62Photoautotrophicorganismscontrolmicrobialab

TheISMEJournal●AlexandraTamm1●DianmingWu1,2●JenniferCaesar3●MartinGrube4●BettinaWeber1Received:13September2017/Revised:21December2017/Accepted:10January2018©TheAuthor(s)2018.ThisarticleispublishedwithopenaccessAbstractBiologicalsoilcrusts(biocrusts)coverabout12%oftheEarth’slandmasses,therebyprovidingecosystemservicesandaffectingbiogeochemicalfluxesonaglobalscale.Theycomprisephotoautotrophiccyanobacteria,algae,lichensandmosses,whichgrowtogetherwithheterotrophicmicroorganisms,formingamodelsystemtostudyfacilitativeinteractionsandassemblyprinciplesinnaturalcommunities.Biocrustscanbeclassifiedintocyanobacteria-,lichen-,andbryophyte-dominatedtypes,whichreflectstagesofecologicalsuccession.Inthisstudy,weexaminedwhetherthesecategoriesincludeashiftinheterotrophiccommunitiesandwhetherthismaybelinkedtoalteredphysiologicalproperties.WeanalyzedthemicrobialcommunitycompositionbymeansofqPCRandhigh-throughputampliconsequencingandutilizedfluxmeasurementstoinvestigatetheirphysiologicalproperties.Ourresultsrevealedthatonce16Sand18SrRNAgenecopynumbersincrease,fungibecomemorepredominantandalphadiversityincreaseswithprogressingsuccession.Bacterialcommunitiesdifferedsignificantlybetweenbiocrusttypeswithashiftfrommoregeneralizedtospecializedorganismsalongsuccession.CO2gasexchangemeasurementsrevealedlargerespirationratesoflatesuccessionalcrustsbeingsignificantlyhigherthanthoseofinitialbiocrusts,anddifferentsuccessionalstagesshoweddistinctNOandHONOemissionpatterns.Thus,ourstudysuggeststhatthephotoautotrophicorganismsfacilitatespecificmicrobialcommunities,whichthemselvesstronglyinfluencetheoverallphysiologicalpropertiesofbiocrustsandhencelocaltoglobalnutrientcycles.IntroductionIndrylandregions,wherevascularvegetationisusuallyquitesparse,theuppermostmillimetersofthesoildevelopbiologicalsoilcrusts(biocrusts),whichcomprisebryo-phytes,algae,fungi(includinglichens),andbacteria(includingcyanobacteria)invaryingproportions[1,2].Multicellularorganismsinthesecommunitiesarepoikilo-hydric[3,4],beingrapidlyreactivatedoncewaterisavailable[5].Thesecharacteristicsallowthemtooutlastperiodsofdroughtandcolonizeextremeenvironments[6].Accordingtothedominatingphotoautotrophicorganism,biocrustsareclassifiedintocyanobacteria-,lichen-,andmoss-dominatedtypes[1,7,8].Thesetypesgenerallyreflectdifferentsuccessionalstages[9],withthecourseandspeedofsuccessionbeinginfluencedbyclimate,soilandtheprecedingdisturbanceevent[10–14].Duringtheearlystagesofbiocrustformation,whencyanobacteriaarefewinnumber,heterotrophicdiazotrophsmaycontributetoN2-fixation[15].Underfavorableenvironmentalconditionscyanobacteria-dominatedbiocrustsmaydevelopintolichen-andbryophyte-dominatedbiocrusts[2].Itiswellknownthatfacilitationplaysamajorroleincommunitysuccession[16,17].Earlystagesinthesuccessionofbio-crustscansufferfromnutrientlimitationsorflourishfromsupplementarynutrients,whichmaykick-starttheprocessofdevelopment[17–19].StefanieMaierandAlexandraTammcontributedequallytothiswork.*[e-mail]*[e-mail]1MaxPlanckInstituteforChemistry,MultiphaseChemistry,Mainz,Germany2KeyLaboratoryofGeographicInformationSciences,MinistryofEducation,SchoolofGeographicSciences,EastChinaNormalUniversity,Shanghai,China3DepartmentofAgriculture&FoodSciences,UniversityofAppliedSciences,Neubrandenburg,Germany4InstituteofPlantSciences,UniversityofGraz,Graz,AustriaElectronicsupplementarymaterialTheonlineversionofthisarticle()containssupplementarymaterial,whichisavailabletoauthorizedusers.1234567890();,:Biocrustshavebeendemonstratedtoplayacentralroleinmanydrylandecosystemprocesses,astheyformthezoneofnutrientaccumulationandtransformation[2].Bypho-tosyntheticuptakeofatmosphericCO2andfixationofatmosphericN2[20],biocrustsserveaselementalsinksintheenvironment.Thesenutrientsserveasfoodsourceforplants,animalsandotherorganismsinoftenstronglydepleteddrylandecosystems[21–23].Thecontributionsofbiocruststocarbonandnitrogencyclesmaybesignificant,ascryptogamicgroundcovers,includingbiocrusts,takeup590Tga−1ofcarboninsteppesanddeserts,whilethebiologicalnitrogenfixationaddsupto25.7Tga−1ofnitrogen[22].Biocrustsareknowntoaffectsoilcarboncycling,asCastillo-Monroyetal.[24]foundthat42%oftheannualsoilrespirationofadrylandecosystemwasattributabletobiocrust-dominatedareas.InKalaharisoils,CO2effluxesresultedfromcyanobacteriaandheterotrophicmicroorganismsinthebelow-crustsoil,whichwereacti-vatedbyrainfall[25,26].Theamountofcarbonminer-alizedandhencethequantityofCO2emissionsisalsodependentontheamountofavailablecarbon[27–32].Thus,thequestionarisesifanalterationofthemicrobialcom-munitywillaffecttherespirationrateandphysiologicalpropertiesofdifferenttypesofbiocrusts.Moststudiesarefocusedontheinteractionbetweenafewpairsofspecies,andneitherthecomplexityofnaturalcommunities,suchasbiocrusts,northepotentialrolesofbioticinteractio