66Thechemodiversityofpaddysoildissolvedorga

RESEARCHOpenAccessThechemodiversityofpaddysoildissolvedorganicmattercorrelateswithmicrobialcommunityatcontinentalscalesHong-YiLi1†,HangWang2†,Hai-TiaoWang3,4,Pei-YongXin5,Xin-HuaXu1,YunMa6,Wei-PingLiu1,Chang-YunTeng1,7,Cheng-LiangJiang1,7,Li-PingLou1,WyattArnold3,4,LaurenCralle3,4,Yong-GuanZhu8,Jin-FangChu5,JackAGilbert3,4*andZhi-JianZhang1,7,9*AbstractBackground:Paddysoildissolvedorganicmatter(DOM)representsamajorhotspotforsoilbiogeochemistry,yetweknowlittleaboutitschemodiversityletalonethemicrobialcommunitythatshapesit.Here,weleveragedultrahigh-resolutionmassspectrometry,amplicon,andmetagenomicsequencingtocharacterizethemoleculardistributionofDOMandthetaxonomicandfunctionalmicrobialdiversityinpaddysoilsacrossChina.WehypothesizedthatvariancesinmicrobialcommunitysignificantlyassociatewithchangesinsoilDOMmolecularcomposition.Results:WereportthatbothmicrobialandDOMprofilesrevealedgeographicpatternsthatwereassociatedwithvariationinmeanmonthlyprecipitation,meanannualtemperature,andpH.DOMmoleculardiversitywassignificantlycorrelatedwithmicrobialtaxonomicdiversity.AnincreaseinDOMmoleculescategorizedaspeptides,carbohydrates,andunsaturatedaliphatics,andadecreaseinthosebelongingtopolyphenolicsandpolycyclicaromatics,significantlycorrelatedwithproportionalchangesinsomeofthemicrobialtaxa,suchasSyntrophobacterales,Thermoleophilia,Geobacter,Spirochaeta,Gaiella,andDefluviicoccus.DOMcompositionwasalsoassociatedwiththerelativeabundancesofthemicrobialmetabolicpathways,suchasanaerobiccarbonfixation,glycolysis,lignolysis,fermentation,andmethanogenesis.Conclusions:Ourstudydemonstratesthecontinental-scaledistributionofDOMissignificantlycorrelatedwiththetaxonomicprofileandmetabolicpotentialofthericepaddymicrobiome.AbioticfactorsthathaveadistincteffectoncommunitystructurecanalsoinfluencethechemodiversityofDOMandviceversa.Decipheringtheseassociationsandtheunderlyingmechanismscanprecipitateunderstandingofthecomplexecologyofpaddysoils,aswellashelpassesstheeffectsofhumanactivitiesonbiogeochemistryandgreenhousegasemissionsinpaddysoils.Keywords:Dissolvedorganicmatter,Paddysoil,Chemodiversity,Microbialdiversity,FT-ICR-MSBackgroundPaddyfields,90%ofwhichareinAsia,feedmorethanhalfoftheworld’spopulation[1].Thecontinuousflood-inginbundedfieldsofcultivatedrice(Oryzasativa)uti-lizes24–30%oftheworld’sdevelopedfreshwaterresourcesandrepresentsoneofthemajorsourcesofinlandaquaticdissolvedorganicmatter(DOM)[1,2].HighconcentrationsandfluxesofDOMfromplantdeb-risduringfloodingseasonstriggermicrobialactivity,whileanaerobicconditionsstabilizeDOMagainstmicro-bialdecayviainteractionswithclaymineralsandironoxides[1,3].DOMplaysacentralroleinbiogeochem-icalprocessesinbothfloodedandunfloodedpaddysoils,aswellasanactiveroleintheglobalcarboncycle[1,4].Recently,theevidence-basedsoilcontinuummodelquestionedthesecondarysynthesisof“humicsub-stances,”orthe“humification,”andinterpretedorganicdebrisasauniquesourceofsoilorganicmatter(SOM)andDOM[5].Thistheoryemphasizedtheinherent*Correspondence:[e-mail];[e-mail];[e-mail]†Hong-YiLiandHangWangcontributedequallytothiswork.3TheMicrobiomeCenter,BiosciencesDivision,ArgonneNationalLaboratory,Lemont,IL60439,USA1CollegeofEnvironmentandNaturalResourceSciences,ZhejiangUniversity,866YuhangtangAve,Hangzhou310058,ChinaFulllistofauthorinformationisavailableattheendofthearticle©TheAuthor(s).2018OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCommonsAttribution4.0InternationalLicense(),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinktotheCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver()appliestothedatamadeavailableinthisarticle,unlessotherwisestated.Lietal.Microbiome(2018)6:187[1,6,7],whichinfluencescarbonbalance,greenhousegasproduction,cropprod-uctivity,andwatereutrophication[8].Therefore,agrow-ingbodyofresearchhasfocusedonthebiogeographyofmicrobialcommunities[9–11].However,despiteeffortstocharacterizethedriversofDOMconcentrationdy-namics[8,12–15],noattemptshavebeenmadetocom-binethesedatasoastounderstandtheassociatedpropertiesofeachandtheenvironmentalfactorsthatdrivethem.Ultrahigh-resolutionFouriertransformioncyclotronresonancemassspectrometry(FT-ICR-MS)enablesdetailedcharacterizationofDOMmoleculardis-tribution[13,16,17].Thisapproachhasbeenappliedtomarine[18,19]andinlandwater[4,20,21],andahand-fulofcomparativeexperimentshaveexaminedsoilDOMatthemolecularlevel[3,14,15,22];however,themicrobialtaxonomicandmetabolicstructuresthatinflu-encethemoleculardistributionofsoilDOMremainunknown.Toourknowledge,nocomprehensivestudyhasyetbeenperformedtoelucidatethena