70Suppressionoftheactivityofarbuscularmycor

TheISMEJournal(2018)12:1296–1307●StephanieJWatts-Williams2●ErikJJoner3●FabioBattini4●AikateriniEfthymiou1●CarlaCruz-Paredes1●OleNybroe1●IverJakobsen1Received:8October2017/Revised:28November2017/Accepted:12December2017/Publishedonline:30January2018©TheAuthor(s)2018.ThisarticleispublishedwithopenaccessAbstractArbuscularmycorrhizalfungi(AMF)coloniserootsofmostplants;theirextra-radicalmycelium(ERM)extendsintothesoilandacquiresnutrientsfortheplant.TheERMcoexistswithsoilmicrobialcommunitiesanditisunresolvedwhetherthesecommunitiesstimulateorsuppresstheERMactivity.ThisworkstudiedtheprevalenceofsuppressedERMactivityandidentifiedmaincomponentsbehindthesuppression.ERMactivitywasdeterminedbyquantifyingERM-mediatedPuptakefromradioisotope-labelledunsterilesoilintoplants,andcomparedtosoilphysicochemicalcharacteristicsandsoilmicrobiomecomposition.ERMactivityvariedconsiderablyandwasgreatlysuppressedin4of21soils.Suppressionwasmitigatedbysoilpasteurisationandhadadominatingbioticcomponent.AMF-suppressivesoilshadhighabundancesofAcidobacteria,andotherbacterialtaxabeingputativefungalantagonists.SuppressionwasalsoassociatedwithlowsoilpH,butthiseffectwaslikelyindirect,astherelativeabundanceof,e.g.,Acidobacteriadecreasedafterliming.Suppressioncouldnotbetransferredbyaddingsmallamountsofsuppressivesoiltoconducivesoil,andthusappearedtoinvolvethecommonactionofseveraltaxa.ThepresenceofAMFantagonistsresemblesthephenomenonofdisease-suppressivesoilsandimpliesthatecosystemservicesofAMFwilldependstronglyonthespecificsoilmicrobiome.IntroductionSoilmicroorganismsarefundamentalforsoilhealthandprovideecosystemservicesthatareessentialforplantpro-duction[1,2].Societalawarenessofagriculturalsustainabilityiscontinuouslygrowing,makingitincreasinglyimportanttounravelthebioticandabioticfactorsindifferentsoilsthatsupportthebeneficialcomponentsoftheirmicrobiome.Arbuscularmycorrhizalfungi(AMF)arepresentinmostsoilsandformsymbioticassociationswithmajorityofcropplants[3].Themycorrhizalsymbiosishasmultiplebeneficialimpactsonnutrientcyclingandplantstresstolerance[4]andrepresentsunder-exploitedpotentialtoincreaseglobalfoodsecurity[5].Hence,awell-developedextra-radicalmycelium(ERM)thatproliferatesinthebulksoilbeyondtherhizosphereisimportantforplantPuptake,whiletheAMFdependontheirhostplantforcarbonnutrition[6,7].ThelargesurfaceareaoftheERMprovidesnutrient-richnichesforcolonisationandgrowthofothersoilmicroorganisms,inparticularbacteria[8].Hence,severalmembersoftheGlomeraceaeincreasetheabundanceofFirmicutes,StreptomycetesandmembersofthefamilyOxalobacteraceaeonhyphae,orinsoilaffectedbyhyphae[9–11].Thehyphae-associatedbacteriamayinreturnaffecttheAMFasexemplifiedbymycorrhizalhelperbacteriathatpromoteAMFhyphalgrowthandrootcolonisation[12,13].Yet,evenbacteriawithsuppressiveeffectshavebeenidentified[14,15].TheseobservationssupportthenotionthatsoilharboursbothstimulatoryandantagonisticbacteriatowardsAMF.However,weknowNannaBSvenningsenandStephanieJWatts-Williamscontributedequallytothiswork.*[e-mail]1DepartmentofPlantandEnvironmentalSciences,UniversityofCopenhagen,Frederiksberg,Denmark2SchoolofAgriculture,FoodandWine,UniversityofAdelaide,GlenOsmondSAAustralia3NorwegianInstituteforBioeconomyResearch,ÅsAkershus,Norway4DepartmentofAgriculture,FoodandEnvironment,UniversityofPisa,Pisa,ItalyElectronicsupplementarymaterialTheonlineversionofthisarticle()containssupplementarymaterial,whichisavailabletoauthorizedusers.1234567890();,:relativelylittleabouthowAMFhyphaeandbacteriainteractinsoiloutsidetherhizosphere,eventhoughthosehyphaerepresentthemajornichewhereinteractionswithsoilbacteriacantakeplace[10].Scatteredevidencesuggeststhatnaturalsoilscansup-pressAMFcolonisationandplantgrowthresponses([16];seealsoreviewbyNehletal.[17]).Inonestudy,theadditionofabacterialsoilfiltratedecreasedthelengthoftheERM[18].Furthermore,thecontributionoftheERMpathwaytoplantPuptakewasnegligibleinoneoutoffiveunsterilesoils,whichotherwiseproducedsimilarlevelsofrootcolonisation[19].Theseobservationsledustospec-ulatethatsoilsmaybeeithersuppressiveorconducivetoERMactivity.Whereassoilssuppressivetowardsplantpathogenicfungi,so-called‘disease-suppressivesoils’,arewell-known[20],itremainsunknownwhethersoil-inducedsuppressionofAMFiscommon.Diseasesuppressionmayberelatedtothetotalmicrobialcommunityinthesoil(generalsuppression),whileinothercases,suppressioniscausedbythespecificeffectsofselectedsoilmicroorgan-isms(specificsuppression)[21].Thus,soilpasteurisationstronglyreducesbothgeneralandspecificdiseasesup-pressionofsoils[22,23],whiletransferabilityofsmallsoilvolumesisakeycharacteristicofspecificsuppression[21].Importantly,suppressiveeffectsmediatedbycomponentsofthesoilmicrobiotamightwellbeconfoundedbyspecificcharacteristicsofthesoilphysicochemicalenvironmentsuchaslowtemperature[24]orlowpH[25,26].Microbialcommunityanalysishasrevealedthatsu