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Fungi, ecosystems, and global change

Kathleen K Treseder, University of California Irvine

Fungi drive many ecosystem dynamics

Decomposition

CO2

Soil C storage

Ophis

CO2 NYBG

Improve plant growth

CO2

Fungal feedbacks on global change

Fungi

Ecosystem function

Global change

Drought

Fungal groups

Soil C storage

Climate change

Possible scenario

+

?

?

?

The Challenge

Microbes to Ecosystems

Soil carbon stocks

r2: 0.06–0.39

Empirical measurements Model estimates

Todd-Brown et al. 2013, Biogeosciences

40+

0

10

20

30

kg m-2

Harmonized World Soil Database

The Challenge

Microbes to Ecosystems

The Challenge

Genes to Ecosystems

Transformative technology

RFLP – Hinf I

Transformative technology

RFLP – Hinf I

02,000,0004,000,0006,000,0008,000,00010,000,00012,000,00014,000,00016,000,00018,000,000

2000 2005 2010 2015

RFLP

Base pairs per study

Transformative technology

RFLP – Hinf I

02,000,0004,000,0006,000,0008,000,00010,000,00012,000,00014,000,00016,000,00018,000,000

2000 2005 2010 2015

Sanger RFLP

Base pairs per study

Transformative technology

RFLP – Hinf I

02,000,0004,000,0006,000,0008,000,00010,000,00012,000,00014,000,00016,000,00018,000,000

2000 2005 2010 2015

Sanger RFLP

Microarray

Base pairs per study

Transformative technology

RFLP – Hinf I

02,000,0004,000,0006,000,0008,000,00010,000,00012,000,00014,000,00016,000,00018,000,000

2000 2005 2010 2015

RFLP

Microarray

454

Base pairs per study

Sanger

Transformative technology

RFLP – Hinf I

02,000,0004,000,0006,000,0008,000,00010,000,00012,000,00014,000,00016,000,00018,000,000

2000 2005 2010 2015

RFLP

Microarray

454

Base pairs per study

Sanger

Illumina

Evolutionary histories of fungi

Treseder, K. K., M. R. Maltz, B. A. Hawkins, N. Fierer, J. E. Stajich, and K. L. McGuire. 2014. Evolutionary histories of soil fungi are reflected in their large-scale biogeography. Ecology Letters 17 (9): 1086-1093.

Current distributions of fungi

Older phyla

Younger phyla

Treseder et al. 2014, Ecology Letters

Cryp

to

Chyt

ridio

Blas

tocl

adio

Ento

mop

htho

ro

Muc

oro

Zygo

Glo

mer

o

Pezi

zo

Sacc

haro

Pucc

inio

Ust

ilagi

no

Agar

ico

Most predictive variable: Precipitation

0

500

1000

1500

2000

2500

3000

Pref

. mea

n an

nual

pr

ecip

. (m

m y

-1 )

P = 0.023

Treseder et al. 2014

Cryp

to

Chyt

ridio

Blas

tocl

adio

Ento

mop

htho

ro

Muc

oro

Zygo

Glo

mer

o

Pezi

zo

Sacc

haro

Pucc

inio

Ust

ilagi

no

Agar

ico

Past climate events

600–800 million yrs ago

Cosmos Magazine

Drier ecosystems Wetter ecosystems

Treseder et al. 2014, Ecology Letters

β1,3-glucan

K. Vega & M. Kalkum

Fungal cell wall

β1,3-glucan

Cell membrane

Chitin

β1,3-glucan improves drought tolerance (Shima et al. 2008)

157 whole fungal genomes

1000 Fungal Genomes Project

β1,3-glucan may facilitate colonization of drier ecosystems

0

1

2

3

4

5

0 1000 2000 3000 4000 5000

β1,3

-glu

can

synt

hase

gen

es

(# p

er 10

,000

gen

es)

Preferred mean annual precipitation (mm y-1)

P = 0.001

En

Us Mu

Pu

Ag

Pe

Sa

Ch Bl Gl Cr

Treseder & Lennon 2015

β1,3-glucan may facilitate colonization of drier ecosystems

0

1

2

3

4

5

0 1000 2000 3000 4000 5000

β-gl

ucan

syn

thas

e ge

nes

(# p

er 10

,000

gen

es)

Preferred mean annual precipitation (mm y-1)

En

Us Mu

Pu

Ag

Pe

Sa

Ch Bl Gl Cr

Xie et al. 2012

Treseder & Lennon 2015

Drought tolerance Recalcitrant

C residues

Linked traits

β1,3-glucan in cell walls

Drought

Fungi with β-glucan

C residues

Soil C storage

Climate change

Potential feedbacks on climate

Recalcitrant

+

+

+ +?

–?

What other traits coincide with β1,3-glucan?

Stress tolerance

∗ Trehalose ∗ Cold-induced RNA

helicase

Decomposition

∗ Lignin breakdown ∗ Cellulose breakdown

Treseder, K. K. and J. T. Lennon. 2015. Fungal traits that drive ecosystem dynamics. Microbiology and Molecular Biology Reviews 79(2): 243-262.

Stress tolerance traits

Trehalose: drought & freezing tolerance Gene: NTH1

Stress tolerance traits

Cold-induced RNA helicase Gene: MRH4

Stabilized RNA: non-functional

RNA helicase

RNA helicase

RNA helicase

Sigrid Hart

Unwound RNA: translatable

Decomposition traits

Lignin peroxidase Gene families: LIP, MNP, VPL

Talbot et al. 2012

Blanchette/Jurgens

Decomposition traits

Quiroz-Castañeda/Folch-Mallol

Crystalline cellulase Gene family: AA9

Decomposition traits

Quiroz-Castañeda/Folch-Mallol

Cellobiohydrolase Gene family: GH7

Morphological groups

Free-living filamentous

fungi

Yeasts

Mycorrhizal fungi

Research questions

Extremes (drought)

Moderate conditions

Decreased soil C storage

Increased soil C storage

Yeast respond positively

Free-living filamentous fungi respond positively

Response traits?

More production of recalcitrant C

Stronger ability to decompose

recalcitrant C

Effect Traits?

Climate ↑CO2

Trait linkage?

↓CO2

More production of recalcitrant C

Stronger ability to decompose

recalcitrant C

157 whole fungal genomes

1000 Fungal Genomes Project

Groups differ in traits

Decomposition Stress tolerance

Treseder & Lennon 2015

Which traits are linked?

0

10

20

30

40

0 5 10 15

Crys

talli

ne c

ellu

lase

AA

9 ge

ne fr

eque

ncy

(# p

er 10

,000

)

Cellobiohydrolase GH7 gene frequency (# per 10,000)

Ind contrast r = 0.47 Spearman’s rho = 0.84

Treseder & Lennon 2015

Linked traits

Trehalase β1,3-glucan synthase

RNA helicase

Lignin peroxidase

Cellulase AA9

Cellulase GH7

Yeasts

Free-living Filamentous fungi

Positive

Negative

Treseder & Lennon 2015

Implications

Extremes (e.g., drought)

Moderate conditions

Decreased soil C storage

Increased soil C storage

Yeast: ↑β1,3-glucan, trehalose, RNA

helicase

Filamentous: ↓β1,3-glucan, trehalose,

RNA helicase

Response traits

Effect traits

Climate ↑CO2 ↓CO2

β1,3-glucan = More recalcitrant C

↑Lignin peroxidase, Cellulases

Next steps?

Genes to Ecosystems

Trait-based models of ecosystems

Initialize

Allison 2012, Ecology Letters

Ophis

NYBG

Acknowledgements

∗ 1000 Fungal Genomes Project

∗ Steve Allison ∗ Linh Anh Cat ∗ Igor Grigoriev ∗ Caitlin Looby ∗ Yev Marusenko ∗ Jim Randerson ∗ Adriana Romero ∗ Michael Buchmeier

∗ DOE Joint Genome Institute

∗ NSF Ecosystems ∗ NSF Integrated Earth

Systems ∗ DOE Program in Microbial

Communities and Carbon Cycling

∗ DOE JGI Community Sequencing Program

Phylogenetic distribution

Gene frequency (# per 10,000 genes)