First Detection of Bat White-Nose Syndrome in Western North America


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First Detection of Bat White-Nose Syndrome in Western North America

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Title:
First Detection of Bat White-Nose Syndrome in Western North America
Series Title:
American Society for Microbiology Journals
Creator:
Lorch, Jeffrey M.
Palmer, Jonathan M.
Lindner, Daniel L.
Ballmann, Anne E.
George, Kyle G.
Griffin, Kathryn
Knowles, Susan
Huckabee, John R.
Haman, Katherine H.
Anderson, Christopher D.
Becker, Penny A.
Buchanan, Joseph B.
Foster, Jeffrey T.
Blehert, David S.
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Wns ( local )
Northwest America ( local )
Disease ( local )
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serial ( sobekcm )

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White-nose syndrome (WNS) is an emerging fungal disease of bats caused by Pseudogymnoascus destructans. Since it was first detected near Albany, NY, in 2006, the fungus has spread across eastern North America, killing unprecedented numbers of hibernating bats. The devastating impacts of WNS on Nearctic bat species are attributed to the likely introduction of P. destructans from Eurasia to naive host populations in eastern North America. Since 2006, the disease has spread in a gradual wavelike pattern consistent with introduction of the pathogen at a single location. Here, we describe the first detection of P. destructans in western North America in a little brown bat (Myotis lucifugus) from near Seattle, WA, far from the previously recognized geographic distribution of the fungus. Whole-genome sequencing and phylogenetic analyses indicated that the isolate of P. destructans from Washington grouped with other isolates of a presumed clonal lineage from the eastern United States. Thus, the occurrence of P. destructans in Washington does not likely represent a novel introduction of the fungus from Eurasia, and the lack of intensive surveillance in the western United States makes it difficult to interpret whether the occurrence of P. destructans in the Pacific Northwest is disjunct from that in eastern North America. Although there is uncertainty surrounding the impacts of WNS in the Pacific Northwest, the presence of the pathogen in western North America could have major consequences for bat conservation. IMPORTANCE White-nose syndrome (WNS) represents one of the most consequential wildlife diseases of modern times. Since it was first documented in New York in 2006, the disease has killed millions of bats and threatens several formerly abundant species with extirpation or extinction. The spread of WNS in eastern North America has been relatively gradual, inducing optimism that disease mitigation strategies could be established in time to conserve bats susceptible to WNS in western North America. The recent detection
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American Society for Microbiology Journals, Vol. 1, no. 4.

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FirstDetectionofBatWhite-Nose SyndromeinWesternNorthAmericaJeffreyM.Lorch,aJonathanM.Palmer,bDanielL.Lindner,bAnneE.Ballmann,aKyleG.George,aKathrynGrif“n,aSusanKnowles,aJohnR.Huckabee,cKatherineH.Haman,dChristopherD.Anderson,dPennyA.Becker,dJosephB.Buchanan,dJeffreyT.Foster,eDavidS.BlehertaU.S.GeologicalSurvey,NationalWildlifeHealthCenter,Madison,Wisconsin,USAa;U.S.ForestService,Northern ResearchStation,CenterforForestMycologyResearch,Madison,Wisconsin,USAb;PAWSWildlifeCenter, Lynnwood,Washington,USAc;WashingtonDepartmentofFishandWildlife,Olympia,Washington,USAd; UniversityofNewHampshire,DepartmentofMolecular,CellularandBiomedicalSciences,Durham,New Hampshire,USAe ABSTRACT White-nosesyndrome(WNS)isanemergingfungaldiseaseofbats causedby Pseudogymnoascusdestructans .Sinceitwas“rstdetectednearAlbany, NY,in2006,thefungushasspreadacrosseasternNorthAmerica,killingunprecedentednumbersofhibernatingbats.ThedevastatingimpactsofWNSonNearctic batspeciesareattributedtothelikelyintroductionof P.destructans fromEurasiato naivehostpopulationsineasternNorthAmerica.Since2006,thediseasehasspread inagradualwavelikepatternconsistentwithintroductionofthepathogenatasinglelocation.Here,wedescribethe“rstdetectionof P.destructans inwesternNorth Americainalittlebrownbat( Myotislucifugus )fromnearSeattle,WA,farfromthe previouslyrecognizedgeographicdistributionofthefungus.Whole-genomesequencingandphylogeneticanalysesindicatedthattheisolateof P.destructans from WashingtongroupedwithotherisolatesofapresumedclonallineagefromtheeasternUnitedStates.Thus,theoccurrenceof P.destructans inWashingtondoesnot likelyrepresentanovelintroductionofthefungusfromEurasia,andthelackofintensivesurveillanceinthewesternUnitedStatesmakesitdif“culttointerpret whethertheoccurrenceof P.destructans inthePaci“cNorthwestisdisjunctfrom thatineasternNorthAmerica.AlthoughthereisuncertaintysurroundingtheimpactsofWNSinthePaci“cNorthwest,thepresenceofthepathogeninwestern NorthAmericacouldhavemajorconsequencesforbatconservation. IMPORTANCE White-nosesyndrome(WNS)representsoneofthemostconsequentialwildlifediseasesofmoderntimes.Sinceitwas“rstdocumentedinNew Yorkin2006,thediseasehaskilledmillionsofbatsandthreatensseveralformerly abundantspecieswithextirpationorextinction.ThespreadofWNSineasternNorth Americahasbeenrelativelygradual,inducingoptimismthatdiseasemitigationstrategiescouldbeestablishedintimetoconservebatssusceptibletoWNSinwestern NorthAmerica.TherecentdetectionofthefungusthatcausesWNSinthePaci“c Northwest,farfromitspreviousknowndistribution,increasestheurgencyforunderstandingthelong-termimpactsofthisdiseaseandfordevelopingstrategiestoconserveimperiledbatspecies. KEYWORDS: Pseudogymnoascusdestructans ,Washington,bat,white-nosesyndrome W hite-nosesyndrome(WNS)isacutaneousinfectionofhibernatingbatscausedby thepsychrophilicfungus Pseudogymnoascusdestructans (1,2).Thedisease,“rst documentedin2006,wassubsequentlyassociatedwithmassivemortalityofcavehibernatingbatspeciesinthenortheasternUnitedStates(3,4).TheemergenceofWNS islikelyduetotheintroductionof P.destructans intonaivebatpopulationsinNorthReceived 27May2016 Accepted 12July 2016 Published 3August2016 Citation LorchJM,PalmerJM,LindnerDL, BallmannAE,GeorgeKG,Grif“nK,KnowlesS, HuckabeeJR,HamanKH,AndersonCD,Becker PA,BuchananJB,FosterJT,BlehertDS.2016. Firstdetectionofbatwhite-nosesyndromein westernNorthAmerica.mSphere1(4):e0014816.doi: 10.1128/mSphere.00148-16 . Editor KatherineMcMahon,Universityof Wisconsin Copyright ©2016Lorchetal.Thisisanopenaccessarticledistributedunderthetermsof the CreativeCommonsAttribution4.0 Internationallicense . AddresscorrespondencetoJeffreyM.Lorch, jlorch@usgs.gov. J.M.L.andJ.M.P.contributedequallytothis article. OBSERVATION ClinicalScienceandEpidemiology crossmark Volume1Issue4e00148-16 msphere.asm.org 1

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America.ThefunguspresumablyoriginatedinEurasia,whereitoccursonbatsbutis notknowntocausesevereinfectionsorpopulationdeclines(5…7).Consistentwitha pointsourceintroductionofanexoticpathogen, P.destructans hasspreadoutward fromtheWNSepicenterinNewYorkbyapproximately200to900kmperyear(Fig.1). Asofspring2016,thefungushadreachedasfarwestaseasternOklahoma,eastern Nebraska,andeasternMinnesota,approximately1,900kmfromthepresumedsiteof introduction. On11March2016,amoribundlittlebrownbat( Myotislucifugus )wasfoundinKing County,WA(UnitedStates),andsubmittedtoalocalwildliferehabilitationcenter.The animalpresentedwithdriedandcontractedareasofcrustedskinonthewingsanddied 2dayslater.Swabsamplesofthewingswerepositivefor P.destructans byreal-timePCR (8),andthebatwascon“rmedtohaveWNSinaccordancewithde“nedhistopathologic criteria(9).Anisolateof P.destructans wasobtainedbyculturingaportionofwingskin onSabourauddextroseagarcontainingchloramphenicolandgentamicinat13°C. IneasternNorthAmerica, P.destructans appearstobespreadingclonally,withall isolatesexhibitingnogeneticdiversityatthemarkersexamined(10).However,isolates ofthefungusfromEuropedisplaysigni“cantgeneticvariation(11).Todetermine whethertheisolateof P.destructans fromWashingtonmatchedtheclonallineagefrom easternNorthAmerica,weconductedwhole-genomesequencingusingtheIonTorrent PersonalGenomeMachine(PGM)ontheWashingtonisolate(NWHC#27099-001),as wellasonthreeadditionalisolatesof P.destructans fromeasternNorthAmerica.These isolatesoriginatedfrom M.lucifugus batscollectedinAlbanyCounty,NY,in2008 (NWHC#20631-008)andinIowaCounty,WI,in2016(NWHC#26994-002)andatricoloredbat( Perimyotissub”avus )inJacksonCounty,AL,in2015(NWHC#44797-145). ForcomparisontoEuropeanisolatesof P.destructans ,weusedwhole-genomedata fromisolatesfromtheCzechRepublic(isolatesCCF3941,CCF3942,CCF4124,and CCF4125)availableintheNCBISRADatabase(accessionnumbers SRR3411506 , SRR3411507 , SRR3411508 ,and SRR3411509 ),aswellastheNorthAmericantypeisolate (NWHC#20631-21;NCBISRAaccessionnumber SRR1952982 ). Sequencingfollowedthemanufacturers(ThermoFisherScienti“c)recommendationsusingthefollowingkits:Ionplusfragmentlibrarykit(catalognumber4471252), FIG1Generalizedspatiotemporalspreadof Pseudogymnoascusdestructans acrossNorthAmerica sincetheinitialdetectionofwhite-nosesyndrome(WNS)inNewYorkin2006.Themapwas generatedusingthenatural-neighborrasterinterpolationtoolinArcMap10.2.1(ESRI,Redlands,CA), basedonfirstdetectionof P.destructans withinacountyorfirstclassificationofacountyassuspect forWNS.ThemapwasgeneratedusingdatafromtheU.S.GeologicalSurvey,NationalWildlifeHealth Center,and https://www.whitenosesyndrome.org/resources/map .Eachcolorrepresentsthespread ofthepathogenduringagivenwinter(hibernation)seasonspanningfromNovembertoMay.Lorchetal. Volume1Issue4e00148-16 msphere.asm.org 2

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IonlibraryTaqManquantitationkit(catalognumber4468802),IonPGMHi-QviewOT2 (OneTouch2)kit(catalognumberA29811),Ion318v2(catalognumber4484354),and IonPGMHi-Qviewsequencingkit(catalognumberA30043).Therawsequencingdata wereprocessedusingthedefaultsettingsintheTorrentSuitesoftwareversion5.0.4. Foreachisolate,weobtainedmorethan12 averagedepthofsequencingcoverage overthe P.destructans genomereference.Single-nucleotidepolymorphisms(SNPs) wereidenti“edfromthenext-generationsequencingreadsusingtheSnippypipeline version3.0(12).Brie”y,readswerealignedtothe P.destructans typeisolate (NWHC#20631-021)referencegenome(13)(GenBankaccessionnumberGCA_ 001641265.1)usingBurrows-WheelerAligner(BWA)version0.7.12-r1044(14),and variantswerecalledusingFreeBayesversion0.9.21-7-g7dd41db(15)withaminimum readcoverageof4(foreachisolate,thegenomecoveragewasatleast98.27%ata4 threshold),minimummappingqualitysetto60,andminimumproportionforvariant evidencesetto90%.AconcatenatedalignmentofcoreSNPs(de“nedasanSNPthat occursatagenomicpositionpresentinallsamples)wasgeneratedusingSnippy,and anunrootedphylogenictreewasinferredfromtheresulting13,379charactersusing theneighbor-joiningmethodandtheJukes-CantorsubstitutionmodelinCLCGenomicsWorkbench9.Asasecondarymethod,maximum-likelihoodanalysiswasperformed usingthegeneraltime-reversible(GTR)substitutionmodelinMEGAversion6.06. Thegenomesequenceoftheisolateof P.destructans fromWashingtonwasstatisticallyindistinguishablefromthefourNorthAmericanisolates,formingacladedistinct fromthefourEuropeanisolates(Fig.2).Althoughtheywerecollectedfromamore con“nedgeographicregion(twohibernaculaintheCzechRepublic),theEuropean isolatesexhibitedmuchhighergeneticdiversitythantheNorthAmericanisolatesand includedbothknownmatingtypes;onlythe MAT1-1 matingtypehasthusfarbeen identi“edamongisolatesfromNorthAmerica(Fig.2)(16).Theminimaldiversityand singlematingtypeobservedamongisolatesof P.destructans fromtheNearcticis consistentwithclonalspreadofthepathogeninNorthAmerica.Theseobservations alsosuggestthattheWashingtonisolateof P.destructans islikelyofNorthAmerican originratherthanrepresentinganindependentintroductioneventfromEurasia. Thetimingandmechanismbywhich P.destructans mayhavereachedthePaci“c Northwestareunclear.Thenearestdetectionof P.destructans isover2,100kmawayin easternNebraska.Inthedecadesince P.destructans was“rstdetectedinNorth America,thefungushasspreadapproximately1,900kmfromthesuspectedintroducFIG2 Phylogeneticrelationshipsbasedonwhole-genomesequenceanalysisofnineisolatesof Pseudogymnoascus destructans fromNorthAmericaandEurope.Acorealignmentof13,379SNPswasgeneratedforeachisolate,usingSnippy (11),andphylogenywasinferredbydrawinganunrootedneighbor-joiningtreesupportedwith1,000bootstrapreplicates (branchlengthsrepresentthenumberofsubstitutionspersite).Asecondanalysisusingmaximumlikelihoodproduced atreewithidenticaltopology.Thusfar,isolatesof P.destructans fromNorthAmericaappeartobeclonal,whereasthere isconsiderablevariationinpopulationsof P.destructans inEurope(eveninthissmallsamplesizeofisolatesfromalimited geographicalrange).Isolatesfrombothmatingtypes( MAT1-1 and MAT1-2 )arefoundinEurope,suggestingthatsexually recombiningpopulationscontributetotheincreaseingenomicvariability.Asinglematingtype( MAT1-1 )isknownfrom NorthAmerica.Bootstrapvalues(neighbor-joininganalysis/maximum-likelihoodanalysis)forwell-supportednodes( > 90) arepresented.White-NoseSyndromeinWashington Volume1Issue4e00148-16 msphere.asm.org 3

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tionsite.Thus,therecentdetectioninWashingtonappearsinconsistentwiththe previouslydocumentedandpredictedpatternofpathogenspread(17).Sequence analysisoftheWashingtonbatsmitochondrialNADHdehydrogenasesubunit1,cytochrome b (cyt b ),andcytochrome c oxidasesubunitI(COI)genes(18,19)mostclosely matchedGenBanksequencesforlittlebrownbatsfromwesternNorthAmerica.Phylogeneticanalysesperformedonthecyt b andCOIgenesfurtherdemonstratedthatthe infectedbatfromWashingtonresidedwithinawell-supportedclade(bootstrapsupport valuesof100and95forthecyt b geneandtheCOIgene,respectively;seeFig.S1inthe supplementalmaterial)thatincludedmembersof M.lucifugus alascensis,asubspecies restrictedindistributiontowesternNorthAmerica.This“ndingsuggeststhatthe animalbecameinfectedwith P.destructans inthePaci“cNorthwestandthatthebat wasnotavagrantfromeasternNorthAmerica,whereWNSisnowendemic.Sampling ofbatsandcaveenvironmentsinthewesternUnitedStatessincethewinterof 2013-2014withoutdetectionofthefungussuggeststhatthepathogenisnotwidespreadorabundantinthisenvironmentinwesternstates(i.e.,over2,000samples testedfromArizona,California,Colorado,Idaho,Montana,Nebraska,NewMexico, Nevada,Oklahoma,Oregon,Texas,Utah,Washington,andWyoming;A.Ballmann, unpublisheddata).Moreintensivesurveillanceeffortstode“netherangeof P.destructans inwesternNorthAmericashouldimproveourunderstandingofthepresence, distribution,andoriginofthispathogeninthePaci“cNorthwest. Thepresenceof P.destructans inwesternNorthAmericahasmajorimplicationsfor conservationofbatpopulations.Theadditionofapotentialseconddiseaseepicenter couldexposenovelhostspeciestothepathogen,acceleratetherateatwhichWNS spreads,andreducetheamountoftimethatwildlifemanagementagencieshaveto developmitigationstrategies.RapidresponsestoWNSinwesternNorthAmericamay bedif“cult,becausethelocationsofhibernationsitesformanywesternbatspeciesare unknownorinaccessible(20,21).Furthermore,thewinteringstrategiesofmanyspecies ofbatsinthePaci“cNorthwestarenotwellunderstood,withsomespeciesknownto foragethroughoutthewinter(22).Consequently,newapproachesmaybenecessaryto facilitatepathogensurveillance,monitordiseaseimpacts,andconductmitigation effortsforWNSinthisregion.Theseverity,magnitude,duration,andpotential ecosystem-leveleffectsofWNSinNorthAmericarankitamongthemostconsequential wildlifediseaseeventseverrecorded.Althoughmuchprogresshasbeenmadein understandingWNSandinmonitoringitsspread,moreworkisneededtodetermine howthediseasedynamicsandimpactsvaryamongbatpopulationsineasternand westernNorthAmerica.Accessionnumbers. NucleicacidsequencesfortheNADHdehydrogenasesubunit1, cytochrome b ,andcytochrome c oxidasesubunitIgenesofthelittlebrownbatwith WNSfromWashingtonareavailableinGenBank(accessionnumbers KX290926 , KX290927 ,and KX463942 ,respectively).Next-generationsequencingdataareavailable throughtheNCBISRAdatabase(accessionnumber SRP075419 )andtheBioProject database(accessionnumber PRJNA322173 ).SUPPLEMENTALMATERIAL Supplementalmaterialforthisarticlemaybefoundat http://dx.doi.org/10.1128/ mSphere.00148-16 . FigureS1,PDF“le,0.3MB. ACKNOWLEDGMENTS WethankBrendaBerlowski-Zier,ElizabethBohuski,StephanieSteinfeldt,andKaren Vanderwolfforassistanceinpreparingsamplesandconductinglaboratorytests. Wedeclarenocon”ictofinterestrelatedtothiswork. Theuseoftrade,“rm,orproductnamesisfordescriptivepurposesonlyanddoes notimplyendorsementbytheU.S.Government. ThisworkwasfundedbytheU.S.GeologicalSurveyandU.S.ForestService.Lorchetal. Volume1Issue4e00148-16 msphere.asm.org 4

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FUNDINGINFORMATION Thiswork,includingtheeffortsofJeffreyM.Lorch,wasfundedbyDOI|U.S.Geological Survey(USGS).Thiswork,includingtheeffortsofDanielL.Lindner,wasfundedby USDA|U.S.ForestService(USFS). REFERENCES 1. GargasA,TrestMT,ChristensenM,VolkTJ,BlehertDS .2009. Geomycesdestructans sp.nov.associatedwithbatwhite-nosesyndrome. Mycotaxon 108: 147…154. http://dx.doi.org/10.5248/108.147 . 2. LorchJM,MeteyerCU,BehrMJ,BoylesJG,CryanPM,HicksAC, BallmannAE,ColemanJT,RedellDN,ReederDM,BlehertDS .2011. Experimentalinfectionofbatswith Geomycesdestructans causeswhitenosesyndrome.Nature 480: 376…378. http://dx.doi.org/10.1038/ nature10590 . 3. BlehertDS,HicksAC,BehrM,MeteyerCU,Berlowski-ZierBM, BucklesEL,ColemanJT,DarlingSR,GargasA,NiverR,Okoniewski JC,RuddRJ,StoneWB .2009.Batwhite-nosesyndrome:anemerging fungalpathogen?Science 323: 227. http://dx.doi.org/10.1126/ science.1163874 . 4. 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VonhofMJ,RussellAL,Miller-ButterworthCM .2015.Range-wide geneticanalysisoflittlebrownbat( Myotislucifugus )populations:estimatingtheriskofspreadofwhite-nosesyndrome.PLoSOne 10: e0128713. http://dx.doi.org/10.1371/journal.pone.0128713 . 20. PerkinsJM,BarssJM,PetersonJ .1990.Winterrecordsofbatsin OregonandWashington.NorthwestNat 71: 59…62. http://dx.doi.org/ 10.2307/3536594 . 21. BoganMA,CryanPM,ValdezEW,EllisonLE,OSheaTJ .2003.Westerncreviceandcavity-roostingbats,p69…77. In OSheaTJ,BoganMA (ed),MonitoringtrendsinbatpopulationsoftheUnitedStatesand territories:problemsandprospects.Informationandtechnologyreport 2003-0003.U.S.GeologicalSurvey,FortCollins,CO. 22. FalxaG .2007.Winterforagingofsilver-hairedandCaliforniamyotisbats inwesternWashington.NorthwestNat 88: 98…100. http://dx.doi.org/ 10.1898/1051-1733(2007)88[98:WFOSAC]2.0.CO;2 . 23. 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