53Consistentresponsesofsoilmicrobialtaxonomi

RESEARCHOpenAccessConsistentresponsesofsoilmicrobialtaxonomicandfunctionalattributestomercurypollutionacrossChinaYu-RongLiu1,2,3*,ManuelDelgado-Baquerizo4,5,LiBi2,JunZhu3andJi-ZhengHe2,6AbstractBackground:Theecologicalconsequencesofmercury(Hg)pollution—oneofthemajorpollutantsworldwide—onmicrobialtaxonomicandfunctionalattributesremainpoorlyunderstoodandlargelyunexplored.UsingsoilsfromtwotypicalHg-impactedregionsacrossChina,here,weevaluatedtheroleofHgpollutioninregulatingbacterialabundance,diversity,andco-occurrencenetwork.WealsoinvestigatedtheassociationsbetweenHgcontentsandtherelativeabundanceofmicrobialfunctionalgenesbyanalyzingthesoilmetagenomesfromasubsetofthosesites.Results:WefoundthatsoilHglargelyinfluencedthetaxonomicandfunctionalattributesofmicrobialcommunitiesinthetwostudiedregions.Ingeneral,Hgpollutionwasnegativelyrelatedtobacterialabundance,butpositivelyrelatedtothediversityofbacteriaintwoseparateregions.WealsofoundsomeconsistentassociationsbetweensoilHgcontentsandthecommunitycompositionofbacteria.Forexample,soiltotalHgcontentwaspositivelyrelatedtotherelativeabundanceofFirmicutesandBacteroidetesinbothpaddyanduplandsoils.Incontrast,themethylmercury(MeHg)concentrationwasnegativelycorrelatedtotherelativeabundanceofNitrospiraeinthetwotypesofsoils.IncreasesinsoilHgpollutioncorrelatedwithdrasticchangesintherelativeabundanceofecologicalclusterswithintheco-occurrencenetworkofbacterialcommunitiesforthetworegions.Usingmetagenomicdata,wewerealsoabletodetecttheeffectofHgpollutiononmultiplefunctionalgenesrelevanttokeysoilprocessessuchaselementcyclesandHgtransformations(e.g.,methylationandreduction).Conclusions:Together,ourstudyprovidessolidevidencethatHgpollutionhaspredictableandsignificanteffectsonmultipletaxonomicandfunctionalattributesincludingbacterialabundance,diversity,andtherelativeabundanceofecologicalclustersandfunctionalgenes.OurresultssuggestanincreaseinsoilHgpollutionlinkedtohumanactivitieswillleadtopredictableshiftsinthetaxonomicandfunctionalattributesintheHg-impactedareas,withpotentialimplicationsforsustainablemanagementofagriculturalecosystemsandelsewhere.Keywords:Soilmicrobialcommunity,Co-occurrencenetwork,Functionalgene,Metagenomics,MercurypollutionBackgroundEnvironmentalpollutionresultingfromhumanactivitieshasagreatimpactonthebiodiversityandfunctioningofterrestrialandaquaticecosystemsandisamajorthreatforhumanhealthacrosstheglobe[1–4].Importantly,recentstudiessuggestedthatchangingclimateexacerbatesglobalmercury(Hg)pollutionbyreleasinghistoricallystockedHginthepermafrost[5,6].SuchathreatisofglobalconcernasHgcanbetransportedglo-bally[7].TheelevatedHginputsintoenvironmentscouldhavesignificanteffectsonsoilbiodiversityandtheirassociatedecosystemfunctions[8,9].Studiescon-ductedatthelocalscaleseemedtosupporttheideathatHgpollutioncanaltersoilmicrobialcommunities[10–12].Moreover,previousworkbasedonshort-termincu-bationexperimentsdemonstratedthatHgamendmentscanalterthesoilmicrobiomeanditsecologicalfunc-tions[13,14].However,muchlessisknownontheroleofHgpollutioninshapingthetaxonomicandfunctional*Correspondence:[e-mail]1StateKeyLaboratoryofAgriculturalMicrobiology,HuazhongAgriculturalUniversity,Wuhan430070,People’sRepublicofChina2StateKeyLaboratoryofUrbanandRegionalEcology,ResearchCenterforEco-EnvironmentalSciences,ChineseAcademyofSciences,Beijing100085,ChinaFulllistofauthorinformationisavailableattheendofthearticle©TheAuthor(s).2018OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCommonsAttribution4.0InternationalLicense(),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinktotheCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver()appliestothedatamadeavailableinthisarticle,unlessotherwisestated.Liuetal.Microbiome(2018)6:183[15,16].Suchecologicalclustersareexpectedtohavemultipleimplicationsforthemaintenanceofsoilfertility,decomposition,andeco-logicalservicesinterrestrialenvironments[17–19].Thereasonisthatdifferentmicrobialecologicalclustersoftenfollowveryspecificenvironmentalpreferences.Forexample,taxawithinsomeecologicalclustershavebeenfoundtostronglycorrelatewithloworhighpH,mesicoraridecosystem,andnutrientavailabilityandprocessesrates[15].However,despitetheimportanceoftheseeco-logicalclustersfortheunderstandingofthesoilmicro-biome,theirresponsetolong-termfieldHgpollutionremainslargelyunexplored[20].IncreasingHgconcen-trationscouldpotentiallyimpacttherelativeabundanceofmajorecologicalclusterswithimplicationsforecosys-temfunctioning.However,empiricalevidenceforsuchassumptionsiscurrentlylac