RESEARCHOpenAccessResilienceoftheresidentsoilmicrobiometoorganicandinorganicamendmentdisturbancesandtotemporarybacterialinvasionKésiaSilvaLourenço1,2,3,AfnanK.A.Suleiman1,A.Pijl1,J.A.vanVeen1,3,H.Cantarella2andE.E.Kuramae1*AbstractBackground:Vinasse,aby-productofsugarcaneethanolproduction,isrecycledbysugarcaneplantationsasafertilizerduetoitsrichnutrientcontent.However,theimpactsofthechemicalandmicrobialcompositionofvinasseonsoilmicrobiomedynamicsareunknown.Here,weevaluatetherecoveryofthenativesoilmicrobiomeaftermultipledisturbancescausedbytheapplicationoforganicvinasseresidue,inorganicnitrogen,oracombinationofbothduringthesugarcanecrop-growingseason(389days).Additionally,weevaluatedtheresistanceoftheresidentsoilmicrobialcommunitytothevinassemicrobiome.Results:Vinasseappliedaloneor30dayspriortoNresultedinsimilarchangesinthesoilmicrobialcommunity.Furthermore,theimpactoftheapplicationofvinassetogetherwithNfertilizeronthesoilmicrobialcommunitydifferedfromthatofNfertilizeralone.Organicvinasseisasourceofmicrobes,nutrients,andorganicmatter,andthecombinationofthesefactorsdrovethechangesintheresidentsoilmicrobialcommunity.However,thesechangeswererestrictedtoashortperiodoftimeduetothecapacityofthesoilcommunitytorecover.Theinvasivebacteriapresentinthevinassemicrobiomewereunabletosurviveinthesoilconditionsanddisappearedafter31days,withtheexceptionoftheAcetobacteraceae(nativeinthesoil)andLactobacillaceaefamilies.Conclusion:OuranalysisshowedthattheresidentsoilmicrobialcommunitywasnotresistanttovinasseandinorganicNapplicationbutwashighlyresilient.Keywords:Seasonalvariation,Microbialecology,Sustainability,Mineralfertilizer,Vinasse,SugarcaneBackgroundBioethanolproductionusingdifferentfeedstocks(e.g.,sugarcane,sugarbeet,corn)produceslargeamountsofor-ganicresiduesthatcanberecycledasorganicfertilizers.Vinasseisaby-productofethanolproductionfromsugar-cane.Braziliscurrentlythelargestsugarcaneethanolpro-ducer(659.1milliontonsofsugarcaneannually)andgeneratesapproximately10–15Lofvinasseforeveryliterofalcoholproduced(27.5billionlitersofethanoland~360billionlitersofvinasseannually)[1,2].Vinasseisusu-allyanacidiccompost(pH3.5–5)intheformofadarkbrownslurrywithahighorganiccontent(chemicaloxy-gendemand,50–150gL−1).Toavoiddischargeinrivers,alternativeusesofvinassehavebeenexplored,includingasafertilizerapplieddirectlytosugarcaneplantations[2]asasourcemainlyofpotassiumbutalsoorganicmatter,nitrogen,andphosphorus.Duetothehighcontentofpo-tassium,therateofapplicationofvinasseasanorganicfertilizerisbasedonthepotentialforgroundwatercon-taminationbypotassiumandisnotsufficienttosupplythetotalNrequired.Consequently,vinasseiscommonlyappliedincombinationwithmineralNfertilizersinsugar-canefieldsinBrazil.Thispracticeofcombinedapplicationofinorganicandorganicfertilizerscontributessignifi-cantlytoincreasedgreenhousegas(GHG)emissionstotheatmosphere,especiallynitrousoxide(N2O)and*Correspondence:E.Kuramae@nioo.knaw.nl1MicrobialEcologyDepartment,NetherlandsInstituteofEcology(NIOO),Droevendaalsesteeg10,6708PBWageningen,TheNetherlandsFulllistofauthorinformationisavailableattheendofthearticle©TheAuthor(s).2018OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCommonsAttribution4.0InternationalLicense(),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinktotheCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver()appliestothedatamadeavailableinthisarticle,unlessotherwisestated.Lourençoetal.Microbiome(2018)6:142(CO2),duetothehighwaterandorganiccontentofvinasse[3–6].Organicfertilizersareconsideredmoreenvironmentallyfriendlythaninorganicfertilizersbecausetheformeral-lowsthenutrientsproducedinagriculturalsystemstoberecycledandimprovessoilquality.However,theapplica-tionoforganicresiduesmightdisrupttheresidentsoilmi-crobialcommunity.Short-andlong-termimpactsofinorganicfertilizationpracticesonsoilmicrobialcommu-nitystructurehavebeenreported[7–11].However,fewstudieshaveevaluatedtheimpactoforganicfertilizerontheresidentsoilbacterialcommunity,particularlyimme-diatelyafterapplicationandthroughouttheplant-growingseason[10,12].Organicfertilizersdirectlyorindirectlycausesmall-scaledisturbancesofsoilhabitatsduetotheirwatercontent,chemicalandorganiccomponents,andintroductionofexogenousmicrobes(dependingonthefeedstocksource)[10].Thesoilmicrobialcommunityisusuallyresistantand/orresilienttoexogenousmicrobesandreturnstotheoriginalstate[10,13].PreviousstudiesofsugarcanehaveshownthatthecombinedapplicationofvinasseandmineralNfertilizercanalterspecificbacterialgroupsandfavorshighemissionsofCO2-CandN2O-N[5,6].WhenvinasseisaddedafewdaysbeforeorafterNfertilizerasanoptiontodecreaseGHGemissions,N2OandCO2emissionsdecreasecomparedwithcombinedap-plication[4],buttheimpactonthemicrobialcommunityisunknown.In