcs are oceanicisland arcs where most volcanoes are submarine (Leat andLarter 2003). In oceanic island arcs and associated back-arc basins, many deep-sea hydrothermal vent sites hostedby active submarine ABA volcanisms have been discov-ered (Ishibashi and Urabe 1995; Gamo et al. 2006). Thechemical characteristics of these ABA hydrothermal sys-tems are significantly different from those of MOR hydro-thermal systems, although they share many commonfeatures derived from the basic reactions and processes ofsubseafloor hydrothermal circulation. In particular, ABAhydrothermal fluids are characterized by large variationsin chemical composition (Ishibashi and Urabe 1995;Gamo et al. 2006). This chemical variability is primarily at-tributed to a variety of host-rock compositions (from bas-altic to rhyolitic), abundant input of volatile elementsfrom magmas (e.g., CO2 and SO2), and the variable waterdepth (shallow to deep) of the submarine volcanoes.ABA hydrothermal systems hosted by mafic rocks ex-

hibit chemical characteristics similar to those of basalt-hosted hydrothermal systems at the MOR (Figure 2). Incontrast, systems hosted by felsic rocks are generallycharacterized by lower pH, higher metal concentrations,and a variable redox state compared to mafic rock-hosted hydrothermal systems (Figure 2). In addition, be-cause of the subduction of hydrated ocean crust beneathvolcanic arcs and back-arc basins as well as the potentialinvolvement of more evolved felsic magmas, the volatilecontent (H2O, CO2, and SO2) of magmas in ABA set-tings is much higher than that in MOR settings (e.g.,Gamo et al. 1997; Embley et al. 2007). ABA hydrother-mal systems are also characterized by wide variations inwater depth, and most are significantly shallower thantypical MOR hydrothermal systems (Figure 3). This re-sults in variations in phase separation (boiling) andhydrothermal fluid temperatures in the subseafloor reac-tion zones, which significantly affect the chemical com-position of the hydrothermal fluids. The maximumtemperatures of the hydrothermal vent fluids in thecompiled data were clearly controlled by the two-phaseboundary of seawater (Figure 3).

SED hydrothermal systemsSome hydrothermal vent sites are covered with sedi-ments, which influence the chemical composition of

their hydrothermal fluids. SED hydrothermal systems arefound in both MOR (e.g., Juan de Fuca, Middle Valley,Escanaba Trough, and Guaymas Basin) and ABA (e.g.,Okinawa Trough) settings in which hydrothermal ventsites are in close proximity to continental runoff sources.Irrespective of differences in tectonic setting or host-rock composition, SED hydrothermal systems have char-acteristic chemical compositions, e.g., relatively high pH,low metal content, and high CH4 and NH3 concentra-tions (German and Von Damm 2004). There are onlyminor differences in chemical composition between SEDhydrothermal systems in MOR and ABA settings (Figure 2).Thus, the chemical features of SED hydrothermal ventfluids are more strongly affected by the sediment than bythe tectonic setting or host-rock composition.

Factors controlling hydrothermal fluid chemistryIt is believed that hydrothermal fluid flux is primarilycontrolled by the crust (magma) production rate, be-cause magmatic heat derived from creation of newoceanic crust (cooling from 1,200°C to 350°C) heatshydrothermal fluids from 2°C to 350°C (e.g., Elderfieldand Schultz 1996). Based on this, Kawahata et al. (2001)estimated that the maximum volume of high-temperaturehydrothermal fluid is twice that of the upper oceanic crust(the volcanic and sheeted dike sequence) and if 65% to85% of the rocks are altered to secondary minerals, thevolumetric water/rock ratio would be 2.3 to 3.1. Thisclearly suggests that high-temperature hydrothermal fluidsare generated under rock-dominated (low water/rockratio) conditions (Kawahata et al. 2001). Therefore, thechemical compositions of hydrothermal fluids are


predominantly controlled by water-rock reactions andfluid-mineral equilibria (Seyfried et al. 1991; Shock 1992;Seyfried and Ding 1995). Thus, host-rock geochemistry isone of the most important factors controlling hydrother-mal fluid chemistry. In addition to the chemical composi-tions of host rocks, however, other processes such asinput of volatiles from magmas, phase separation ofhydrothermal fluids, and interactions with sediment alsohave a significant impact on the observed compositions ofhydrothermal fluids.

Chemical composition of host rocksDifferences in the rock types in the reaction zone canlead to large variations in the hydrothermal fluid chem-istry, because the bulk chemical composition and pri-mary minerals in the source rock control the reactionsequences and their chemical equilibria.

Mafic rocks Most ocean basins (including MOR andABA settings) are of mafic composition (mainly basaltic).The chemical systematics of mafic rock-seawater sys-tems (particularly basalt-seawater systems) have beenwell characterized based on field observations, hydro-thermal experiments, and theoretical studies (Bischoffand Dickson 1975; Mottl and Holland 1978; Seyfriedand Mottl 1982; Mottl 1983; Reed 1983; Bowers andTaylor 1985; Seyfried 1987; Von Damm 1990, 1995;Seyfried et al. 1988, 1991; Shock 1992; Saccocia et al.1994; Wetzel and Shock 2000; Butterfield et al. 2003;Nakamura et al. 2007).Basalt-hosted hydrothermal fluids have relatively low

pH at 25°C and 1 atm (generally 3 to 4) and notable en-richment in base metals (e.g., Fe and Mn) and dissolvedgases (e.g., H2, CO2, and CH4) compared to seawater(Figure 2). The in situ pH of the basalt-hosted ventfluids are neutral to weakly acidic, significantly differentfrom the pH measured at 25°C and 1 atm in laboratoryexperiments (German and Von Damm 2004). This dis-crepancy is mainly caused by dissociation of H+-bearingaqueous complexes (e.g., HCl0) due to cooling duringsample processing (Shock et al. 1989; Seyfried et al.1991; Ding and Seyfried 1992; Ding et al. 2005). Anotherpossible mechanism of pH change is precipitation ofmetal sulfides below the seafloor, producing protons(German and Von Damm 2004).In high-temperature MOR vent fluids, most metals are

enriched by up to 7 to 8 orders of magnitude comparedto seawater. The stability of chloride complexes (e.g.,FeCl2

0) increases with increasing temperature, and there-fore, most metal ions are present in high-temperaturefluids as chloride complexes (Helgeson et al. 1981; Dingand Seyfied 1992). The substantial increase in the metalsolubility produces the high concentrations in the ventfluids.

Basalt-hosted hydrothermal fluids are also highly re-ducing, as evidenced by the presence of H2S ratherthan SO4, as well as by significant amounts of H2,CH4, Fe

2+, and Mn2+. These chemical features are gen-erally consistent with phase-equilibrium calculationsinvolving the observed primary and secondary minerals(feldspar, chlorite, epidote, quartz, magnetite, anhydrite,pyrite, and pyrrhotite) and seawater at in situ hydro-thermal fluid temperatures and pressures (Bowerset al. 1988; Seyfried et al. 1988, 1999; Saccocia andSeyfried 1990; Seyfried and Ding 1995; McCollum andShock 1998; Wetzel and Shock 2000). Time-seriesmeasurements of chemical compositions of hydrother-mal fluids in MOR regions have indicated steady-stateconcentrations of dissolved species (Campbell et al. 1988;Bowers et al. 1988; Butterfield et al. 1994; Von Damm1988, 1995, 2000), reflecting clear solubility control bymineral phases in the subseafloor reaction zones and re-charge zones.

Ultramafic rocks Compared with hydrothermal fluidsin mafic rock-hosted systems, ultramafic rock-associatedhydrothermal fluids are characterized by conspicuousenrichment in H2 in the presence or absence of phaseseparation processes (Figure 2). Production of H2 duringserpentinization of ultramafic rocks results from reac-tion of water with Fe2+-bearing minerals, primarily oliv-ine and pyroxene. In these reactions, Fe2+ is partiallyoxidized to Fe3+ by the water, resulting in precipitationof magnetite in the serpentinite. The water reduced bythe Fe2+ also produces H2. One of the important chem-ical features of ultramafic rocks that constrains abundantH2 production during serpentinization is relatively lowAl concentrations. Low Al activity results in formationof alteration minerals (particularly serpentines and bru-cite) that have a tendency to exclude Fe2+ from theirstructure. This leads to oxidation of Fe2+ by water toform magnetite. In contrast, because mafic rocks havehigher Al contents than ultramafic rocks, a muchgreater proportion of the Fe2+ is sequestered in Al-bearing alteration minerals (e.g., chlorite), limiting oxi-dation of Fe2+ to Fe3+. Thus, hydrothermal alteration ofmafic rocks generates much lower amounts of H2 andmagnetite than serpentinization of ultramafic rocks,even though the Fe content of basaltic rocks is higherthan that of ultramafic rocks. Basaltic rock-hosted ventfluids typically exhibit H2 concentrations of 10 mmol/kg H2 has frequently been re-ported for ultramafic rock-associated fluids (Additionalfile 1). The potential for even higher H2 concentrations(>100 mmol/kg) has been suggested by both petrologi-cal (Frost 1985; Alt and Shanks 1998) and experimental(Berndt et al. 1996; McCollom and Seewald 2001)studies.


In addition, ultramafic rock-associated hydrothermalfluids are often characterized by CH4 enrichment(Figure 2). Although the origin of CH4 in these fluids iscontroversial, it is generally thought to be derived fromreduction of CO2 by high concentrations of H2 throughabiotic methanogenesis (Nakamura et al. 2009). How-ever, the hydrothermal fluid CH4 concentrations are al-ways disequilibrated with the concomitant H2 and CO2concentrations, suggesting that the subseafloor hydro-thermal circulation system is an open system with re-spect to CH4 content. Enriched CH4 (>0.5 mmol/kg) hasalso been observed in hydrothermal fluids from certainbasalt-hosted systems at the MOR (Figure 2; LuckyStrike and Menez Gwen hydrothermal fields) (Additionalfile 1). Both of these fields are located in the northernMid-Atlantic Ridge, where several ultramafic rock-associated hydrothermal systems have been discovered.Based on geological and geochemical lines of evidence, ithas been suggested that the high CH4 concentrations inthese basalt-hosted hydrothermal fluids were caused byserpentinization of ultramafic rocks somewhere in thesubseafloor (Charlou et al. 2000).

Felsic rocks Hydrothermal systems hosted by felsic rockshave been identified only in ABA settings (Figure 1). Felsicrock-hosted hydrothermal fluids are characterized by rela-tively low pH and enrichment in H2S, CO2, K, Mn, and Fecompared to mafic rock-hosted fluids (Figure 2). Thechemical characteristics of felsic rock-hosted hydrother-mal fluids are generally consistent with experimental re-sults for seawater-felsic rock interactions (e.g., Hajash andChandler 1981). For example, felsic rocks contain highconcentrations of incompatible elements such as K. En-richment of K in felsic rock-hosted fluids originates fromthe bulk rock composition. In addition, the lower pH is at-tributed to the low ability of felsic rocks to consume H+ insolution. The pH of a hydrothermal solution is lowered byremoval of Mg2+ via precipitation of Mg-hydroxysulfateduring heating of the seawater (Bischoff and Seyfried1978) and by formation of Mg-bearing alteration minerals(e.g., smectite and chlorite) during seawater-rock interac-tions (Mottl 1983). In a basalt–seawater system, the H+

generated in the fluid is consumed by dissolution of Cafrom the reacted rocks (Seyfried and Mottl 1982; Mottl1983). Mg-Ca exchange reactions control the fluid pH toapproximately neutral under in situ conditions (Seyfriedand Mottl 1982; Wetzel and Shock 2000). However, be-cause felsic rocks are relatively depleted in Ca, their abilityto buffer pH changes is significantly lower than that oftheir mafic counterparts.Low pH in hydrothermal fluids promotes leaching of

heavy metals through water-rock interactions. This ul-timately results in high concentrations of heavy metals,although the initial concentrations of heavy metals in

felsic rocks are lower than those in basaltic rocks. TheFe and Mn concentrations in deep-sea hydrothermalfluids are correlated not only with Cl concentrations butalso with pH (Figure 4). Moreover, the Fe/Cl and Mn/Clratios for hydrothermal fluids exhibit strong correlationswith pH (Figure 4). This clearly shows that the concen-trations of heavy metals in deep-sea hydrothermal fluidsare mainly controlled by the pH of the hydrothermalfluids.

Inputs of magmatic volatilesEnrichment of H2S and CO2 in felsic rock-hosted hydro-thermal fluids cannot be explained only by water-rockinteractions. Instead, enrichment in these volatiles canbe caused by inputs of magmatic volatiles into hydro-thermal systems. ABA magmas (particularly those thatare felsic in composition) have very high concentrationsof volatile elements and molecules, and hydrothermalfluids that are highly enriched in sulfur and/or CO2 havebeen observed in ABA hydrothermal systems, mainlyhosted by more siliceous rocks, e.g., andesite, calcite,and rhyolite rather than by basalt (Gamo et al. 1997;Sakai et al. 1990; Inagaki et al. 2006; Lupton et al. 2006,2008). Therefore, enrichment in CO2 and H2S of felsicrock-hosted hydrothermal fluids is likely due to signifi-cant inputs of magmatic volatiles into these hydrother-mal systems.Dissolution of CO2 gas into a hydrothermal fluid re-

sults in production of H+ in the fluid via the followingreaction:

CO2 þH2O ¼ HCO3− þHþ: ð2Þ

Compared to that for SO2 (see below), the dissociationconstant of this reaction is much smaller, particularlyunder high-temperature conditions. It is therefore be-lieved that the effect of CO2 on the fluid pH is not verysignificant. However, segregation of CO2 from upwellinghydrothermal fluids in the subseafloor can result in con-sumption of H+ in the fluid, increasing the pH. Even asmall pH increase during ascent of the hydrothermalfluid can cause subseafloor precipitation of metal-sulfideminerals, resulting in low heavy metal concentrations inthe hydrothermal fluids. This process would be expectedin hydrothermal systems with significant inputs of CO2but not SO2 from magma, such as hot spot-influencedMOR hydrothermal systems and basalt-hosted arc-backarc hydrothermal systems.Volatile sulfur species in the magma have a more sig-

nificant effect on deep-sea hydrothermal systems. Thepredominant gaseous sulfur species in magma are SO2and H2S (Wallace and Edmonds, 2011). Although dissol-ution of H2S does not significantly affect hydrothermalfluid chemistry, that of SO2 into hydrothermal fluids

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Figure 4 Plots of (A) Fe, (B) Mn, (C) Fe/Cl, and (D) Mn/Cl versus pH for hydrothermal vent fluids. These plots clearly show that concentrationsof Fe and Mn in hydrothermal vent fluids are mainly controlled by pH.


increases the f O2 and sulfuric acid in the fluids via thefollowing reactions:

2SO2 þ 2H2O ¼ 2H2S0 þ 3O2 ð3Þ

2SO2 þO2 þ 2H2O ¼ 2HSO4− þ 2Hþ: ð4Þ

Once the f O2 of the hydrothermal fluid reaches thesulfate-sulfide boundary via reaction (3), sulfuric acid isproduced by reaction (4). The presence of sulfuric acidcan cause a significant decrease in pH. Because the solu-bility of heavy metals is quite sensitive to pH, the pH de-crease caused by SO2 promotes dissolution of heavymetals from the reacted rocks. Volatile inputs frommagmas occur intermittently, and even during such ac-tivity, the chemistry of hydrothermal fluids is controlledby reactions induced by both volatile inputs and water-rock interactions. Therefore, it is likely that the chemicalcomposition of the fluids, as is typical of open and dy-namic systems, significantly varies with space and time.

Nevertheless, felsic rock-hosted hydrothermal systemsaffected by magmatic volatile inputs clearly exhibit highconcentrations of base metals and low pH (Figure 4).

Phase separationAs described above, the concentrations of all compo-nents in hydrothermal fluids exhibited positive or nega-tive correlations with Cl, except for H2, CO2, and CH4in several samples affected by serpentinization of ultra-mafic rocks, CO2 inputs from magma, and CH4 inputsfrom sedimentary organic matter and/or microbial pro-cesses (Figure 2). Deep-sea hydrothermal fluids oftenreach temperatures high enough that they separate intovapor and brine phases. The phase separation tem-perature depends primarily on the pressure conditions(i.e., water depth) of the hydrothermal system. The ob-served temperatures of hydrothermal fluids from variousvent sites were clearly limited by the two-phase bound-ary of seawater (Bischoff and Pitzer 1989) (Figure 3).Phase separation and subsequent remixing of the vapor


and brine phases produce hydrothermal fluids with awide range of salinities, from 1 order of magnitude lowerto several times higher than that of seawater (Figure 2).The chemical properties of the vapor and brine phases

are quite different from each other and from their parentfluid, because each of the chemical species in the parentfluid is distributed preferentially into the vapor and li-quid phases according to their physical and chemicalproperties during phase separation (Butterfield et al.2003; Foustoukos and Seyfried 2007). The concentra-tions of gaseous species greatly increased with decreas-ing Cl concentration, indicating the strong affinity ofthese volatile components for the vapor phase (Figure 2).In contrast, the positive correlations between the Cl con-centration and other dissolved species that are primarilyionic (e.g., Na+ and Cl−) indicate the strong affinity ofthese species for the liquid phase. In addition, the rela-tionships between the Cl concentration and the ratios ofelements to chloride clearly showed a strong increase inthe ratios of gaseous species to chloride with decreasingCl concentration (Figure 5). The Si/Cl ratio also slightlyincreased with decreasing Cl concentration. This indi-cates that, in addition to gaseous species, neutral speciessuch as SiO2

0 have some affinity for the vapor phase. Onthe other hand, there was little change in the ratios ofionic species with Cl concentration as a result of phaseseparation, indicating that they all partition strictly intothe brine phase. These chemical behaviors of thedissolved species during the phase separation and parti-tioning into hydrothermal fluids result in formation oflow-Cl, vapor-dominated fluids enriched in gases and ofresidual brines enriched in ionic species and depleted ingases.

Presence of sedimentsSED hydrothermal systems have chemical compositionsdistinct from those of other hydrothermal fluids. Com-pared to those of sediment-starved MOR and ABAhydrothermal systems, SED hydrothermal fluids gener-ally have relatively high pH, lower heavy metal contents,and higher CH4 and NH4

+ concentrations (Figure 2)(German and Von Damm, 2004). The very high CH4concentrations of hydrothermal fluids in SED systemsare attributed to thermal decomposition of organic mat-ter at high temperatures during hydrothermal reactionsat discharge zones and/or microbial methanogenesis atrelatively low temperatures at sedimentary rechargezones (Lilley et al. 1993; Kawagucci et al. 2011, 2013).Likewise, the source of NH4

+ in SED hydrothermal sys-tems is considered to be thermal decomposition and mi-crobial ammonification of organic matter (Kawagucciet al. 2011, 2013). High concentrations of NH4

+ in thesehydrothermal fluids provide an NH3/NH4

+ buffer thatmaintains the relatively high pH of the fluid (German

and Von Damm, 2004). This greatly decreases the solu-bility of metal-sulfide minerals, leading to low heavymetal concentrations in the hydrothermal-vent fluids.

Effects of hydrothermal fluid chemistry on thebioavailable energy yieldThe chemosynthetic primary producers that sustaindeep-sea hydrothermal vent ecosystems utilize inorganicsubstances (e.g., H2S, CO2, H2, and CH4) derived fromhydrothermal vent fluids as energy and carbon sources.Thus, deep-sea hydrothermal vent ecosystems should beat least partially controlled by the chemical compositionof the hydrothermal fluids. The effects of hydrothermalfluid compositions on deep-sea hydrothermal vent eco-systems based on the energy yields available to variouschemolithotrophic metabolisms are described below.

Hydrogen sulfide (H2S)In all of the deep-sea hydrothermal systems in all set-tings, the potential energy yields for sulfur-oxidizingchemolithotrophy (thiotrophy) using H2S in the hydro-thermal fluids were uniformly high at >10 J/kg mixedfluid (Figure 6A). Even in ultramafic rock-associatedhydrothermal systems with relatively low H2S concentra-tions, the metabolic energy of sulfur oxidation (H2S oxi-dation) was nearly identical to that in other types ofhydrothermal systems, some of which had 2 orders ofmagnitude higher H2S concentrations (Figure 6A). Thisuniformity is attributed to the relatively high concentra-tions of H2S (mostly >1 mmol/kg) present in hydrother-mal fluids in all of the hydrothermal systems. As aresult, the amount of H2S always exceeded the O2 con-centration throughout the habitable temperature rangein the mixing zones, except at very low temperatures(several degrees Celsius). The potential energy yield ofsulfur-oxidizing chemolithotrophy is therefore solelycontrolled by the dissolved O2 concentration in the sea-water (which is globally similar in all deep-sea water).Thus, concentrations of H2S in end-member hydrother-mal fluids may not significantly affect the abundanceand composition of sulfur oxidizers.The exception is in hydrothermal plumes, where much

higher seawater mixing ratios (>1000) and low tempera-tures (up to several degrees Celsius) are found. In hydro-thermal plume environments, the concentration of H2Sin the source hydrothermal fluid, rather than theseawater-dissolved O2, becomes the limiting factor forsulfur-oxidizing chemolithotrophic metabolism.

Hydrogen (H2)In contrast to H2S, variations in the H2 concentrationdirectly affected the potential energy for the chemolitho-trophic microbial population, not only for aerobic H2 oxi-dation but also for most anaerobic energy metabolisms

Figure 5 Plots of major element to Cl ratios versus Cl for hydrothermal vent fluids.


other than anaerobic methane oxidation. This feature ispartially attributed to the wide range of H2 concentrationsin hydrothermal fluids. For example, typical basalt-hostedhydrothermal fluids had H2 concentrations of

1

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(A) H2S oxidation

(C) SO4 reduction

(B) H2 oxidation

(D) Methanogenesis

(E) Aerobic CH4oxidation

(F) Anaerobic CH4oxidation

(G) Fe2+ oxidation

MOR-BMOR-UABA-MABA-FSED-MORSED-ABA

(See figure on previous page.)Figure 6 Metabolic energy yields versus H2S, H2, CH4, and Fe2+ concentrations in hydrothermal fluids. Potential metabolic energyavailable from (A) thiotrophic (H2S-oxidizing) O2 reduction as a function of the H2S concentration in the end-member hydrothermal fluid; (B)hydrogenotrophic O2 reduction, (C) hydrogenotrophic SO4 reduction, and (D) hydrogenotrophic methanogenesis as a function of the H2 concentrationin the end-member hydrothermal fluid; (E) aerobic methanotrophy and (F) anoxic methanotrophy as a function of the CH4 concentration in theend-member hydrothermal fluid; and (G) Fe2+-oxidizing O2 reduction as a function of the Fe

2+ concentration in the end-member hydrothermal fluidare plotted for each kilogram of mixing water for four temperature ranges. The temperature ranges of 2 mmol/kg for psychrophiles)(Figure 6E).

Iron (Fe)Variation in the Fe2+ concentration of the hydrothermalfluids was also large, from the nanomole per kilogramlevel to the millimole per kilogram level (comparable tothe ranges for H2 and CH4 concentrations). This vari-ation in the Fe2+ concentration of the hydrothermalfluids could affect aerobic iron-oxidizing chemolithotro-phy. The potential energy yield from the aerobic Fe oxi-dation reaction was well correlated with the Fe2+

concentration in the hydrothermal fluid (Figure 6G).However, for highly Fe2+-enriched hydrothermal fluids(>0.2 mmol/kg for hyperthermophiles to >2 mmol/kgfor psychrophiles), the amount of available metabolic en-ergy was saturated with respect to the Fe2+ concentra-tion in the end-member hydrothermal fluid (Figure 6G).The metabolic energy yield potentially obtained fromaerobic oxidation of 1 mol of Fe2+ was several timessmaller than that from aerobic oxidation of 1 mol ofH2S, H2, or CH4 (Figure 6). This may affect the relativeabundance of aerobic Fe-oxidizer populations in deep-sea hydrothermal vent ecosystems.In contrast to aerobic Fe-oxidizing chemolithotrophy,

there was an essentially negligible energy yield predictedfor anaerobic Fe3+ reduction using H2 or CH4 for all


types of deep-sea hydrothermal fluids and systems. Thisis attributed to an extremely low concentration of Fe3+

in both seawater and hydrothermal fluids.

Effect of the geological setting of the hydrothermalsystem on the bioavailable energy yieldIn the MOR-B and all ABA settings (comprising mostdeep-sea hydrothermal systems), almost all potentiallybioavailable energy can be obtained from aerobic metab-olism (Figure 7). The end-member hydrothermal fluids inthese settings contain only small amounts of H2 and CH4(other than highly vapor-enriched hydrothermal fluids).The most energetically favorable chemolithotrophic me-tabolism was aerobic sulfur oxidation (Figure 8A). Thus,aerobic sulfur oxidizers are the chemolithoautotrophicpopulation most likely to sustain primary production inthese deep-sea hydrothermal vent ecosystems.In the MOR-B and ABA-M settings, aerobic oxidation

of H2 and CH4 were the second most available metabolicreactions, particularly at higher temperatures (lowermixing ratios). On the other hand, in the ABA-F setting,aerobic Fe2+ oxidation was the second most favorablechemolithotrophic metabolism (Figure 8A). These differ-ences are directly related to the different chemical com-positions of the end-member hydrothermal fluids (e.g.,H2, CH4, and Fe

2+ concentrations) in these settings, ul-timately derived from the oxidation state of the magmasand/or volatile (particularly SO2) inputs into the hydro-thermal fluids. Relatively little energy was predicted tobe available from anaerobic chemolithotrophic metabo-lisms for these settings, except for temporally andspatially limited habitats induced by phase separation ofhydrothermal fluids (Figure 8B).In the MOR-U and SED settings, the potential energy

from aerobic oxidation of H2 or CH4 exceeded that fromaerobic sulfur oxidation at higher temperatures (lowermixing ratios) (Figure 8A). More importantly, in thesesettings, considerable energy for primary production canbe obtained from anaerobic chemolithotrophic metabo-lisms and populations (Figure 8B). Particularly in high-temperature habitats, anaerobic chemolithotrophs areexpected to play a prominent role as primary producers(Figure 8A, B). This represents a marked difference inpotential chemolithotrophic microbial communities be-tween the MOR-U and SED settings and the more com-mon MOR-B and ABA settings.In the MOR-U setting, because of the high H2 concen-

trations in end-member fluids, both aerobic and anaer-obic H2-trophic population reducers were energeticallydominant primary producers (Figure 8A, B). In addition,the total potentially bioavailable energy yields in themixing zones were greater in the MOR-U setting than inthe typical MOR-B and ABA settings (Figure 8A, B).Thus, the MOR-U deep-sea hydrothermal environments

may supply more abundant and diverse energy sourcesfor biological production.In the SED setting, aerobic methanotrophy could be

competitive with aerobic sulfur oxidation in all tem-perature ranges (Figure 8A). Interestingly, among allpossible chemolithotrophic metabolisms, anaerobic (sul-fate-reducing) methanotrophy was by far the mostfavorable energy-generating metabolism, particularly inhigh-temperature habitats (Figure 8B). The total amountof potentially bioavailable energy yield in the mixingzones of habitats in the SED setting was also greaterthan in the typical MOR-B and ABA settings.

Comparison of existing chemolithotrophic microbialcommunities with the results of thermodynamic modelingAbove, we have provided the theoretical basis for relation-ships between the geological environments of hydro-thermal activity (e.g., tectonic settings, basement-rockgeochemistry, abundance of sediments, magmatic volatileinput, and phase separation related to subseafloor hydro-thermal processes), physical and chemical variations inhydrothermal fluids, and the compositional diversity ofpotentially bioavailable energy for various vent-endemicchemolithotrophic metabolisms estimated using thermo-dynamic models. We have shown that the abundance andcomposition of chemolithotrophic energy metabolisms inhydrothermal vent biological communities is directly con-strained by the physical and chemical characteristics ofthe hydrothermal mixing zones of habitats, which are sub-ject to the physical and chemical properties of end-member hydrothermal fluids. Furthermore, the physicaland chemical characteristics of the end-member hydro-thermal fluids are substantially controlled by the geo-logical settings that host the hydrothermal systems. Thus,it seems likely that the abundance and composition ofchemolithotrophic energy metabolisms in microbial com-munities located in a given deep-sea hydrothermal systemcould be systematized in terms of geological backgroundsbased on the results of the thermodynamic models.In typical mixing zones in deep-sea hydrothermal habi-

tats, chemolithotrophic microbial communities consist oforganisms with three typical lifestyles: surface-attached orbiofilm-forming free-living entities, planktonic free-livingentities, and symbiotic entities. Here, we discuss potentialpatterns in chemolithotrophic microbial communitydevelopment delineated by recent microbiological investi-gations (biogeochemical, ecological, and molecular ap-proaches) for representative hydrothermal mixing zonesof habitats in which the predominant organisms have dif-ferent lifestyles.

Hydrothermal plumesHydrothermal plumes are typical of mixing zone habitatsthat host planktonic free-living microbial communities

MOR-B MOR-U ABA-M SED-MOR

EPR MAR CIR

MA

R CIR

Ker

mad

ecLau PACMANUS

Vie

nn

a W

oo

ds Juan de Fuca

Guaymas

Oki

naw

a Tr

ou

gh

Figure 8 Metabolic energies available from each (A) aerobic and (B) anaerobic reactions shown in Table 1. Calculations were performedfor H2 oxidation, H2S oxidation, methanotrophy, and Fe

2+ oxidation (aerobic reactions) and hydrogenotrophic methanogenesis, hydrogenotrophic SO4reduction, anoxic methanotrophy, and anaerobic Fe3+ reduction (anaerobic reactions) at the 89 hydrothermal vent sites in MOR-B, MOR-U, AMA-M,ABA-F, SED-MOR, and SED-ABA settings. Shaded areas represent hydrothermal vents issuing highly vapor-rich (


methanotrophic Gammaproteobacteria and ammonia-oxidizing Betaproteobacteria and Thaumarchaeota domin-ate the microbial communities in spatially and temporallyvarying hydrothermal plume habitats.An increasing number of recent observations appear

consistent with our conclusions based on thermo-dynamic estimates of bioavailable energy yields in low-temperature mixing zones: (1) aerobic sulfur oxidation isthe most common and basic chemolithotrophic energymetabolism in global deep-sea hydrothermal systems, (2)aerobic Fe2+ and Mn2+ oxidation are less abundant butwidespread metabolisms, and (3) aerobic methanotrophyand ammonia oxidizer are dominant in SED systems,respectively.

Diffusing hydrothermal fluidsMicrobial communities in relatively low-temperature dif-fusing hydrothermal fluids have been investigated in awide variety of geographically diverse hydrothermal sys-tems (Huber and Holden 2008; Huber et al. 2009; Perneret al. 2011, 2013a, 2013b; Akerman et al. 2013; Campbellet al. 2013). These are mainly planktonic free-livingcommunities under conditions in which the end-member fluids have already mixed with infiltrated sea-water in relatively shallow subseafloor environments inthe recharge and discharge regions of hydrothermalfluids (Bemis et al. 2012). In addition to planktonic free-living populations, these microbial communities alsoinclude detached epilithic and biofilm-forming compo-nents entrained by the fluid flows.Hydrothermal fluids diffusing at the seafloor would be

expected to combine all growing, living, and dead popu-lations and components within the entire subseafloorfluid flow path in the discharge. This differs from micro-bial communities in hydrothermal plume habitats inwhich most microbial populations are indigenously grow-ing from planktonic origins in deep-sea water (Lesniewskiet al. 2012). Thus, it is challenging to clearly understandthe relationships between the diversity and compositionof the observed microbial populations and hydrother-mal fluid chemistry based on existing biological andgeochemical data for diffusing fluid habitats. However,several studies have recently suggested the dominanceof sulfur oxidizers in typical MOR-B settings and thepresence of hydrogen oxidizers in MOR-U settings(Perner et al. 2011, 2013a; Akerman et al. 2013). Theseresults are generally consistent with our thermodynamicpredictions of relationships among microbial metabo-lisms and functions, hydrothermal fluid chemistry, andgeological background.On the other hand, a very recent study producing

function-focused quantitative estimates, based on H2and sulfide consumption and CO2 assimilation activitiesas well as metagenomic 16S rRNA and functional gene

analyses, has indicated that even in H2-poor hydrother-mal fluids in MOR-B settings, H2 oxidation-based pri-mary production is highly attractive despite the low H2content (Perner et al. 2013b). This leads us to considerthat low-temperature diffusing flow is the product ofcomplex subseafloor processes (including seawater-hydrothermal fluid mixing, conductive cooling, variousredox reactions, and mineral precipitation), and thus,the simple batch-mixing model employed in this studymay not be able to accurately reproduce all of theseprocesses.Geochemical data sets for low-temperature diffusing

flows remain scarce. Thus, further quantitative estimatescombined with in situ or detailed chemical measure-ments will be needed to more accurately describe inter-actions among the physical and chemical processes,bioavailable energy yields from chemolithotrophic me-tabolisms, and community development in diffusinghydrothermal fluids.

Chemosynthetic invertebratesChemolithotrophic symbionts hosted by deep-sea vent-endemic chemosynthetic invertebrates represent import-ant primary producers in global deep-sea hydrothermalecosystems. Their biomass production and functionsmay be constrained by the energy states of the habitatsof both the symbionts and the host animals (Dubilieret al. 2008), as productivity and energy metabolism in atight symbiotic association are strongly regulated by theinteraction of the symbiont with the physiology andecology of the host animal (Dubilier et al. 2008). Therehave been numerous studies of the basic relationshipsbetween the in situ physical and chemical conditions ofhabitats and the abundance and composition of energymetabolisms in deep-sea hydrothermal chemosyntheticsymbioses (Beinart et al. 2012; Petersen et al. 2011;Suzuki et al. 2006; Watsuji et al. 2010, 2014). However,the energy conversion yield of the primary production ofchemolithotrophic symbionts is likely one of the mostimportant factors in the establishment of chemosyn-thetic symbioses, affecting the selection, acquisition, andbreeding of specific bacterial counterparts. In particular,episymbioses and horizontally transmitted endosymbio-ses, in which symbionts are acquired from the proximalenvironments of habitats in their larval and adult stagesin each generation, would be expected to be morestrongly affected by the energy states of chemolitho-trophic symbiont metabolisms than vertically transmit-ted endosymbioses.Recently, several studies have been conducted of the

relationship between the activity of chemolithotrophicsymbionts and hydrothermal fluid chemistry, e.g., aseries of studies on epibiotic microbial communities inthe galatheid crab Shinkaia crosnieri in Okinawa Trough


(Watsuji et al. 2010, 2012, 2014). The epibiotic microbialcommunities of S. crosnieri abdominal setae consist pri-marily of the sulfur-oxidizing Epsilonproteobacteria andGammaproteobacteria and methanotrophic Gammapro-teobacteria (Watsuji et al. 2010, 2012, 2014). These re-sults are generally consistent with the results of ourthermodynamic modeling, indicating high bioavailableenergy yields from both sulfur- and CH4-oxidizing reac-tions at low temperatures (high seawater mixing ratios)in the Okinawa Trough (Figure 8). The abundance ofepibiotic methanotrophic gammaproteobacterial popula-tions and methanotrophic activity vary among the S.crosnieri populations recovered from different hydro-thermal fields (Iheya North and Hatoma Knoll fields)(Watsuji et al. 2010). As suggested by our model calcula-tions, these variations are likely correlated with the insitu CH4 concentrations in the S. crosnieri colonies. Thismay, in turn, be associated with the CH4 concentrationsin the end-member hydrothermal fluids, although CH4concentrations in the Hatoma fluids have not yet beenpublished.Another notable example is the dual endosymbiotic

(thiotrophic and methanotrophic) populations of ventmussels living in different geological settings of deep-seahydrothermal vent sites in the MAR and the EasternPacific (Petersen et al. 2011). Based on thermodynamicmodeling of preferred H2-trophic energy metabolism,genetic characterization of a key enzyme gene for H2-trophic energy metabolism, and functional analyses ofH2 consumption and CO2 fixation of endosymbionts inBathymodiolus puteoserpentis in a typical MOR-Uhydrothermal system (Logatchev field), Peterson et al.(2011) clearly demonstrated that the thiotrophic popula-tion in dual endosymbiosis of the Logatchev B. puteoser-pentis use H2 and H2S comparably as energy sources forprimary production. This was the first reported exampleof chemosynthetic symbiosis sustained by an inorganicenergy source (H2) other than H2S (reduced sulfur spe-cies) or CH4. In other words, this study first revealedthat compositional variations in H2, H2S, and CH4 in themixing zones of chemosynthetic macrofaunal habitatsaffect the patterns and functions of episymbioses andendosymbioses in chemosynthetic microbial-faunal as-sociations. Peterson et al. (2011) also showed that thethio- and H2-trophic endosymbionts hosted by differ-ent Bathymodiolus populations living in geographicallyand geologically distinct hydrothermal systems of theMAR and Pacific (all H2-starved MOR-B hydrothermalsystems) had much lower specific H2 consumption ac-tivities than the endosymbiotic population from theH2-abundant MOR-U hydrothermal system (Logatchevfield). Although not fully quantitative, these results pro-vide strong evidence that the metabolic activity of chemo-lithotrophic symbionts is controlled by hydrothermal fluid

chemistry and is related to the geological backgroundof the hydrothermal system, as suggested by our modelcalculations.Recently, metagenomic and metatranscriptomic ap-

proaches have also been used to study possible bio-geochemical associations with Alviniconcha (deep-seahydrothermal-vent snail) holobionts (host/symbiont as-sociations) that dwell in a broad region of the EasternLau Spreading Center (ELSC) (Beinart et al. 2012; Sanderset al. 2013). Different holobiont patterns have been foundin the Alviniconcha populations obtained from the mixingzones of colonies in four different hydrothermal systemsin the ELSC. The endosymbionts were classified into threegroups: Sulfurimonas-type Epsilonproteobacteria, gamma-1-type Gammaproteobacteria, and gamma-Lau-type Gam-maproteobacteria (Beinart et al. 2012), all of which areknown to be typical sulfur (and H2) oxidizers. The Alvini-concha holobiont and endosymbiont distributions variedfrom the northern to the southern region of the ELSC,which have somewhat different geological settings (Beinartet al. 2012). The ELSC has been well characterized fromnorth to south in terms of geological properties (such asthe spreading stage and rate, magmatic productivity, geo-chemistry, and host-rock geochemistry) (Tivey et al.2012). Reflecting the change in geological setting, thechemical compositions of the end-member hydrothermalfluids also change from relatively reduced and H2- andH2S-enriched (approximately 500 μM and approximately5 mM, respectively) in the north to relatively oxidized andH2- and H2S-depleted (approximately 30 μM and approxi-mately 3 mM, respectively) in the south (Beinart et al.2012). The endosymbiont species shift from predomin-antly Sulfurimonas-type Epsilonproteobacteria in thenorth to predominantly gamma-1-type Gammaproteobac-teria and finally to both types of Gammaproteobacteria inthe south (Beinart et al. 2012). Interestingly, the compos-itional abundance of both the endosymbiotic microbialcomponents and the expressed key gene transcripts forvarious energy metabolisms vary with the regional geo-chemical gradient (Sanders et al. 2013). Under relativelyreduced and H2- and H2S-enriched conditions, the com-positional abundance of mRNAs related to H2- andsulfur-oxidizing metabolisms throughout the entire endo-symbiont transcriptome is highly elevated (Sanders et al.2013). The compositional abundances of the mRNAs ofthese energy metabolisms throughout the entire endosym-biont transcriptome are likely associated with the activitiesof these energy metabolisms in the endosymbiotic popula-tions of the Alviniconcha host individuals.Our geochemical modeling suggests that changes in

the H2S concentration from north to south in the ELSC(approximately 5 mM to approximately 3 mM) shouldnot significantly affect sulfur-oxidizing metabolisms,whereas H2-oxidizing metabolisms could be affected by


the change in H2 concentration (approximately 500 μMto approximately 30 μM) (Figure 6). Indeed, based ondifferences in the expression of hydrogenases betweenEpsilonproteobacteria and Gammaproteobacteria indi-viduals, Sanders et al. (2013) suggested that H2 oxidationmay play a larger role in the energy metabolism of holo-bionts with Epsilonproteobacteria. Thus, the change inH2 concentration, rather than the H2S concentration,may account for differences in the holobiont patternsfound in the Alviniconcha populations in the ELSC. Al-though future studies are needed to elucidate the degreeto which Epsilonproteobacteria endosymbionts rely onH2 for energy production, this may be additional evi-dence supporting the relationship between geologicalconstraints on hydrothermal fluid chemistry and thecompositions and functions of chemosynthetic microbialsymbionts in deep-sea hydrothermal environments.

Chimney structures and sedimentsThe compositional and functional diversity of microbialcommunities has been most extensively explored in deep-sea vent chimney structures that host high-temperaturehydrothermal fluid emissions (Nakagawa and Takai 2008;Takai and Nakamura 2010, 2011; Takai et al. 2006b).These microbial communities consist of typical epilithic(mineral surface-attached) and/or biofilm-forming popula-tions and are sustained by the redox disequilibria formedin the chimney wall via diffusive mixing between the in-ternal hydrothermal fluid and external seawater. Thus, theabundance and composition of chemolithotrophic energymetabolisms in the chimney microbial communities aredirectly controlled by the energy states of the chimneyhabitats, resulting in good approximations by the thermo-dynamic calculations of the simple batch-mixing model.Using data for both end-member hydrothermal fluids

and chimney microbial communities obtained from sixdeep-sea hydrothermal systems with different geologicalsettings, Takai and Nakamura (2010, 2011) constructedintra-field and inter-field comparisons between theabundance and composition of chemolithotrophic en-ergy metabolisms predicted by thermodynamic modelingand the microbial community composition determinedthrough quantitative cultivation methods. Based on boththe thermodynamic modeling and microbiological cha-racterization, statistically significant correlations betweenthe H2 concentration in the hydrothermal fluid or theestimated potential energy yield of H2-trophic methano-genesis and the cultivatable population size of hydroge-notrophic methanogens were found. More recently, inaddition to quantitative cultivation methods, statisticalphylotype compositional analyses of 16S rRNA andother functional genes have also been used to demon-strate significant correlations between H2-trophic che-molithotrophy in chimney microbial communities and

hydrothermal fluid H2 concentrations, particularly inMOR-U hydrothermal systems (Flores et al. 2011; Rousselet al. 2011). Our geochemical model provides consistentexplanations for the results of these studies. Specifically,the energy yields of anaerobic (and aerobic, in most cases)H2-trophic reactions were well correlated with the H2concentrations of hydrothermal fluids (Figure 6). Inaddition, thermophilic H2-trophic methanogens and sul-fate/sulfur reducers are predominantly found in H2-enriched deep-sea hydrothermal systems in the MOR-Usetting (Figure 8). It is thus very likely that serpentinization-driven H2 enrichment in hydrothermal fluids is animportant geochemical factor that directly controls thethermodynamic energy potential, biomass, and product-ivity of H2-trophic chemolithotrophs.Similar to the apparent relationship between H2 con-

centrations in hydrothermal fluids and the abundance ofH2-trophic chemolithotroph populations, our thermody-namic calculations also identified a possible relationshipbetween CH4 enrichment and the abundance of anaero-bic methanotroph populations (particularly thermophilicmethanotrophic sulfate reducers) in SED hydrothermalsystems (Figure 8). In low-temperature habitats (e.g.,hydrothermal plumes, diffusing fluids, and chemosyn-thetic animal symbioses), many molecular signals andmetabolic activities of aerobic methanotrophy have beenobserved. However, the existence of anaerobic thermo-philic methanotrophic sulfate reducers has been inferredonly from lipid biomarker signals (Schouten et al. 2003).Recently, thermophilic anoxic CH4-oxidizing SO4-reducingactivities have been directly verified at up to 70°C inthe sediments of the Guaymas Basin hydrothermal field(Holler et al. 2011). In addition, possible microbial compo-nents of thermophilic anaerobic methane oxidizers, con-sortia of ANME-1a Archaea and HotSeep-1 clusterDeltaproteobacteria, have been identified via FISH analysis(Holler et al. 2011). Similar phylotypes of potentiallythermophilic ANME-1a Archaea have also been found inhydrothermal sediments and diffusing fluids of SEDhydrothermal systems such as the Axial Seamount andEndeavour Segment fields in the Juan de Fuca Ridge andthe Yonaguni Knoll IV field in the Okinawa Trough(Nunoura et al. 2010; Merkel et al. 2013). Because thesephylotypes of thermophilic anaerobic methanotrophic Ar-chaea remain resistant to cultivation, quantitative cultiva-tion methods are not feasible. However, other quantitativetechniques targeting 16S rRNA and functional gene tran-scripts together with direct metabolic activity measure-ments are now available (e.g., Beal et al. 2009; Watsujiet al. 2012, 2014). Such quantitative estimates will providemultiple lines of evidence for the relationship betweenCH4 enrichment in SED hydrothermal systems and theabundance of thermophilic methanotrophic sulfate re-ducers in mixing zone habitats.


Takai and Nakamura (2010) have also noted that phaseseparation has a considerable impact on intra-field varia-tions in hydrothermal fluid chemistry. In microbiologicalstudies of the Iheya North field in the middle OkinawaTrough and the Mariner field in the Lau Basin, in-creased populations of anaerobic and aerobic H2-trophicchemolithotrophs (e.g., Methanococcales and Aquifi-cales) were observed, potentially due to phase separationof hydrothermal fluids (Nakagawa et al. 2005b; Takaiet al. 2008). However, in studies of the Yonaguni KnollIV field in the Southern Okinawa Trough, H2-trophic(and thiotrophic) chemolithotrophs (e.g., Methano-coccales, Desulfurococcales, Nautiliaceae, and Thiore-ductoraceae) were the dominant microbial componentsin both vapor- and brine-rich hydrothermal fluids(Nunoura and Takai 2009). Although H2S concentrationdata for the Yonaguni Knoll IV fluid have not yet beenreported, our geochemical model calculations indicatethat if the H2 concentrations of the end-member hydro-thermal fluids were well below approximately 1 mmol/kg,the metabolic energy available from both aerobic andanaerobic H2-trophic reactions would be directly corre-lated with the H2 concentration of the fluids (Figure 6).The H2 concentrations in the vapor- and brine-richhydrothermal fluids venting at the Iheya North field(0.045 and 0.096 mmol/kg, respectively) and the Marinerfield (0.012 and 0.13 mmol/kg, respectively) are well belowapproximately 1 mmol/kg and thus, phase separation-induced H2 variations may directly affect the availableenergy yields from aerobic and anaerobic H2-trophic re-actions. In contrast, the H2 concentrations in the fluidsat the Yonaguni Knoll IV field (0.8 to 3.6 mmol/kg) aremostly above approximately 1 mmol/kg, resulting insaturation of the metabolic energy available from aer-obic hydrogenotrophic reactions, particularly at highertemperatures (Figure 6). In addition, the bioavailableenergy yield from hyperthermophilic anaerobic reac-tions is nearly comparable to that from aerobic thio-trophic reactions, even in brine-rich hydrothermalfluids (Figure 6). This may explain why there are nomajor differences in abundance or composition of mi-crobial communities between the vapor- and brine-richhydrothermal fluids in the Yonaguni Knoll IV field(Nunoura and Takai, 2009).

ConclusionsWe have provided an overview of variations in the geol-ogy, geochemistry, microbial energy metabolisms, andcommunity development associated with global deep-seahydrothermal systems. Relationships among the geo-logical backgrounds of hydrothermal activities (e.g., tec-tonic settings, basement rock geochemistry, abundanceof sediments, magmatic volatile inputs, and phase separ-ation related to subseafloor hydrothermal processes),

physical and chemical variations in hydrothermal fluids,and compositional diversity of potentially bioavailableenergy for various vent-endemic chemolithotrophic me-tabolisms have been elucidated through thermodynamicmodeling of redox states in hydrothermal mixing zonehabitats. In addition, these relationships have been em-pirically substantiated by recent multidisciplinary bio-geochemical and microbiological studies of existingmicrobial communities and their metabolic functions inrepresentative deep-sea hydrothermal systems in differ-ent geographic locations and geological settings.However, thermodynamic estimates of potential energy

for possible chemolithotrophic metabolisms are basedon certain simplifications, particularly with respect toquantitative representations of mixing of source hydro-thermal fluids and seawater and the kinetic effects ofabiotic reactions, cellular uptake and excretion of energysources, and enzymatic functions on energy metabolism.These shortcomings may result in differences betweenthe theoretical predictions and actual configurations andpatterns in some cases. To characterize the in situ physicaland chemical characteristics of hydrothermal mixing zonehabitats at high spatial and temporal resolution, severalelectrochemical sensors have been developed and appliedto various habitats such as diffusing hydrothermal fluidsand chemosynthetic animal colonies. However, these sen-sors have some technical challenges, including multiplechemical interferences, relatively narrow dynamic ranges,and the need for in situ calibration (Luther et al. 2012). Adeep-sea in situ membrane inlet mass spectrometry(MIMS) method has also been developed and used for insitu measurement of volatile and time-sensitive chemicalspecies (Wankel et al. 2010). These newly developed insitu measurement tools will enable more precise estimatesof the energy states of habitats of chemolithotrophic mi-crobial communities. Improvement and development ofbiogeochemical and microbiological characterization tech-niques are also necessary to understand the functionaland metabolic abundance and composition of microbialcommunities in deep-sea hydrothermal environments. It isa significant challenge to quantify the biomass, productiv-ity, and functions of dominant microbial components indeep-sea vents. Comprehensive characterizations of in situmRNA assemblages using such tools as GeoChip technol-ogy (Wang et al. 2009) and the metatranscriptomic ap-proach (Dahle et al. 2013) will likely prove more objective,quantitative, and effective than employing elaborate quan-titative cultivations using numerous media for intra-fieldand inter-field comparisons of microbial communities andtheir functions. Successfully overcoming these challengesis essential for clarifying the relationships between geology,geochemistry, microbial energy metabolisms, and com-munity development associated with global deep-seahydrothermal activities.


Additional file

Additional file 1: Chemical compositions of end-memberhydrothermal fluids and seawater used in this study. Data are from89 hydrothermal vent sites in MOR-B, MOR-U, AMA-M, ABA-F, SED-MOR,and SED-ABA settings.

AbbreviationsABA: arc-backarc; ABA-F: felsic rock-hosted hydrothermal system in anarc-backarc setting; ABA-M: mafic rock-hosted hydrothermal system in anarc-backarc setting; MOR: mid-ocean ridge; MOR-B: basalt-hostedhydrothermal system in a mid-ocean ridge setting; MOR-U: ultramaficrock-hosted hydrothermal system in a mid-ocean ridge setting;SED: sediment-associated; SED-ABA: sediment-associated hydrothermalsystem in an arc-backarc setting; SED-MOR: sediment-associatedhydrothermal system in a mid-ocean ridge setting.

Competing interestsThe authors declare that they have no competing interests.

Authors’ contributionsBoth KN and KT proposed the topic, conceived of and designed the study,compiled and processed the data, and wrote the paper. Both authors readand approved the final manuscript.

AcknowledgementsWe would like to thank the two anonymous reviewers for their constructiveand helpful comments, which have significantly improved the manuscript.This research was financially supported by the Ministry of Education, Culture,Science, and Technology (MEXT) of Japan through the special coordinationfund Project TAIGA: Trans-crustal Advection and In situ BiogeochemicalProcesses of Global Subseafloor Aquifer.

Author details1Precambrian Ecosystem Laboratory (PEL), Japan Agency for Marine-EarthScience and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka,Kanagawa 237-0061, Japan. 2Current address: Department of SystemsInnovation, School of Engineering, The University of Tokyo, 7-3-1 Hongo,Bunkyo-ku, Tokyo 113-8656, Japan. 3Subsurface Geobiology AdvancedResearch (SUGAR) Project, Japan Agency for Marine-Earth Science andTechnology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061,Japan.

Received: 8 November 2013 Accepted: 15 March 2014Published: 22 April 2014

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