24Effectivenessofecologicalrescueforaltered

ORIGINALARTICLEEffectivenessofecologicalrescueforalteredsoilmicrobialcommunitiesandfunctionsKadiyaCalderón1,3,AyméSpor1,3,Marie-ChristineBreuil1,DavidBru1,FlorianBizouard1,CyrilleViolle2,RomainLBarnard1andLaurentPhilippot11Agroécologie,AgroSupDijon,INRA,UniversitéBourgogneFranche-Comté,Dijon,Franceand2CNRS,Centred’EcologieFonctionnelleetEvolutive,UMR5175,MontpellierCedex5,FranceSoilecosystemsworldwidearesubjectedtomarkedmodificationscausedbyanthropogenicdisturbancesandglobalclimatechange,resultinginmicrobialdiversitylossandalterationofecosystemfunctions.Despitethepaucityofstudies,restorationecologyprovidesanappropriateframeworkfortestingthepotentialofmanipulatingsoilmicrobialcommunitiesfortherecoveryofecosystemfunctioning.WeusedareciprocaltransplantdesigninexperimentallyalteredmicrobialcommunitiestoinvestigatetheeffectivenessofintroducingmicrobialcommunitiesindegradedsoilecosystemstorestoreN-cyclefunctioning.MicrobialdiversitylossresultedinalternativecompositionalstatesassociatedwithimpairedN-cyclefunctioning.Here,theadditionofcomplexmicrobialcommunitiestothesealteredcommunitiesrevealedapivotalroleofdeterministiccommunityassemblyprocesses.ThediversityofsomealternativecompositionalstateswassuccessfullyincreasedbutwithoutsignificantrestorationofsoilN-cyclefunctioning.However,inthemostdegradedalternativestate,theintroductionofnewmicrobialcommunitiescausedanoveralldecreaseinphylogeneticdiversityandrichness.Thesuccessfulsoilcolonizationbynewlyintroducedspeciesforsomecompositionalstatesindicatesthatpriorityeffectscouldbeoverriddenwhenattemptingtomanipulatemicrobialcommunitiesforsoilrestoration.Altogether,ourresultshowedconsistentpatternswithinrestorationtreatmentswithminoridiosyncraticeffects.Thissuggeststhepredominanceofdeterministicprocessesandthepredictabilityofrestorationtrajectories,whichcouldbeusedtoguidetheeffectivemanagementofmicrobialcommunityassemblagesforecologicalrestorationofsoils.TheISMEJournaladvanceonlinepublication,24June2016;doi:10.1038/ismej.2016.86IntroductionSoilmicroorganismsformoneofthelargestbiodi-versityreservoirsonearth.Theyalsohaveessentialrolesinecosystemfunctionssuchasbiogeochemicalcycling(Falkowskietal.,2008;Waggetal.,2014).However,biodiversitylossisnowrecognizedasoneofthemainthreatsconfrontedbysoils(CommissionoftheEuropeanCommunity,2006),withincreasingevidencethatthiscanalterecosystemfunctioningandstability(BardgettandvanderPutten,2014;Waggetal.,2014).Onlyrecently,soilmicroorgan-ismshavebecomeofinterestinrestorationecologyaskeysoilengineersthatmaybemanipulatedtore-establishbiodiversityandfunctionsindegradedecosystems(Youngetal.,2005;Heneghanetal.,2008).Nevertheless,mostworkinrestorationecologyisstillfocusedonplants(KardolandWardle,2010).Microorganismsareatbestusedtostudythebelow-groundimpactofre-introducingflora(Smithetal.,2003)ortopromoteplantestablishmentthroughsymbioticinteractions(Requenaetal.,2001).Forexample,Kardoletal.(2008)investigatedwhethertheintroductionofmicroorganismsbyspreadingsoilfromadonorlatesuccessionsitewouldfacilitategrasslandrestoration.Theunsuccessfulestablish-mentoflatesuccessionalplantspecieswasattrib-utedtopoorcolonizationofthesoilbytheintroducedmicroorganisms.Ontheotherhand,Smithetal.(1998)foundthatinoculationwitharbuscularmycorrhizalfungipromotesthedevelop-mentofearlysuccessionaltallgrassprairiecommu-nities.Thesediscrepanciesillustratetheneedforstudiesusingamicrobialcommunity-widerestora-tionapproachtoassesstheestablishmentandsurvivalofmicroorganismsforsuccessfulecologicalrestorationofsoils.Restoringsoilfunctioningischallenging,asmicro-bialecosystemdynamicsarecomplex,nonlinearandpartlyunpredictable(Nemergutetal.,2013).Histor-icalcontingency,knownaspriorityeffects,variesbetweenspeciesandenvironmentsandcanpreventcolonizationbylate-arrivingspecies(VannetteandCorrespondence:LPhilippot,Agroécologie,AgroSupDijon,INRA,UniversitéBourgogneFranche-Comté,Dijon,21000,France.E-mail:[e-mail]6March2016;revised29April2016;accepted10May2016TheISMEJournal(2016),1–12©2016InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/16).Theoccurrenceofalternativestablestatesduringcolonizationprocessescanalsoimpedethecompleterecoveryofcommunitystructureandecosystemfunctions,asshowninothersystems(Moreno-Mateosetal.,2012).However,ourunder-standingoftheroleofspeciesinteractionsandofidiosyncraticeffectsintherestorationtrajectoryofmicrobialbiodiversityandfunctioningislimiteddespitebeingcrucial(Harris,2009;Laughlin,2014).Here,weexaminedtheeffectivenessofintroducingmicrobialcommunitiesinalteredcommunities,torecoversoilbiodiversityandfunctioning.Wehypothesizedthatpriorityeffectsandthebiodiver-sitylevelofthealready-establishedcommunitiesbutalsoofthenewlyintroducedcommunitiesareofimportanceforcommunityassemblyandsuccessfulrestoration.Theinfluenceoftherelatednessbetweenthealready-establishedcommunitiesandthenewlyintroducedcommunitiesonpriorityeffectswasassessedusingareciprocaltrans