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published:24August2021
doi:.694866
FirstDescriptionofaSatelliteDNAin
Manatees’CentromericRegions
Mirela Pelizaro Valeri 1,Guilherme Borges Dias 2,Alice Alves do Espírito Santo 1,
Camila Nascimento Moreira 3,Yatiyo Yonenaga-Yassuda 3,Iara Braga Sommer 4,
Gustavo C. S. Kuhn 1andMarta Svartman 1*
1 LaboratóriodeCitogenômicaEvolutiva,DepartamentodeGenética,EcologiaeEvolução,InstitutodeCiênciasBiológicas,
UniversidadeFederaldeMinasGerais,BeloHorizonte,Brazil,2 DepartmentofGeneticsandInstituteofBioinformatics,
UniversityofGeorgia,Athens,GA,UnitedStates,3 DepartamentodeGenéticaeBiologiaEvolutiva,InstitutodeBiociências,
UniversidadedeSãoPaulo,SãoPaulo,Brazil,4 CentroNacionaldePesquisaeConservaçãodaBiodiversidadeMarinhado
Nordeste,InstitutoChicoMendesdeConservaçãodaBiodiversidade,Brasília,Brazil
TrichechusmanatusandTrichechusinunguisarethetwoSireniaspeciesthatoccurin
,manyaspectsoftheirbiologyremain
understudied, usedthe
(satDNAs)in
 reportthefirstdescriptionofTMAsat,asatDNAcomprising~%of
Editedby:thegenome,with~684 ,TMAsat
-Ruano,showedsimilarmonomerlength,chromosomelocalizationandconservedCENP-B
UniversityofEastAnglia,
United Kingdombox- alsodetectedthissatDNAintheDugongdugonand
Reviewedby:-joiningtreeshowsthat
NevenkaMestrovic,,,,-
RudjerBoskovicInstitute,Croatiaspecificclusters, detected
IsidoroFeliciello,
UniversityofNaplesFedericoII,ItalyadivergentTMAsat-likehomologoussequenceinelephantsandhyraxes,butnotinother
*Correspondence:mammals,suggestingthissequencewasalreadypresentinthecommonancestorof
MartaSvartmanPaenungulata,
******@
acentromericsatDNAinmanateesandwillfacilitatetheinclusionofSireniainfuture
Specialtysection:studiesofcentromeresandsatDNAbiology.
Thisarticlewassubmittedto
EvolutionaryandPopulationKeywords:tandemrepeats,Trichechusmanatus,Trichechusinunguis,chromosomemapping,fluorescentinsitu
Genetics,hybridization,TAREAN
asectionofthejournal
FrontiersinGenetics
Received:13April2021INTRODUCTION
Accepted:30July2021
Published:
Citation:familyincludestheDugongdugonandtheSteller’sseacowHydrodamalisgigas,thelatternow
ValeriMP,DiasGB,Espíritoextinctduetooverhunting,andtheTrichechidaefamilyincludesthreemanateespecies:Trichechus
SantoAA,MoreiraCN,manatus,Trichechusinunguis,andTrichechussenegalensis(Domning,2018).Dugongdugon
Yonenaga-YassudaY,SommerIB,
occursacrosscoastalwatersintheIndo-WestPacificOcean,
KuhnGCSandSvartmanM(2021)
FirstDescriptionofaSatelliteDNAintothewestcoastofAfrica,,theWestIndianmanatee,,
Manatees’,
:
doi:.694866Brazil,(Bonvicinoet al.,2020).
FrontiersinGenetics||Volume12|Article694866
AllextantsireniansareconsideredasvulnerablebytheAnotheraspectofsatDNAsevolutionistheirrelationshipwith
InternationalUnionforConservationofNatureandNaturalmobileelements,sincethereareseveralexamplesofsatDNAs
Resources(IUCN;Deutschet al.,2008;Keith,2015;Marmontelderivedfromtransposonsandretrotransposonsinplantsand
et al.,2016;MarshandSobtzick,2019).animals(reviewedinMeštrovićet al.,2015).
TheWestIndianmanateehastworecognizedsubspecies:TherepetitiveDNAfractionofmanatees’genomeshasbeen
Trichechusmanatuslatirostris(FloridaManatee),foundinthepoorlystudied, used
UnitedEstatesandGulfofMexicocoasts,(Novák
(Antilleanmanatee),foundintheCaribbean,CentralandSouthet al.,2017,2020)pipelinetoexplorethesatDNAspresentin
,we describeforthefirsttimethecentromeric
,whichwe foundtobe also
,thedugong,andinthe
’ characterizedthissequencein
.
,we investigatedthepresenceoftheTMAsatsequence
fromtheUnited ,whichallowedusto
populationssouthoftheAmazonRivermouth(Viannaet al.,establisharoughtimelineforitsorigin.
2006;Barroset al.,2017;Limaet al.,2019,2021).Hybrids
onthesympatricareaattheAmazonRivermouthMATERIALSANDMETHODS
(Viannaet al.,2006;Limaet al.,2019;Lunaet al.,2021).
SatelliteDNAs(satDNAs)areatypeofrepetitiveDNADenovoIdentificationofSatelliteDNAs
,we usedwhole-genome
arraysoftandemrepeatswithvariableunitlength,(accessionnumberSRR328416)
–
associatedwithchromosomelandmarkssuchascentromeres,NCBIandtheTAREANpipeline(Nováket al.,2017).Thefirst
telomeres,-basedclustering,whichperforms
satDNAsdonotencodeproteins,theyareassociatedwithalltoallsimilaritycomparisonsofDNAsequencingreads,resulting
,
ofheterochromatinattelomeresandcentromeres,anditexaminesthepresenceofcircularorglobula-likegraphstructures
maintenanceofchromosomeintegrityandgenomestabilitytoidentifypotentialtandemrepeats,classifiedasputativehighor
(reviewedinShapiroandvonSternberg,2005;Biscottiet al.,(~100 bplong)
2015;Shatskikhet al.,2020).SatDNAscanformhigher-orderusedinthisanalysiswererandomlysampledbyTAREAN,comprising
repeat(HOR)unitsmadeofmultimerswithanumberof~%(870,965reads) pgestimatedgenomesize(Kasai
divergedmonomersthataretandemlyrepeatedasaset(reviewedet al.,2013).Thereadsthatmakeupeachclusterarepartially
inPlohlet al.,2012;Vlahovićet al.,2016).HORorganizationassembledintocontigsthatwereusedforrepeatannotationwith
hasbeenfoundinseveralsatDNAs,includingthealfacentromerictheCENSORwebserver(Kohanyet al.,2006)thatcontainsa
satDNAinhumans,andmaybe relevanttothecentromericcollectionofMammaliarepeatsfromRepBase,updatedin08-24-
function(Sujiwattanaratet al.,2015;Sullivanet al.,2017).In2020(Baoet al.,2015).Thesinglepotentialtandemrepeatcluster
addition,satDNAsmonomersequencescanpresentinternal(13)withglobula/ring-likestructurewasanalyzedindetailthrough
repetitions,whichmaybe (accession
relevanttocentromericfunction(KasinathanandHenikoff,)usingtheBLASTntoolwithdefaultparameters
2018).CentromericsatDNAsinmammalsusuallypresentthe(Altschulet al.,1990)toverifyifthesequenceisatandemrepeat.
CENP-Bbox,aconserved17 bpregionknowntobe theInadditiontotheannotationusingtheCENSORwebserver,this
DNA-bindingdomainforthecentromericproteinB(CENPB),clusterwasannotatedthroughBLASTnsimilaritysearchesagainst
withninenucleotides(nTTCGnnnnAnnCGGGn)composingthewholenucleotidecollection(nr/nt).
themostevolutionarilyconserveddomain(ECD;Muroet al.,TheidentifiedsatDNAsequencewascharacterizedregarding
1992;Masumotoet al.,2004;Alkanet al.,2011;Kasinathanitsgenomeproportion,monomerlength,ATcontent,andpresence
andHenikoff,2018).
evolution,
arequicklyhomogenizedacrosstherepeatfamilyandfixedtheassemblyprocessbyapplyingak-mer-basedapproachtoobtain
inreproductivelyisolatedpopulations,resultinginintraspecificalessfragmentedmonomerconsensus,butitrestrictsitselftothe
repeathomogeneitybutinterspecificdivergenceDover,(1982;50%mostprevalentk-,we chose
Plohlet al.,2012;Smalecet al.,2019).Moreover,accordingthewhole-genomeassemblyresourceasamorerepresentative
tothelibrarymodel,(MCS)
ofsatDNAssequenceswithmostlyquantitativeinterspeciesofTMAsatwasgeneratedusingGeneious()
differencesduetoexpansionorcontraction(evenelimination)witha25%thresholdand66monomericsequencesretrievedfrom
duringtheevolution(FryandSalser,1977;Meštrovićet al.,1998).thereferencegenome,previouslyalignedwiththemusclealigner
FrontiersinGenetics||Volume12|Article694866
length,ATcontent,(FISH)wasperformedusing
featurewasalsoconductedintheGeneioussoftwareusingthetheTMAsatcloned(MW272776)sequenceasprobeonmetaphase
diagonalplotmethodinhighsensitivemode,
of50 bpandidentitythresholdof60%.with200 ngofbiotin-labelledprobes,following(Valeriet al.,
WesearchedforthepresenceofTMAsatinthetwoother2020).Theanalysesandimageacquisitionwereperformed
SireniaspecieswithasequencedgenomeavailableinNCBI,underaZeissAxioimager2epifluorescencemicroscopeequipped
(underaccessionnumbersofassembledgenomewithaCCDcameraandwiththeAxioVisionsoftware(Carl
)andZeissMicroImaging,Jena,Germany),respectively.
(underaccessionnumbersofassembled
SRR12067498).First,we usedTMAsatsequenceasqueryin
DNApolymorphismsandnucleotidediversityalongthesatDNA
BLASTnsimilaritysearchesagainsttheseassembledgenomes.
sequenceswereanalyzedusingthesoftwareDnaSP 
Inaddition,we alsousedtherawIlluminareads(~150 bp
(Rozaset al.,2017)withthesamemonomersequencesused
long)andTAREANtoidentifyTMAsatinthesegenomes.
,,.
TheanalyzedreadswererandomlysampledbyTAREAN
Inthisanalysis,themonomersequenceswerepreviouslyaligned
totalizing1,038,927 ,097 
withthemusclemethod(Edgar,2004)implementedinMEGA
Xandthewindowlengthandstepsizeweresetfor10and
usingmonomericsequencesretrievedfromthereferencegenome
1 bp,
afterBLASTsearches,
variableiftheyexhibitedmorethantwoSDsbelloworabove
thenucleotideaveragevariability,respectively.
obtainedusingthefiveclonedsequencesobtainedbyPCR.
,,
.
,
implementedinMEGAXandusedfortheconstructionofa
BiologicalSamplesneighbor-
,t