31Biophysicalprocessessupportingthediversity

FEMSMicrobiologyReviews,fux039doi:10.1093/femsre/fux039ReviewarticleREVIEWARTICLEBiophysicalprocessessupportingthediversityofmicrobiallifeinsoilRobinTeconandDaniOr∗SoilandTerrestrialEnvironmentalPhysics,DepartmentofEnvironmentalSystemsScience,ETHZ¨urich,Universit¨atstrasse16,8092Z¨urich,Switzerland∗Correspondingauthor:InstituteofBiogeochemistryandPollutantDynamics,ETHZurich,Universit¨atstrasse16,8092Z¨urich,Switzerland.Tel:[phone];Fax:[phone];E-mail:[e-mail]:Soilmicroorganismsliveincomplexporespaceswherenutrientheterogeneityandwaterdynamicsplayafundamentalroleinshapingtheirecology,diversityandfunctionsatallscales.Editor:StaffanKjellebergABSTRACTSoil,thelivingterrestrialskinoftheEarth,playsacentralroleinsupportinglifeandishometoanunimaginablediversityofmicroorganisms.Thisreviewexploreskeydriversformicrobiallifeinsoilsunderdifferentclimatesandland-usepracticesatscalesrangingfromsoilporestolandscapes.Wedelineatespecialfeaturesofsoilasamicrobialhabitat(focusingonbacteria)andtheconsequencesformicrobialcommunities.Thisreviewcoversrecentmodelingadvancesthatlinksoilphysicalprocesseswithmicrobiallife(termedbiophysicalprocesses).Readersareintroducedtoconceptsgoverningwaterorganizationinsoilporesandassociatedtransportpropertiesandmicrobialdispersionrangesoftendeterminedbythespatialorganizationofahighlydynamicsoilaqueousphase.Thenarrowhydrologicalwindowsofwettingandaqueousphaseconnectednessarecrucialforresourcedistributionandlongerrangetransportofmicroorganisms.Feedbacksbetweenmicrobialactivityandtheirimmediateenvironmentareresponsibleforemergenceandstabilizationofsoilstructure—thescaffoldingforsoilecologicalfunctioning.Wesynthesizeinsightsfromhistoricalandcontemporarystudiestoprovideanoutlookforthechallengesandopportunitiesfordevelopingaquantitativeecologicalframeworktodelineateandpredictthemicrobialcomponentofsoilfunctioning.Keywords:soilmicrobiology;microbialecology;vadosezone;soilphysics;microbialinteractions;bacterialcommunitiesINTRODUCTIONMicroorganismshavebeennamed‘stewardsofthebiosphere’(JanssonandFredrickson2010),andperhapsnowhereelseontheplanetisthistitlemorefittingthaninsoil.Globally,soilmi-crobesarethedriversofkeybiogeochemicalcyclesinvolvingcar-bon,nitrogen,phosphorus,ironandmore.Theiractivitycon-tributestoawidevarietyofsoilecosystemfunctions,includingthecyclingoforganicmatterandnutrients,andtheemergenceofsoilstructure.Thesefunctionsaretightlyassociatedwithessentialecosystemgoods(e.g.food,fiber,wood)andservices(regulatinggreenhousegasemissions,sequestratingcarbon,assuringwaterquality,mitigatingerosion,attenuatingpol-lutants,suppressingpathogensandpromotingplantgrowth)(Brussaard2012).Microbialactivityisthusessentialtoahealthyandfertilesoil.Thisisacrucialfactatatimewherethreatstosoilqualityandfertilityaremountingatanalarmingrate.ThecentralityofsoilservicestolifeontheplanetpromptedtheFoodandAgriculturalOrganizationoftheUnitedNationstodeclare2015theinternationalyearofsoils(FAO2015)inanefforttoraiseglobalawarenessregardingsoil’sroleandtheurgentneedtopre-servethisthinlayeroftheterrestrialsurfacethatteemswithlife(Wallander2014).Received:17November2016;Accepted:10July2017CFEMS2017.ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionNon-CommercialLicense(),whichpermitsnon-commercialre-use,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited.Forcommercialre-use,[e-mail]12FEMSMicrobiologyReviewsSomeportraysoilasanunfavorablehabitatformicrobiallifeduetoitsharshandfluctuatingenvironmentalconditions,yetevidencesuggeststhatmicroorganismsthriveinsoils(Stotzky1997).Onegramofsurfacesoilmaycontain109–1010prokaryoticcells(bacteriaandarchaea),104–107protists,∼100moffungalhyphaeand108–109viruses(Srinivasiahetal.2008;Batesetal.2013;BardgettandvanderPutten2014;BradyandWeil2014).Thesevaluestranslatetoprokaryoticbiomassexceeding5tonsperhectareinsomesoils,withfungalbiomassrangingfrom1to15tons(BradyandWeil2014).Soilsalsohosttremendousge-neticdiversity:communityDNAreassociationmethods(TorsvikandØvre˚as2007)haveshownthatthetotalgenomicdiversityofbacterialcommunitiesfromunperturbedpasturesoilsmayexceedthediversityfoundinaquaticcommunitiesbythreeor-dersofmagnitude,withthehighestdiversityestimatesrangingfromthousandstomillionsofdistinctprokaryoticspecies(orOTUs,operationaltaxonomicunits)pergramofsoil(TorsvikandØvre˚as2002;Torsvik,Øvre˚asandThingstad2002;Gans,Wolin-skyandDunbar2005;SchlossandHandelsman2006;Roeschetal.2007).Moreover,afewgramsofsoilcontainhundredsoffungalandprotistanspecies(Batesetal.2013;Peay,KennedyandTalbot2016).Presently,thetrueextentofmicrobialdiver-sitycanonlybeestimated,notyetmeasured(LoceyandLennon2016;Peay,KennedyandTalbot2016).Ourlimitedknowledgeofbiodiversityanditslinkswithspecificecosystemfunctionshasmotivatedseveralsoilmetagenomicsinitiativesinthepastfewyears(Nesmeetal.2016),notablytheTerraGenomeconsor-tiumin2009(Vogeletal.2009),theEarthMicro