Microorganism Biofilm

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Fro the firt oece of oxygen prodced y arinecyanoacteria ~3.5 iion year ago1 to the ethano-gen xriating in the war, caron-rich wap of theCaronifero period2, icroia procee hae ongeen key drier of, and reponder to, ciate change.It i widey accepted that icroorgani hae payed akey part in deterining the atopheric concentrationof greenhoe gae, incding caron dioxide (CO

2),

ethane (CH4) and nitro oxide (N

2O) (which hae the

greatet ipact on radiative forcing), throghot ch ofEarth hitory. What i ore open to deate i the partthat they wi pay in the coing decade and centrie,the ciate feedack that wi e iportant, and howhankind ight harne icroia procee to an-age ciate change. The feedack repone of icro-organi to ciate change in ter of greenhoe gafx ay either apify (poitie feedack) or redce

(negatie feedack) the rate of ciate change. With thetwenty-firt centry projected to experience oe ofthe ot rapid ciatic change in or panet hitory,and with iogenic fxe of the ain anthropogenicgreenhoe gae eing tied integray to icroorgani,iproing or ndertanding of icroia proceeha neer een o iportant.

In terretria ecoyte, the repone of pantconitie and yiotic icroorgani, cha ycorrhiza fngi and nitrogen-fixing acteria, tociate change i we ndertood, oth in ter ofphyioogy and conity trctre39. Howeer, therepone of the heterotrophic icroia conitie in

oi to ciate change, incding waring and ateredprecipitation, i e cear. Thi i a crcia factor, a itdeterine the natre and extent of terretria-ecoytefeedack repone. Howeer, ndertanding therepone of icroia conitie to ciate changei copicated y the at and argey nexpored dier-ity of icroiota fond in the terretria enironent,for which ony a few exape of food we hae eenfy contrcted10. Ao, different terretria ecoytecoprie different icroia conitie, and thi ifrther coponded y effect of and e, other di-trance (ch a anageent practice)and differ-ent iogeographica pattern (ditrition of icroiaconitie oer pace and tie)11,12.

In thi Reiew, we exaine the direct and indirecteffect of ciate change on terretria icroia co-nitie and the iogeocheica procee that they

nderpin. We dic the tifactoria and tidirec-tiona interaction and feedack etween aoe-grondand eow-grond conitie, a we a oi aioticpropertie and their iportance in feedack reponeto ciate change. We ao arge that ing new, ophi-ticated oecar and iocheica too to etter nder-tand icroia repone can iproe the predictionof feedack repone to ciate change in ter ofgreenhoe ga eiion. Finay, we addre the effectof oi ntrient cycing and the feedack repone ofnet greenhoe ga fxe, and expore way in whichterretria icroorgani cod e expoited for theitigation of anthropogenic ciate change.

*MacaulayLand Use

Research Institute,

Aberdeen AB15 8QH, UK.Centre for Plants and the

Environment, University of

Western Sydney, Penrith

South, DCNSW 1797,

Australia.Institute of Biological and

Environmental Sciences,Cruickshank Building,

St Machar Drive, Aberdeen

AB24 3UU, UK.||Soil and Ecosystem Ecology

Laboratory, Lancaster

Environment Centre,

Lancaster University,

Lancaster LA1 4YQ, UK.School of GeoSciences,

University of Edinburgh,

Edinburgh EH9 3JW, UK.

Correspondence to B.K.S.

email:

[email protected]

doi:10.1038/nrmicro2439

Radiative forcing

A measure of the influence that

a factor has in altering the

balance of incoming and

outgoing energy in the

Earthatmosphere system. It

is an inde of the importance

of the factor as a potential

climate change mechanism.

Microorganisms and climatechange: terrestrial feedbacksand mitigation optionsBrajesh K. Singh*, Richard D. Bardgett||, Pete Smith and Dave S. Reay

Abstract | Microbial processes have a central role in the global fluxes of the key biogenic

greenhouse gases (carbon dioxide, methane and nitrous oxide) and are likely to respond

rapidly to climate change. Whether changes in microbial processes lead to a net positive ornegative feedback for greenhouse gas emissions is unclear. To improve the prediction of

climate models, it is important to understand the mechanisms by which microorganisms

regulate terrestrial greenhouse gas flux. This involves consideration of the complex

interactions that occur between microorganisms and other biotic and abiotic factors.

The potential to mitigate climate change by reducing greenhouse gas emissions through

managing terrestrial microbial processes is a tantalizing prospect for the future.

R E V I E W S

NATuRE REvIEWs |Microbiology vOlumE 8 | NOvEmbER 2010 |779

20 Macmillan Publishers Limited. All rights reserved10
mailto:[email protected]:[email protected]


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Heterotrophic

Of an organism: able to use

organic compounds asnutrients to produce energy

for growth.

Autotrophic

Of an organism: able to

synthesize organic carbon

from the fiation of inorganic

carbon (for eample, by

photosynthesis or

chemosynthesis).

Dissolved inorganic

carbon pool

The sum of inorganic carbon in

solution.

Net primary productionThe part of the total energy

fied by autotrophic organisms

that remains after the losses

through autotrophic

respiration.

Methanogenesis

The process by which methane

is produced by microorganisms

(mainly archaea).

Methanotrophic

Of an organism: able to use

methane as a nutrient to

produce energy for growth.

Nitrification

The conversion of NH3

into a

more oidized form such as

nitrate or nitrite.

Denitrification

The reduction of oidized

forms of nitrogen to N2O and

dinitrogen.

Reactive nitrogen

Nitrogen in a form that

can undergo biological

transformations, such as

nitrite and nitrate.

Microbial control of greenhouse gas emissions

undertanding the phyioogy and dynaic of icro-ia conitie i eentia if we are to increae orknowedge of the contro echani inoed ingreenhoe ga fxe13,14. Thi topic ha receied it-te attention owing to the aption that icroiaconity trctre ha itte reeance to arge-caeecoyte ode15, and to the ack of theoretica ack-grond and technoogie to eare the at dierityof icroia conitie in natra enironentand deterine their ink to ecoyte fnctioning.Neerthee, recent adance in oecar techniqeand their appication to the characterization of o-caednctiae icroorgani ha tarted to proidean iproed ndertanding of icroia contro ofgreenhoe ga eiion14.

Carbon dioxide. In the goa caron cyce, annaeiion of CO

2fro the rning of foi fe are

dwarfed y the natra fxe of CO2

to and fro theand, ocean and atophere. Crrent ee of ato-

pheric CO2 depend argey on the aance etweenphotoynthei and repiration. In ocean, photoynthe-i i priariy carried ot y phytopankton, whereaautotrophic and heterotrophic repiration retrn chof the caron taken p dring photoynthei to thedissolved inorganic carbon pool16,17. For terretria eco-yte, the ptake of CO

2fro the atophere y

net primary production i doinated y higher pant,t icroorgani contrite greaty to net caronexchange throgh the procee of decopoition andheterotrophic repiration (FIG. 1a), a we a indirecty,throgh their roe a pant yiont or pathogen andy odifying ntrient aaiaiity in the oi18.

Approxiatey 120 iion tonne of caron aretaken p each year ypriary prodction on and19,and ~119 iion tonne of caron are eitted, haf yatotrophic (ainy pant) repiration and haf y het-erotrophic oi icroorgani20. Together, the and andocean contitte a net ink of ~3 iion tonne of car-on each year, effectiey aoring aot 40% of crrentCO

2eiion fro foi fe e.

In addition, 1 iion to 2 iion tonne of caron areadded to the atophere each year21 throgh changein and e (predoinanty tropica deforetation).Frtherore, ecae oi tore ~2,000 iion tonneof organic caron, their ditrance y agrictre andother and e can greaty tiate the rate of organic

atter decopoition and net eiion of CO2 to theatophere22. For exape, deep poghing or drain-age of organic, caron-rich oi i known to tiaterate of decopoition and repiration, ecae it gieicroorgani greater acce to oth ried organiccaron and oxygen23. Throgh ch ctiation andditrance, oi are etiated to hae aready ot40 iion to 90 iion tonne of caron ince haninterention egan24. Athogh thee repone areediated y icroia actiity, it i generay thoghtthat change in the trctre and dierity of terretriaicroia conitie wi hae itte effect on CO

2pro-

dction at the ecoyte ee ecae, nike CH4

and

N2O prodction, CO

2prodction ret fro nero

icroia procee. Howeer, recent finding hae cha-enged thi aption y proiding eidence of a directink etween CO

2fxe and change in the trctre

and phyioogy of the icroia conity14,25.

Methane. Goa eiion of CH4

are argay eenore directy controed y icroorgani than ei-ion of CO

2. Natra eiion (~250 iion tonne

of CH4

per year)are doinated y icroia methano-genesis, a proce that i carried ot y a grop of anaer-oic archaea in wetand, ocean, ren and teritegt. Howeer, thee natra orce are exceeded yeiion fro han actiitie (ainy rice ctia-tion, andfi, foi fe extraction and ietock far-ing) (~320 iion tonne of CH

4per year), which,

aide fro oe eiion fro foi fe extraction,

Figure 1 | gu a ux. a | In terrestrial

ecosystems, atmospheric carbon dioxide (CO2) is fixed into

sugars by the autotrophic (mainly plant) communities in

the presence of daylight. Plants release a great portion of

fixed carbon back to the atmosphere through autotrophic

respiration. Along with the release of a substantial portion

of newly fixed carbon through their roots, plant litters form

a main source of energy for soil heterotrophs, including

microorganisms and animals; this carbon pool is respiredback to the atmosphere through heterotrophic respiration.

A smaller amount of organic carbon remains unused and is

stored in the soil. Some organic carbon is also used by some

microorganisms for energy, but at a slower rate. CO2

is also

released into the atmosphere by anthropogenic activites

such as fossil fuel burning (not shown). | The methane

(CH4) cycle involves the conversion of organic residues

(sugars) into CH4

by methanogenesis, which is mainly

carried out by a specialized group of archaea, called

methanogens, under anoxic conditions. However, most

CH4

produced in soils is immediately oxidized by

methanotrophs, which use CH4

as a source of energy. This

is mainly an aerobic process, and the availability of oxygen

is a rate-limiting step. Methanotrophs also oxidize some

atmospheric CH4. The CO2 produced by methane oxidationthen enters into the CO

2cycle (part a). | The substrates for

nitrous oxide (N2O) production, ammonium (NH

4+) and

nitrate (NO3

), enter soils in various forms. Atmospheric

dinitrogen (N2) can be deposited in the soil following

fixation by soil microorganisms and is subsequently

converted to NH4

+; alternatively, reactive forms (mainly

NO3

and NH3) can be deposited in precipitation or as dry

deposition. Sources of N2O, including fixed N

2, can also be

released from organic residues from plants and animals,

animal waste and nitrogen fertilizers. The major source of

anthropogenic substrate is agricultural application of

nitrogen fertilizers and manure. In soil, a considerable

amount of NH4

+ is used by plants and microorganisms,

and the remaining portion is transformed into NO3

by

NH3-oxidizing bacteria and archaea through nitrification.Most NO

3 is converted into N

2via various nitrogen oxides

(including N2O) by denitrification processes (carried out

by denitrifying bacteria), and these then escape in the

atmosphere. Some nitrate is leached into the groundwater,

and some is used by plants. CH3COOH, acetic acid; C

6H

12O

6,

glucose; H2, hydrogen gas; H

2O, water; NO

2, nitrite;

O2, oxygen gas.

R E V I E W S

780 | NOvEmbER 2010 | vOlumE 8 www.au.m/w/m



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Atmospheric CO2

Autotrophic respirationC6H12O6 + 6O2 6CO2 + 6H2O + ATP

Photosynthesis6CO2 + 6H2O C6H12O6 + 6O2

Heterotrophic respirationC6H12O6 + 6O2 6CO2 + 6H2O+ ATP

Decomposition by soilmicroorganisms and animals

Plants Animals

Nitrogenfertilizer

Organic carbon

Atmospheric CO2

Atmospheric CH4Photosynthesis6CO2 + 6H2O C6H12O6 + 6O2

Methane oxidation2CH4 + O2 CO2 + H2 + H2O2CO2 + O2 2CO2

MethanogenesisCH3COOH CH4 + CO2

Organic carbonand sugars

CH4 consumptionCH4

Atmospheric N2O

NH4+Nitrificationa NH3 + O2 NO2

+ 3H+

b NO2

+ H2O NO3

+ 2H+

Denitrification2NO3

+ 12H+ N2 + 6H2O

Nitrogen fixation

N2 + 6H+ 2NH3

NO3

Ammoniaoxidisers

Nitrogen-fixingbacteria

Denitrifiers

Methanogens

Methanotrophs

Leaching

a

b

c

are ao predoinatey drien y icroorgani 21.Methanotrophic acteria ere a a crcia ffer tothe hge aont of CH

4prodced in oe of thee

enironent (FIG. 1b). The o-caed ow-affinityethanotroph (actie ony at a CH

4concentration of

>40 part per iion; ao caed type I ethanotroph),which ainy eong to the ca Gaaproteoacteria,can often cone a arge proportion of the CH

4pro-

dced in oi efore it ecape to the atophere26. ForCH

4aready in the atophere, ethanotrophic acte-

ria ay ao act a a net CH4

ink. The o-caed high-affinity ethanotroph (actie at a CH

4concentration of


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iogeographica pattern of icroia conitie, a

we a the fnctiona ink etween icroorgani andpant conitie.

There i tantia eidence to gget that ciatechange wi hae oth direct and indirect effect on ter-retria icroia conitie and their fnction. Theeffect of increaed CO

2ee on icroia coni-

tie are often indirect, a they are ediated y cacadingeffect on pant etaoi, growth and dierity, andthe aociated change in oi phyicocheica proper-tie ch a oi oitre and reorce qaity (caronto nitrogen ratio)33. The ain direct effect of ciatechange on oi icroorgani are ikey to e caedy change in teperatre and oitre content. Thee

factor can affect procee ch a greenhoe ga fxin two way: y odifying the phyioogy of exitingicroia popation and/or y changing the trctreof the icroia conity. For exape, at higher te-peratre, ot icroorgani grow and e trateat fater rate, o the rate at which procee ch a re-piration occr ay change; howeer, the contro echa-ni reain the ae. In the econd cenario, in whichciate change faciitate a hift in icroia-conitytrctre, the proce rate and the echani of con-tro ight change, ecae the new icroia co-nity wi hae different phyioogie13(BOx 1). In extreecae, thi ay ret in the o of a particar proce(caed y, for exape, the o of an entire fnctionagrop, ch a denitrifier or ethanogen) and/or theproinence of a preioy inignificant proce (caedy, for exape, a hift in conity copoition toone with higher phyioogica capaiitie in organiccaron decopoition; BOx 1)13,34. beow we dic thegreenhoe ga fxe that ret fro icroia feed-ack repone to change in ciate and atopheric

copoition, incding increaed CO2 and teperatre,and atered precipitation.

Carbon dioxide. It i generay accepted that increaed e-e of CO

2qantitatiey and qaitatiey ater the reeae

of aie gar, organic acid and aino acid fro pantroot35, and thi can tiate icroia growth andactiity. Thi can then change the CO

2fx depending

on the aaiaiity of ntrient (ch a nitrogen)4,3638(FIG. 2). In the ong ter, it i arged that the increae inicroia ioa a a ret of increaed caron reeaey the root can ead to ioiization of oi nitrogen,therey iiting the nitrogen aaiae for pant and cre-ating a negatie feedack that contrain ftre increaein pant growth36. Thi, in trn, ay ead to an increaedoi caron to nitrogen ratio, which faor higher fn-ga doinance and dierity18,39,40. Fngi generay haehigher caron aiiation efficiencie (that i, they toreore caron than they etaoize) than acteria, and fn-ga ce wa ainy conit of caron poyer (chitin andeatin) that are ch ore reitant to decopoitionthan thoe in acteria ce erane and wa (pho-phoipid and peptidogycan). A a ret, in ecoytedoinated y fngi, oi repiration rate are typicay ow,which increae the potentia for caron eqetration40.Thi cenario i ikey to occr ony when nitrogen i agrowth-iiting factor, ch a in teperate foret41,42.

Howeer, eera tdie hae hown that increaed e-e of atopheric CO

2can ead to tantia increae

in oi repiration4346, and that, in genera, eow-grondrepone to increaed CO

2are often greater than aoe-

grond repone in the ae yte46. Conerey, inoe cae, ecae oi icroorgani preferentiaye aie caron oer copex caron, rate of itterdecopoition wi ow down, which in trn ay owerCO

2eiion y repiration and faor caron eqe-

tration in the oi. Change in the qaity and qantity ofcaron ppied y pant can ao infence the feedackrepone y directy affecting the phyioogy and trctreof the oi icroia conity27,47.

Box 1 | Microorganisms, process rates and climate models

The relationship between global changes (altered temperature, carbon dioxide (CO2)

levels and precipitation) and the rate of processes such as denitrification and

respiration can change according to the response of microbial communities. For

example, a soil process (such as the decomposition of organic carbon) converts a

component from state 1 to state 2 at a rate k, and it is assumed that the process is

mediated by the soil biota present (see the figure, part a). In the first scenario (see the

figure, part ), global change directly influences the functioning of existing microbialcommunities without altering the community structure. This may cause a shift in

the process rate, but its behaviour and controls remain unchanged. However, as in the

second scenario (see the figure, part ), a shift in microbial community structure causedby global change could also alter the fundamental control mechanism of the process.

Most ecosystem models and all climate models that include a description of microbial

processes use first-order rate kinetics, which assume that the microbial population is

sufficient to carry out the function (for example, decomposition) and that the rate of

the process is modified by environmental factors such as temperature and moisture.

This approach works well within the parameterized limits of the model, and process

rates largely follow trajectories that are mimicked well by such formulations. What is

not known, however, is what happens if the climate changes beyond the parameterized

limits. For example, if the structure of the microbial community changes in such a way

that the function also changes, a discontinuity in the response may occur and the

response could move to a different trajectory (see the figure, part ). Such threshold

effects cannot be represented in the current structure of ecosystem and coupled-climatemodels. Understanding these potential threshold effects and identifying the systems

and processes for which they are likely to be of greatest importance remain key

challenges for microbiology.

Figure part a is modified, with permission, from REF. 34 (1998) Wiley and Sons, and figure

parts and are modified, with permission, from REF. 13 (1998) Wiley and Sons.

State 1

Soilbiota

Rate = k

State 2

Rate

ofprocess

3

2

1

042 6

Global change

Community changed

Community unchanged

0

Rate

ofprocess

3

2

1

042 6

Global change0

Future conditionsCurrent conditions

a

c

b

Global change

R E V I E W S




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Plant biomass

CO2 levels

Carbon release

Soil biotaSufficientnitrogen

Limitednitrogen

Oligotroph-dominatedcommunity

Low CO2 flux High CO2 flux

Copiotroph-dominatedcommunity

Carbonsequestration

Carbonsequestration

Permafrost

Soil that remains permanently

frozen.

Recalcitrant carbon

A form of carbon that is

resistant to microbial

decomposition owing to its

chemical structure and

composition.

Peatland

An area dominated by deep

organic soils.

The aerage goa rface teperatre i predictedto increae y etween 1.1 and 6.4 C y 2100 (REF. 21),and thi ight ao hae an effect on oi caron eqe-tration y potentiay acceerating heterotrophic icro-ia actiity. The enitiity of tae and aie fractionof oi organic caron to teperatre change i thoghtto ary greaty. For exape, increaed thaw rate anddepth in high-atitde permafrost render the arge tockof organic caron in thee oi (400 Petagra (Pg);that i, 4,000 iion tonne) nerae to increaeddecopoition rate48. Withot the aancing effect oforganic caron inpt fro aoe-grond priary pro-dction, thi cod ret in a arge and ncontroaepoitie-feedack effect49.

Oera, increaed teperatre ha een directyinked to increaed oi repiration, and a goa aerageteperatre increae of 2 C i predicted to increae oicaron reeae y 10 Pg, ainy owing to increae inicroia actiity5052. Thi i thoght to e ecae theincreaed teperatre wi tiate the e of aie car-

on; howeer, recalcitrant carbon i diere and copexin trctre, o it teperatre enitiity i ncertain.Thi cenario i frther copicated y the roe of eni-ronenta contraint in organic caron decopoi-tion, incding phyica and cheica protection againtenzyatic actiity, and the ipact of droght, food andteperatre on enzyatic actiity and on the aaiaiityof oxygen52. moreoer, thee enironenta contraintare theee affected y ciate change. Therefore,predicting the effect of teperatre increae on carontock ha een diffict. In oe cae, increaed te-peratre ay ead to a o of oi organic caron, epe-ciay in teperate ecoyte53,54. Indeed, a recent tdy

how that een te waring (y approxiatey 1 C)can increae the ecoyte repiration rate in a arc-tic peatland, particary in the rface ayer55. Thii indicatie of a arge and ong-ating poitie feedackof the organic caron tored in northern peatand to thegoa ciate yte, athogh the echani of thirepone reain ncear56.

becae different icroia grop hae ditinctoptia teperatre range for growth and actiity,increaed teperatre can affect the copoition ofthe icroia conity, which in oe cae codredce the reeae of oi organic caron owing to theo of acciatized icroia grop57. For exape,an increae in teperatre in a high-atitde ecoytereted in an p to 50% decreae in acteria and fn-ga andance and oi repiration, a we a a phyo-genetic hift in the fnga conity58, ggeting thatincreaed teperatre doe not away ead to enhancedcaron o to the atophere. To copicate atterfrther, thee change in repiration cod e caedy hift in the copoition and actiitie of icroia

conitie or y change in the qaity and qantity ofoi organic caron59,60.specificay, there i eidence thatwaring of oi ead to a decreaed reatie andanceof fngi and to change in acteria conity trctrein arctic ecoyte61, t the ong-ter redction inoi repiration de to waring cod ao e caed ythe eqentia reoa of eaiy decopoae organiccaron that ret fro an initia tiation of deco-poition. It i ao poie that oe oi organic caroni phyicay and cheicay protected fro icroiadecopoition59,62.becae there are o any ariae,the etiation of caron o y ciate change i nre-iae63, and redcing thi ncertainty wi e a ajoradanceent.

Another key deterinant of the terretria icroiaconity trctre and the decopoition rate of oiorganic caron i oi oitre, which wi e affectedy the 20% increae or decreae in precipitation ratethat ha een predicted y the Intergoernenta Paneon Ciate Change21. microia conitie repondto oitre ee directy, ecae they reqire waterfor phyioogica actiitie, and indirecty, owing to theeffect of changing oi oitre on ga diffion rateand oxygen aaiaiity. The effect of changing precipita-tion on the feedack repone of oi icroorganito ciate change ay therefore e de to the directeffect on icroia phyioogy and conity trc-

tre. long period of drier condition ay iit icro-ia growth and decopoition64 and ay coneqentyhae a negatie-feedack effect on caron fxe in oeecoyte. Howeer, oi drying ay increae oxygenaaiaiity and enhance caron cycing in wetand andpeatand, therey haing a poitie-feedack effect onCO

2fxe65.

It i iportant to note that feedack repone caedy atered teperatre and oitre wi differ etweendifferent ecoyte and region. For exape, increa-ing teperatre i ikey to hae a ore prononcedeffect in apine, arctic and teperate region ecaeicroia growth i often iited y teperatre in

Figure 2 | A m ua m ua mx a au

ma a. Increased levels of carbon dioxide (CO2) result in a higher plant

biomass and a higher rhizodeposition of carbon, which increases microbial biomass and

activity in the short term. However, in the long term, limitation of mineral nutrients such

as nitrogen may constrain this response. Such mineral limitation will affect the

dominance of oligotrophic and copiotrophic microorganisms in a given ecosystem,

which in turn may influence CO2

flux.

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Water table

The level at which the

groundwater pressure is the

same as the atmospheric

pressure.

thee ecoyte. Conerey, increaed droght condi-tion ay hae a tronger effect in tropica region, athi ay cae arge change in root growth and tan-tia redction in icroia ioa or hift in icro-ia conity trctre66,67. Therefore, the chaengei to qantify the feedack effect of ciate change ongreenhoe ga fx at oth the ecoyte and regionacae and then to integrate thi inforation to prodceore rot prediction on a goa cae.

Methane. CH4

i the econd ot iportant anthropo-genic greenhoe ga in ter of tota ciate forcing,and icroia tiization (ethanotrophy) i the argetterretria ink. Therefore, to etter predict CH

4ei-

ion, it wi e eentia to ndertand the repone ofCH

4fx to ciate change.

The repone of icroorgani-ediated CH4

fxe to change in ciate and atopheric copo-ition are a ncertain a thoe of CO

2fxe. Recent

anaye gget that ciate waring, particary athigh atitde, ay ead to a tantia increae in net

CH4 eiion fro perafrot and wetand, whichwi ere a a notae poitie feedack to goa ci-ate waring68. Athogh warer condition ight eexpected to increae the actiitie of oth ethanogenand ethanotroph when other factor are not iiting,it i y no ean cear whether thi repone wod eaanced and how it ight affect net CH

4eiion go-

ay. siiary, increaed net priary prodction andatered water table depth and oi water content, whichare ikey to occr foowing ciate waring in oeecoyte ch a arctic tndra, cod enhance eth-anogenei and net CH

4eiion, wherea redced

precipitation and drying of oi in other area codproote oxygen aaiaiity (and therefore CH

4

oxidation)and o redce net CH

4eiion69.

seera tdie hae hown that increaed CO2

e-e ead to a tantia decreae (p to 30%) in CH

4

ptake y oi icroorgani and to an increaedCH

4effx70,71. Howeer, the echani y which CH

4

ptake i decreaed reain nknown. In oe tdie,pant-ediated increae in oi oitre expain redc-tion in CH

4conption72,73, wherea in other tdie,

redced CH4

oxidation ha een fond to occr with-ot concoitant increae in oi oitre74. IncreaedCO

2ee ay affect CH

4eiion indirecty throgh

their effect on icroia actiity and phyioogy, and iti poie that pant-ediated increae in oi oi-

tre in the preence of increaed CO2 eein the oiwi ead to ore anoxic condition, therey increaingethanogenei and redcing ethanotrophy. Howeer,higher teperatre and redced oitre are thoghtto increae net CH

4ptake y terretria ecoyte, a

they inariay increae ga diffion rate and icroiaacce to oxygen and atopheric CH

4.

mot experienta deign to date hae teted theipact of one ciate ariae (for exape, increaedteperatre) on CH

4fx, t for etter prediction we

need to inetigate icroia repone in tifactoriaexperienta deign in which any interacting ciatic

ariae can e teted. In one ch tdy, oth increaed

teperatre and CO2

ee were teted itane-oy, and it wa reported that the tiatory effect ofincreaed CO

2ee on CH

4fx wa offet y increa-

ing teperatre75. Thi finding i in agreeent with aneary report tating that increaed teperatre enhancedCH

4ptake, wherea increaed CO

2ee decreaed it,

and it wa ggeted that the effect of oth treatentwa indirect and ediated throgh their ipact on oioitre72.

Increaed CO2ee hae een reported to redce the

andance of ethanotroph y p to 70% (REF. 76), othe feedack repone of CH

4fx cod ao e caed

y a hift in fnctiona icroia conitie. Indeed,preio tdie hae hown that CH

4fxe that occr

owing to change in and e are reated to change inthe copoition77,78 and andance79,80 of the ethano-troph conity. It i poie that change in CH

4

fx that are de to increaed CO2

ee or teperatreare ao reated to change in the andance and co-nity trctre of ethanotroph, t thi reqirefrther inetigation. soe tdie hae ao fond that

the andance of type II ethanotroph decined inrepone to increaing precipitationand teperatre81,82.Howeer, a recent tdy in a perafrot tndra areaoered the oppoite effect of increaed teperatreon thee icroorgani83, which ay gget that theethanotrophic conitie of different ecoyterepond differenty to atered teperatre and precipi-tation. Athogh the aaiae data gget a tantiarepone of the icroorgani-ediated CH

4fx rate

to projected change in ciate and atopheric co-poition, frther tdy of the teperatre enitiity ofdifferent grop of ethanogen and ethanotroph,and it interaction with oitre and CO

2ee acro

different ecoyte, i eentia to ore accrateypredict ftre terretria CH

4fxe.

Nitrous oxide. The direct effect of change in ciateand atopheric copoition on icroorgani-ediated fxe of N

2O ay e e prononced than

the effect on CO2

and CH4

fxe, with goa ei-ion eing priariy dependent on the ppy of reac-tie nitrogen (ch a NH

3and nitrogen oxide (NOx)).

Together with indtriaization and riing eiionof NOx fro foi fe rning, the intenification ofagrictre and aociated NH

3eiion ha ed to a

threefod to fiefod increae in the reeae of reactienitrogen oer the pat centry21. sch increaed aai-

aiity of reactie nitrogen in terretria ecoyte iikey to ret in enhanced nitrification and denitrifi-cation and, therefore, enhanced N

2O prodction84, t

again, the type and extent of interaction with ciatechange reain poory ndertood.

soe tdie hae reported a decreae in denitrifi-cation actiity at increaed ee of CO

2(REFS. 85,86),

wherea other reported no effect87,88. moreoer, oetdie reported an increaed N

2O eiion nder

increaed CO2

ee,t ony

when exce inera

nitrogen wa aaiae70,89. Thi ay gget that whenreactie nitrogen aaiaiity i ow an ecoyte wihow redced N

2O eiion nder increaed CO

2ee,

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Arable land

Land that is used for growing

crops.

Mineralization

The conversion of organic

carbon into inorganic forms,

mainly CO2.

wherea the reere wi e tre for an ecoyte withhigh reactie nitrogen aaiaiity. There i itte infora-tion aaiae on the icroia ai of ch change inN

2O fx, t hift in the trctre of NH

3-oxidizing

acteria conitie and decreae in their andancender increaed CO

2ee hae een oered90.

There are ao contradicting report on the tepera-tre enitiity of nitrifying and denitrifying icroiaconitie91. One anayi of preio tdie85 con-cded that projected increae in teperatre wod notgreaty affect nitrifying or denitrifying enzye. Howeer,other tdie hae fond that the proportion of the totaN

2O fx that i aociated with nitrification decreae at

higher teperatre, and thi wa inked to a change intrctre of the NH

3-oxidizing acteria conity92.

Ftre reearch on thi topic hod therefore foc onaeing N

2O prodction y nitrifying and denitrifying

icroorgani in reponeto a changing aaiaiity ofreactie nitrogen, and on it interaction with change inciate and atopheric copoition.

Microbial communities and mitigation optionsThe anipation of terretria ecoyte offera potentiay powerf ean y which to itigateanthropogenic ciate change. beow, we dic trate-gie that cod e ed to anage icroia coni-tie in the oi o that they contrite toward itigatingciate change.

Managing microbial communities to reduce carbondioxide emissions. Crrenty, oi contain aot 2,000 Pgof organic caron, which i twice the aont of caron inthe atophere and three tie the qantity fondin egetation21,93. The capacity of different and type

(for exape, woodand, patre and arable land) to torecaron differ, and it ha een ggeted that and ecan e anaged to eqeter a frther 1 Pg of caron peryear in oi93,94; thi potentia ha receied conideraecientific attention9598. Howeer, thi ay not e ea-iy achieae on a goa cae owing to the copexioogica echani that contro the incorporationof organic caron into oi, a we a the infence ofchanging aiotic factor, ch a oitre, teperatre,and e and nitrogen enrichent, which ao affect oicaron poo97,99. Foret oi are conidered to e epe-ciay effectie at toring caron, in part ecae of a highandance of fngi in the oi reatie to acteria, whichfaor caron eqetration (ee aoe)67,98,100,101.

To anage the oi icroia conitie toincreae caron eqetration, it wi e iportantto ndertand their ecoogy and fnction. Thi i achaenge in itef, ecae of or inaiity to character-ize the pecie dierity and fnction of oi icroiaconitie and or ack of theoretica principe inicroia ecoogy, ch a the definition of a pecie

and the factor driing conity foration andtrctre 102. Neerthee, there i oe eidencethat acteria can e categorized on the ai of theircaron mineralization capacity and can e diided intocopiotrophic (characterized y high growth rate onaie caron and doinant in ntrient-rich eniron-ent) and oigotrophic (ow-growing and doinantin ntrient-iited ecoyte) pecie103. It ha eenggeted that the Acidoacteria are oigotrophic,wherea the Proteoacteria and the Actinoacteria forcopiotrophic conitie (BOx 2). It can e arged thatanipating and e (for exape, changing froarae and to foretry) and and anageent practice(for exape, ing ow-nitrogen-inpt agrictre)ay proote the growth of oigotrophic conitie.Howeer, the ecoogica trategie of other doinanticroia taxa need to e ndertood. It i tre that nota taxa in a phy wi e either copiotrophic or oigo-trophic57, and th phya aone ay not e a predictorof caron o fro the oi103. It i therefore eentiathat we e rapidy deeoping technoogie ch ahigh-throghpt eqencing to etter ndertand oiicroia dierity. moreoer, eerging technoogiech a etagenoic, etatrancriptoic, eta-proteoic and tae-iotope proing (sIP) t eed to exaine the phyioogica aiitie and roe ofindiida taxa in a gien ecoyte (BOx 3). Ony then

can we egin to predict whether a particar oi i anet caron eitter or ink aed on icroia ecoogy.Thi approach can e frther expanded y coiningetagenoic with sIP to find ot the pecific fnctionof a icroia popation in a conity. Ftre workhod attept to e thi approach to differentiateetween popation that e aie caron and thoethat proote caron eqetration.

In agrictre, the often arge oe of oi organiccaron owing to ctiation can e redced y ow- andno-tiage practice, which faor oi conitiedoinated y fngi101. sch agroecoyte preentthe increae in icroia decopoition and repiration

Box 2 | Classification of bacteria on the basis of carbon mineralization

Owing to our inability to culture most microorganisms, functional classification of

bacterial communities has not been possible. However, recent findings suggest that

microorganisms can be classified into oligotrophs and copiotrophs. For example, a

combined experimental and meta-analysis study carried out on the rates of organic

carbon mineralization found that the phylum Acidobacteria exhibits oligotrophy,

whereas the class Betaproteobacteria and the phylum Bacteroidetes follow

copiotrophic lifestyles103

. A second study provided further evidence that bacterialcommunity composition influences heterotrophic respiration and that changes in

bacterial community composition can potentially influence soil carbon storage 121.

This study reported that the class Gammaproteobacteria and phylum Firmicutes

become dominant at the expense of the Acidobacteria in rain forest soils and are

responsible for enhanced mineralization of dissolved organic carbon and, therefore,

for increased soil respiration. These two studies, along with others122, suggest that

soils dominated by oligotrophs (such as the Acidobacteria) may have low carbon

turnover and, consequently, low carbon dioxide emission and higher carbon

sequestration.

Culturing oligotrophs from the natural environment is a long-standing problem. A

recent study123 showed that the trophic structure of microorganisms in marine systems

is reflected in their genomic contents and can be used as a proxy for uncultured

microorganisms. This indicates that we can classify uncultivable microorganisms into

trophic groups on the basis of their genome structure. Based on this study, a model was

developed that allows us to define the types of bacteria that specific ocean niches cansustain. Such a system could and should be used for defining microorganisms in a

terrestrial ecosystem. Use of such information in the future may improve the

predictions made by climate models.

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Grassland

Land that has grass as the

dominant vegetation.

that coe fro poghing and ditrance22, and it haeen propoed that widepread adoption of thi practicecod ead to eqetration of p to 55 Pg of organiccaron in rface oi104. Howeer, there are ao poi-e trade-off, a ow- or no-tiage agrictre ha eenfond, in oe cae, to enhance eiion of N

2

O frooi (owing to increaed rate of denitrification that arede to anaeroic condition in copacted oi), thereyoffetting oe of the enefit of increaed oi carontorage23. The conerion of cropand to peranentgrassland, which cae a id-p of organic atter atthe oi rface105,106, cod ao increae caron eqe-tration. Frtherore, the pant fnctiona dierity ondegraded or agrictray iproed oi54,96,107,108 code anipated to anage the ee of caron reeaedin the oi. Concoitant appication of nitrogen-aedfertiizer cod, in oe cae, enhance oi carontorage y increaing pant prodction and y ppre-ing icroia decopoition of recacitrant organic

atter109,110.There i contradictory eidence aot the effect of

nitrogen enrichent on oi caron tock, and thereforeit i not poie to ake weeping tateent aot howoi caron ink wi repond to nitrogen enrichent 99.moreoer, to reaize the rea potentia of oi to eqetercaron in the ong ter, we need to frther or nder-tanding of the interaction etween different ciatic(teperatre, oitre ee and water tae ee), oi(pH, oitre content and trctre) and iotic (acte-ria, fnga and archaea oi fana, and pant and theirconer) propertie that infence oi caron cycing,which i crrenty iited.

Managing microbial communities to reduce methaneemissions. Or ndertanding of the icroioogy ofgreenhoe ga cycing i ore copete for CH

4than

for CO2

or N2O, a the pathway i ipe and pecia-

ized icroorgani are inoed. Howeer, any ofthe aoe ncertaintie ao appy to the anageentof terretria CH

4fxe. becae ot atopheric CH

4

i prodced y icroorgani, it i theoreticay feai-e to contro a tantia proportion of CH

4eiion

fro terretria ecoyte y anaging icroia co-nity trctre and procee. The ioogica oxidationof CH

4y ethanotroph accont for ony ~5% of the

goa ink of atopheric CH4

(~30 iion tonne peryear)111 and ay therefore ee e iportant. Howeer,ethanotroph are ao reponie for the oxidationof p to 90% of the CH

4prodced in oi efore it can

ecape to the atophere112. It i we etaihed thatconerion of arae and or graand to foret ret ina tantia redction in CH

4fx113,114, and it i eident

that oth the type and andance of ethanotrophare iportant for predicting CH

4fx77,79,115. Howeer,

no crrent ciate ode conider thi finding, oftre reearch t foc on incorporating thee dataand interaction to iproe prediction of CH

4fxe

acro ario ecoyte. Thi knowedge can ao eappied to the redction of CH

4eiion y changing

and e and anageent. In rice ctiation, for exa-pe, ethanotroph hae ong payed a crcia part inaoring a proportion of the CH

4prodced and, a a

ret, iproed anageent of fooding freqency anddration cod redce net eiion y increaing oxy-gen aaiaiity in oi116. There i ao great potentia toake effectie e of inhiitor of ethanogenei, cha aoni phate fertiizer, in anaged yte toproote the growth of phate redcer at the expeneof ethanogen117. To redce ethane eiion frorinant ietock, trategie incde iproing feedqaity and directy inhiiting ethanogen conitiein the ren ing antiiotic, accine and aternatieeectron acceptor22.

Managing microbial communities to reduce N2O emis-

sions. A ajor orce of anthropogenic N2O eiion

i the e of nitrogen fertiizer in agrictre. A a -tantia proportion of appied fertiizer i eitted inthe for of N

2O, etter targeted fertiizer appication,

which redce the aaiaiity of nitrogen to icro-organi, can tantiay decreae N

2O eiion.

Potentia trategie incde redcing the aont of fer-tiizer and appying it at an appropriate tie (when cropdeand for nitrogen i high and eaching-o rate areow), ing ow-reeae fertiizer, and aoiding nitro-gen for that are ikey to prodce arge eiion oreaching oe (ch a nitrate in wet oi). siiary,iproed and drainage and etter anageent prac-tice to iit anaeroic condition in oi (for exape,and copaction and exceie wetne) cod redcedenitrification rate and, th, N

2O eiion. Finay,

for the itigation of N2O fxe fro agrictre, the

e of nitrification inhiitor in fertiizer to iit nitrateprodction and eqent eaching or denitrification

Box 3 | Advances in linking microbial communities to ecosystem function

Recent developments in molecular and genomic methods provide a golden

opportunity to assign ecological roles to different microbial taxa. Meta-omic

techniques have greatly advanced this area of science. Metagenomics involves the

direct isolation of DNA from environmental samples, its cloning into a vector and

its transfer into a surrogate host. Subsequent sequencing of all inserts provides

information on the type, diversity and functional ability of the microorganism.

Although covering all genomes will have logistical and cost constraints,metagenomics is useful if the aim of a study is to know the composition and

functional potential of a microbial community124,125. The presence of genes is only

an indicator of functional potential, and several genes are never expressed in a

microbial system. This problem can be overcome by first extracting RNA from the

sample and then constructing cDNA before sequencing (called metatranscriptomics).

This approach is now further improved by direct sequencing of RNA, which removes

bias associated with the synthesis of cDNA from RNA126. Metaproteomics, which

involves the direct extraction of proteins from the environment and their analysis by

mass spectrometry, has also greatly progressed recently. However, to fully use this

approach to link a microbial community with its ecological function, protein

databases need to be expanded.

Stable-isotope probing (SIP) is the most widely used method of microbial-community

analysis and involves tracking the incorporation of stable-isotope atoms from a

particular substrate into microbial cell components (such as DNA and RNA)127.

SIPmetagenomics is already providing new information on uncultivablemicroorganisms that oxidize methane or degrade pollutants128. In this case,

DNA from microorganisms that use labelled substrate is separated from other

microbial DNA before cloning. This ensures that most of the clones contain inserts

originating from the microorganisms that provide targeted functions, and therefore

reduces the number of clones to be screened to a manageable level.

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Response ofthe plant and

animalcommunity

Biological variables Climate variables

Soilgeochemistry

Response ofthe microbialcommunity

ImpactofCO2

Impact ofaltered

precipitation

Impact of temperature

Microbial adaption andfeedback response

Ecosystem response, includinggreenhouse gas flux

oe i now a we-etaihed trategy23. Thee andiiar icroorgani-ediated trategie (BOx 4) hae

great potentia to redce greenhoe ga eiion frothe and e and agrictra ector.

Conclusions and perspectives

There i conen aong cientit that goa ciatechange i happening and that the increae in goaaerage teperatre ince 1900 can e argey attri-ted to han actiitie. Howeer, there reain chncertainty aot prediction of ftre greenhoega eiion and the repone of thee eiion tofrther change in the goa ciate and atophericcopoition. To hep tacke thi ncertainty, there i

a need to etter ndertand terretria icroia feed-ack repone and the potentia to anage icroia

yte for the itigation of ciate change. There ian rgent need to iproe the echanitic ndertand-ing of icroia contro of greenhoe ga eiionand the interaction etween the different aiotic andiotic coponent that regate the. Thi ndertand-ing wi hep to reoe arge ncertaintie aot theprediction of feedack repone of icroorganito ciate change and wi enae the knowedge to eincorporated into ftre ode of ciate change andterretria feedack.

It i crrenty diffict to know whether change inprocee that are aociated with ciate change areroght aot y the effect of ciate change on oiicroia conitie, y change in oi aiotic fac-tor or y interaction etween the two. moreoer, it incear how icroorgani repond to ciate changeand therefore what their potentia i to infence ciatefeedack acro ecoyte and aong enironen-ta gradient. Another ie that need to e taken intoconideration i that, to date, ot tdie hae focedon one greenhoe ga, wherea eidence gget thaticroorgani-ediated fxe of different greenhoegae repond differenty to ciate change. For exape, iti aed that coneration of peatand wi enhance car-on eqetration, t thi ay ao increae CH

4fxe,

o the effect on net greenhoe ga fx i ti ncear.On the ai of the aoe inforation, we propoe

eera topic of reearch that need to e prioritized todeeop icroorgani-ediated approache to iti-gate ciate change. Firt, we need to etter ndertandand qantify icroia repone to ciate change tocoprehend ftre ecoyte fnctioning. second, weneed to caify icroia taxa in ter of their fnctionaand phyioogica capaiitie and to ink thi infora-tion to the ee of ecoyte fnction. Third, we need toiproe or echanitic ndertanding of icroia con-tro of greenhoe ga eiion and icroia reponeto itaneo ciatic factor, ch a waring, ateredprecipitation and increaed CO

2ee, acro different

ecoyte. Forth, we need to deeop a fraework

Box 4 | Microorganisms as a source of biofuels

Perhaps the most enticing and controversial area of microbial climate engineering is the substitution of fossil fuel energy

sources with biofuels. As strong sources of methane (CH4) production, landfill sites are increasingly being used for heat

and electricity generation. Numerous large-scale sites across the developed world now routinely collect the CH4

produced and either pipe it directly into the gas supply network or use it on-site for electricity generation and space

heating. Such use of landfill CH4

provides the double climate benefit of avoided CH4

emissions and substitution of fossil

fuels129. An extension of this technology is the use of anaerobic digestion of manure, sewage and other organic wastes to

maximize methanogenesis for methane collection and use. Such optimized systems also help to avoid the more diffuseemissions of nitrous oxide (N

2O) and CH

4to the atmosphere that occur when such wastes are applied directly to soils130.

For liquid biofuels generated from agricultural crop and residue feedstocks, microorganisms are again at the heart of

current efforts to increase production and reduce fossil fuel use28,131. Suggested solutions to some of these problems

include the use of cellulosiccrop and forest residues as the feedstock for biofuel production: recent advances include

the discovery of a fungus that can convert woody material into biodiesel132 and the production of ethanol by a modified

Escherichia coli133. Such discoveries have prompted further optimism that extant or engineered microorganisms can be

used to improve the net climate benefits of biofuels134. Similarly, the production of algal biomass under controlled

conditions and its subsequent conversion to biodiesel or ethanol also helps to avoid the land-use changes, food price

increases and N2O penalties that are associated with many first-generation biofuels such as corn ethanol 135.

Figure 3 | A amw uu a ma a a

a . It is important to understand the responses of individual

microbial species and whole microbial communities, as well as their interactions with

other soil biota and plants, to single climatic variables (such as increased levels of

carbon dioxide (CO2) and changes in temperature and precipitation) and in

multifactorial experimental conditions. This approach should be then tested in

contrasting ecosystems differing in climatic, nutritional, chemical and physical

properties. Such an integrated approach is essential for gaining a mechanistic

understanding of microbial adaptation and feedback responses to individual and

interacting global changes. This understanding then can be exploited to predict

the feedback response at the ecosystem level using various climate models.

R E V I E W S




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to incorporate icroia data (ioa, conity,dierity and actiity) into ciate ode to redcencertainty and to iproe etiation and prediction.Fifth, we need to etter ndertand the effect of ciatechange on aoe-grond and eow-grond interactionand ntrient cycing, a we a the roe of thee interac-tion in odating the repone of ecoyte to goachange. Finay, we need to deeop a fraework aedon the aoe fie point to potentiay anage natraicroia yte to enhance caron eqetrationand/or redce net greenhoe ga eiion.

To anwer the aoe chaenge, we need to e aninterdicipinary approach that incde icroiaecoogy, enironenta genoic, oi and pant ci-ence, and ecoyte odeing. There hae een -tantia adanceent in the technoogie that can eed to exaine icroia conitie and to reatethe to ecoyte fnction (BOx 3). Thee technoogiehod e appied to tdy how particar taxa repondto indiida and tipe ciate ariae and howch repone infence ecoyte fnction (FIG. 3).

There i aready oe eidence of icroia contro ofgreenhoe ga fx14,118, and it ha een hown that eenhort-ter eaona change in caron fx i reated tohift in icroia conitie118. Howeer, frthertdie are needed acro ecoyte type, and a et-ter echanitic ndertanding of fndaenta ecoy-te procee i reqired to predict the agnitde of

effect ing ciate ode119,120 and to redce ncer-taintie in prediction. Thi can e achieed ing twocopeentary approache: a redctionit approach,in which the repone of indiida taxa or coni-tie i teted eparatey for each enironenta ariae(increaed teperatre, precipitation and CO

2concen-

tration) to proide iportant echanitic inforation;and a tifactoria approach that ao conider trophicinteraction to accont for the interactie (ynergitic orantagonitic) effect of ariae. Recenty, attept haeeen ade to incorporate icroia data (ioa, andenzye and growth kinetic) into ciate ode14,118.Howeer, to frther iproe prediction, we need toincorporate data on icroia dierity, conitytrctre and phyioogica capaiitie of ario taxa.Ony after we hae ch an iproed ndertanding oficroia repone can a fraework on anageent oficroia yte for redced greenhoe ga eiione deeoped.

microorgani cod either greaty hep in ciatechange itigation, or proe diatro y exacerating

anthropogenic ciate change throgh poitie-feedackechani. No acadeic artice i copete withot aca for ore reearch, t edo i there an area that of icroioogy and ciate change that rgentyreqire o ch ore reearch effort and that ha och at take. microorgani ay e ot of ight, twe cannot afford for the to e ot of ind.

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AcknowledgementsThe authors thank C. Campbell, G. Grelet and C. Macdonald

for detailed discussions and comments on the manuscript.

P.S. holds a Royal Society Wolfson Research Merit Award.

Competing interests statementThe authors declare no competing financial interests.

FURTHER INFORMATIONBrajesh K. Singhs homepage:

http://www.macaulay.ac.uk/molecularmicrobiology

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