37Themicrobialecologyofpermafrost

Anestimated25%ofthelandareaonEarthisunder-lainbypermafrost.Theclassicdefinitionofpermafrostissoilthathasremainedfrozen(thatis,below0°C)foratleast2consecutiveyears.However,someancientper-mafrosthasremainedfrozenduringseveralperiodsofglaciation.Infact,permafrostcanbeupto1–3millionyearsoldintheArcticandevenolderinAntarctica.Dependingonthelocationandclimaticconditionsatthetime,thelandsurfacethatisnowpermafrostwasnotinitiallyfrozenandmayhavebeencoveredwitheithervegetationorwater.Someoftheplantandanimalmate-rialandmicrobialbiomassthataccumulatedduringtheCO2-richatmosphereandwarmperiodsinthehistoryoftheEarthbecamepreservedinthepermafrostdur-ingcoolingandglaciationevents.Althoughtheplantsandanimalsthatbecametrappedduringthistransitionmettheirdemise,currentevidencesuggeststhatmanyofthemicroorganismswereabletoadaptandevenremainactive.Recentresearchsuggeststhatpermafrostregionswillbeaffectedbyincreasesinglobaltemperaturesandsubsequentpermafrostthawwillprobablynotonlyresultinincreasedactivationofindigenouspermafrostmicro-organismsbutwillalsounlockconsiderableamountsofcarbonandnutrientsthatcanbeusedfortheiracceler-atedgrowth.InthisReview,wesummarizeourcurrentknowledgeofthemicrobialecologyofpermafrost.PermafrostregionsaroundtheglobePermafrostisastructurallyheterogeneoushabitat,andtherearedifferenttypesofpermafrostindiffer-entgeographicallocations(FIG.1).Moreover,therearedifferenceswithinlocationswithrespecttopermafroststructure,organic-mattercontentandage.Permafrostistraditionallyclassifiedaseithercontinuousordiscon-tinuousandischaracterizedbytheamountandtypeoficethatitcontains1.Ingeneralterms,permafrostisdifferentfromallotherhabitatsandcontainsfeaturesthataredifferentfromunfrozensoil,sedimentandrock.Permafrostisoverlainbyaso-called‘activelayer’thathasbeenexposedtoseasonalfreeze–thawcycles.Theactivelayercanvaryinthicknessfromafewcentimetrestoseveralmetres.Owingtoglobalwarming,thedepthoftheactivelayerhasbeenshowntobeincreasinginmanylocationsoverthepastfewdecades,resultinginasubsequentdeclineintheunderlyingpermafrost1–4.Duringglacialperiods,largeregionsoftheNorthAmericanandScandinavianArcticwerecoveredwithice,andremnantsofthisiceremaininGreenlandandthenortheasternCanadianArctic.Bycontrast,largeregionsofthepermafrostareasinAsiaandAlaskawerenotrecentlyglaciatedbutarefrozennonetheless.Theseincludeperenniallyfrozenandloess-like(thatis,wind-blown)depositionscalledYedomathatcompriseaspe-cifictypeofpermafrostformationthatismainlyfoundinNortheastSiberiaandisrichinorganicmatter(thatis,approximately2%carbon)withanicecontentof50–90%thatcanbehundredsofmetresthick4.PeatdepositsarealsocommoninthesouthernpartoftheArcticperma-frostregion.Substantialvariationshavebeenobservedinpermafrosttemperatures,rangingfrom−2°Cto−10°CintheArctic,withsomesitesbelow−15°C(REF. 2).Althoughonly0.36%(49,800km2)oftheAntarcticregionisice-free,permafrostispresentbeneathalmostallofthisarea3.However,therearelargedifferencesinwateravailabilityacrossthecontinent;forexample,theRossSearegionhasastrongmoisturegradient,inThemicrobialecologyofpermafrostJanetK.Jansson1–5andNeslihanTas¸1Abstract|PermafrostconstitutesamajorportionoftheterrestrialcryosphereoftheEarthandisauniqueecologicalnicheforcold-adaptedmicroorganisms.Thereisarelativelyhighmicrobialdiversityinpermafrost,althoughthereissomevariationincommunitycompositionacrossdifferentpermafrostfeaturesandbetweensites.Somemicroorganismsareevenactiveatsubzerotemperaturesinpermafrost.Anemergingconcernistheimpactofclimatechangeandthepossibilityofsubsequentpermafrostthawpromotingmicrobialactivityinpermafrost,resultinginincreasedpotentialforgreenhouse-gasemissions.ThisReviewdescribesnewdataonthemicrobialecologyofpermafrostandprovidesaplatformforunderstandingmicrobiallifestrategiesinfrozensoilaswellastheimpactofclimatechangeonpermafrostmicroorganismsandtheirfunctionalroles.1EcologyDepartment,EarthSciencesDivision,LawrenceBerkeleyNationalLaboratory,OneCyclotronRoad,MS70A‑3317Berkeley,California94720,USA.2JointGenomeInstitute(JGI),2800MitchellDrive,WalnutCreek,California94598,USA.3JointBioEnergyInstitute(JBEI),5885HollisStreet,Emeryville,California94608,USA.4DanishCenterforPermafrost(CENPERM),UniversityofCopenhagen,OesterVoldgade10,DK‑1350Copenhagen,Denmark.5DepartmentofPlantandMicrobialBiology,UniversityofCalifornia,111KoshlandHall,Berkeley,California94720‑3102,USA.CorrespondencetoJ.K.J.e‑mail:[e-mail]:10.1038/nrmicro3262Publishedonline12May2014REVIEWS414|JUNE2014|VOLUME12©2014MacmillanPublishersLimited.AllrightsreservedYedomaApermafrosttypethatismainlyfoundinNortheastSiberia.Itischaracterizedbyhighlevelsoforganicmaterialandupto90%icecontent.Carbonthatistrappedinthispermafrostissuggestedtobesusceptibletomicrobialdecompositionfollowingthaw,resultinginthepotentialreleaseoflargequantitiesofgreenhousegasesintotheatmosphere.CryopegsPermafrostzonesthathavehighdissolved-solidscontents(forexample,ahighsaltconcentrationintheporewater),thusdepressingthefreezingpointofwater.TalikAlayerofunfrozengrou