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The complete mitochondrial genome of a new invader fish in France, the pink salmon Oncorhynchus gorbuscha (Walbaum, 1792) (Teleostei, Salmonidae)

Author: Denys, Gaël P.J.; Josset, Quentin; Ferreira, Amélie Verde; Dettaï, Agnès
Publisher: Zenodo
DOI: 10.26028/cybium/2024-005
Source: https://zenodo.org/records/14681590/files/source.pdf
The comple e mi ochond ial genome o a new in ade ish in F ance,
he pink salmon Onco hynchus go buscha (Walbaum, 1792)
(Teleos ei, Salmonidae)
by
Gaël P.J. Denys* (1, 2), Quen in Josse (3, 4), Amélie Ve De Fe ei A (5) & Agnès De Aï (5)
Cybium 2024, 48(2): 111-120. h ps://doi.o g/10.26028/cybium/2024-005
In oduc Ion
he anad omous Paci ic salmons Onco hynchus spp.
a e na i e o he Paci ic coas s o no h-wes e n Ame ica
and no h-eas e n Asia and ha e a high in e es o aquac-
ul u e, ec ea i e ishing and comme cial ishe ies (F oese
and Pauly, 2022). Many species we e he e o e in oduced
all o e he wo ld since he end o he 19 h cen u y wi h a -
ying success (sco and C ossman, 1973). in F ance, h ee
species we e in oduced ( he ainbow ou O. mykiss (Wal-
baum, 1792), he Coho salmon O. kisu ch (Walbaum, 1792)
and he Chinook salmon O. shawy scha (Walbaum, 1792))
bu only O. mykiss now emains (Pe sa e al., 2020). since
2017, ano he Paci ic salmon, he pink salmon Onco hyn-
chus go buscha (Walbaum, 1792), has in aded no he n
eu ope e e y odd yea (see Bagliniè e e al., 2020; Beaula-
on e al., 2021). his species has a e y s ic and simple
li e cycle: indi iduals li e wo yea s, spending 18 mon hs in
ma ine wa e s be o e b eeding in eshwa e . Adul s measu -
ing abou 50 cm mig a e in i e s om June o Augus o
Asia ic popula ions o om July o sep embe o Ame i-
can ones, and die a e spawning (Hea d, 1991). his spe-
cies migh ha e an impac on he p eda ion, he compe i ion,
he disease ansmission on na i e ish species bu also on
human heal h h ough apewo m in ec ions wi h Diphyl-
lobo h ium nihonkaiense yamane, Kamo, Bylund & Wik-
g en, 1986 (A izono e al., 2009; Van de Vee and nen wig,
2015). Cu en ly, i s impac on na i e eu opean salmonids
Abs ac . – he pink salmon Onco hynchus go buscha ( eleos ei, salmonidae) is a no h Paci ic species.
i a i ed in no he n eu ope h ough eshwa e mig a ion each odd yea since 2017, c ea ing managemen
issues. in his s udy, we sequenced a comple e mi ochond ial genome o a pink salmon caugh in he B esle
i e (F ance) wi h a museum ouche . he sequence is 16,695 bp in leng h and is simila o p e ious mi og-
enomes published wi hin his genus. Leng h he e oplasmy on he con ol egion o his species was de ec ed, as
desc ibed in p e ious molecula s udies. We es ed se e al p ime s commonly used o me aba coding s udies on
ou ma ke s (12s, 16s, Coi and Cy b), and all allow he disc imina ion o his species. his mi ogenome is a
e e ence o molecula iden i ica ion, o ins ance in like en i onmen al DNA s udies.
Résumé. – Le génome mi ochond ial comple d’un nou eau poisson éléos éen in asi en F ance, le sau-
mon ose Onco hynchus go buscha (Walbaum, 1792) (Teleos ei, Salmonidae).
Le saumon ose Onco hynchus go buscha (Teleos ei, Salmonidae) es une espèce du Paci ique No d a i ée
en eu ope du no d a ec une mig a ion en eau douce chaque année impai e depuis 2017, géné an des p oblèmes
de ges ion. Dans ce e é ude, nous a ons séquencé le génome mi ochond ial comple d’un saumon ose d’un
spécimen en egis é en collec ion e cap u é dans la i iè e B esle (F ance). La séquence a une longueu de
16 695 pb e es similai e à d’au es mi ogénomes publiés chez ce gen e. Cependan , nous a ons mis en é idence
une hé é oplasmie de longueu su la égion de con ôle pou ce e espèce con i man les é udes moléculai es
p écéden es. nous a ons égalemen es é plusieu s amo ces cou ammen u ilisées pou les é udes de mé aba co-
ding su qua e gènes (12s, 16s, Coi e Cy b). ous les ma queu s pe me en la disc imina ion de ce e espèce.
no e mi ogénome peu ê e u ilisé comme é é ence pou l’expe ise moléculai e, pa exemple pou des app o-
ches d’ADn en i onnemen al.
© SFI
Recei ed: 13 Jul. 2022
Accep ed: 23 Jan. 2024
Pub. online: 1 Ma . 2024
Edi o : O. O e o
Key wo ds
Mi ogenome
Pink salmon
Long PC
sample mul iplexing
Me aba coding
Genome announcemen
(1) UA Pa imoine na u el – Cen e d’expe ise e de données (2006 oFB – Cn s – MnHn – i D), Muséum na ional d’His oi e
na u elle, 36 ue Geo oy-sain -Hilai e CP 41, 75005 Pa is, F ance. [email p o ec ed]
(2) UM Biologie des o ganismes e écosys èmes aqua iques (Bo eA 8067), MnHn, Cn s, i D, sU, UCn, UA, 57 ue Cu ie CP26,
75005 Pa is, F ance.
(3) O ice F ançais de la Biodi e si é, Di ec ion Reche che e Appui Scien i ique, Se ice “Conse a ion e Ges ion Du able des Espèce
exploi ées”, 92 chaussée de Pica die, 76260 eu, F ance. [email p o ec ed].
(4) Pôle Ges ion des Mig a eu s Amphihalins dans leu en i onnemen , oFB, in Ae, ins i u Ag o, UniV Pau & Pays Adou /e2s
UPPA, 65 ue de sain -B ieuc, 35000 ennes, F ance.
(5) ins i u de sys éma ique, e olu ion, Biodi e si é, isyeB – UM 7205 – Cn s, MnHn, UPMC, ePHe, Muséum na ional d’His oi e
na u elle, so bonne Uni e si és, 57 ue Cu ie CP26, 75005 Pa is, F ance. [email p o ec ed], [email p o ec ed]
* Co esponding au ho
Mi ogenome o onco hynchus go buscha De n y s e a l .
112 Cybium 2024, 48(2)
seems o be limi ed (Mo e al., 2018; Beaula on e al., 2021),
excep maybe on sea lamp ey Pe omyzon ma inus Linnae-
us, 1758 (A ms ong e al., 2018; Mo e al., 2018; Bonnyaud
and Denys, 2021). Howe e , i was demons a ed ha he
p esence o ish ca casses a e spawning en iches he i e s
wi h ma ine nu ien s ha po en ially impac he ecosys em
(A ms ong e al., 2018; Mo e al., 2018). i can also p o-
ide new high-income eeding oppo uni ies h ough egg o
y consump ion by na i e species ( aspu ina e al., 2016;
Dunlop e al., 2021). F ance eco ded he sou he nmos pink
salmon occu ences in Eu ope wi h a i s obse a ion in he
Canche i e (Pas-de-Calais depa men ) and wo obse a-
ions in B i anny (Cô es-d’A mo and Finis è e depa men s)
in 2017, ollowed by six addi ional obse a ions: wo in he
B esle i e (seine-Ma i ime depa men , no mandy), one
in he somme i e (somme depa men ) and in he Légue
i e (Finis è e depa men ) and wo o he s in he Manche
depa men in 2021 (Beaula on e al., 2021; Bonnyaud and
Denys, 2021).
hese obse a ions we e done mainly by angle s o ideo
coun ing-s a ions, so he numbe o occu ences is ce ainly
unde es ima ed. Molecula ools like he en i onmen al DnA
app oach would be necessa y o comple e he ange o me h-
ods used o he su ey o in asi e species (e.g., sepul eda
e al., 2020). se e al s udies al eady used his me hod in he
na i e and newly in aded a eas using as molecula ma k-
e s sequence agmen s o he mi ochond ial nADH2, he
cy och ome oxidase subuni 1 (Coi) and he cy och ome
b ma ke s (Mizumo o e al., 2018; Duda e al., 2021; Ga -
gan e al., 2022). Howe e , he popula MiFish and F ench
en i onmen al DNA (eDNA) s udies on ishes use he 12S
ma ke (e.g., Miya e al., 2015; Valen ini e al., 2016). in he
GenBank sequence eposi o y, wo mi ogenomes a e al eady
a ailable bu hey all lack associa ion o a ouche o an o i-
gin o he han hei ha che y, and he e o e canno be ali-
da ed as e e ence sequences (s ohm e al., 2016).
in his pape , we desc ibe he mi ogenome o O. go -
buscha om a ouche specimen caugh in he no h o
F ance, ob ained by a double-mul iplexing app oach. his
mi ogenome will be help ul o link he di e en molecula
s udies made on his axon, especially hose abou he gene ic
a iabili y wi hin e en and odd yea s popula ions using di -
e en molecula ma ke s (con ol egion, Cy b and nADH2)
ha a e he e o e no di ec ly compa able (e.g., sa o and
U awa, 2017; Podlesnykh e al., 2020) and, as molecula e -
e ence, o molecula iden i ica ion using any ma ke om
DnA ba coding sensu Hebe e al. (2003) o eDnA analy-
ses (sch oe e e al., 2020). We p o ide he diagnos ic si es
o his species on me aba code ma ke s al eady published
o eDnA s udies.
MATERIAL AND METHODS
Vouche
he ouche specimen is s o ed in he na ional ich-
hyological Collec ions o he Muséum na ional d’His oi e
na u elle (MnHn), ca alogued MnHn-iC-2022-0168
(Fig. 1), and o igina es om he CoLisA a chi e (Ma ch-
and e al., 2018). he specimen (443 mm o s anda d leng h
(sL) o 1178 g), a male, was caugh on July 23 d, 2021 in
he B esle i e a eu (no mandy; La : 50.050628 Long:
1.418690), whe e he F ench Biodi e si y Agency (oFB)
ope a es a scien i ic ap since 1981 (Josse e al., 2021).
iden i ica ion was made acco ding o Bagliniè e e al.
(2020): p esence o a hump on he back, black ongue and
elonga ed black spo s on he caudal in.
B ie ma e ial and me hod
DNA ex ac ion was ca ied on a in-clip s o ed in 95%
e hanol on an epMo ion obo using a Mn Biomedical
ex ac ion ki and p o ocol. h ee long o e lapping PC s o
6-7 kbp we e done ollowing Denys e al. (2020). sequenc-
ing was pe o med using a double-mul iplexing app oach
(Hinsinge e al. 2015; Denys e al., 2020). sequencing
was pe o med on illumina Miseq a he iCM (ins i u du
Ce eau e de la Moelle épiniè e, Pa is V) using 250 pai ed-
end s anda d V2. he mi ogenome was assembled wi h he
Geneious 11.2.2 so wa e (Kea se e al., 2012) mapping
Figu e 1. – Vouche o he sequenced mi ogenome, MnHn-
iC-2022-0168, 443 mm sL, B esle i e a eu (seine-Ma i ime
Dep .), 24 h July 2021, oFB coll; c edi pho o: Q. Josse /oFB.
Figu e 2. – Co e age depending on posi ion in he mi ogenome
assembly.
De n y s e a l . Mi ogenome o onco hynchus go buscha
Cybium 2024, 48(2) 113
immed pai ed eads on a e e ence sequence (GenBank
accession numbe eF455489) using he Geneious 11 sensi-
i i y pa ame e se “low sensi i y/ as es ” o he Geneious
mappe , and ca e ully quali y con olled by eye along hei
whole leng h in addi ion o he s anda d con ols. he assem-
bly o he con ol egion (C ) had a misma ch wi h he e e -
ence sequence (Appendix 1), so a second assembly by elon-
ga ion om he assembled sequence wi hou he C was pe -
o med o econs uc he C wi hou cons aining i h ough
he e e ence. he consensus sequence was anno a ed using
Mi oAnno a o (iwasaki e al., 2013).
Sequence quali y
76,484 eads (a e age leng h: 249.6) we e assembled
om he sequencing o he 3 long ange PC s. he ead
co e age h oughou he en i e sequence anges om 438
o 3561, wi h a mean ead co e age o 1147.1 old (Fig. 2).
Assembly s a is ics o each long agmen a e gi en in
able i.
Phylogene ic econs uc ion
Mi ogenomes om wo Onco hynchus go buscha
CM029873 and eF455489 (= nC_010959) as well as en
o he Onco hynchus species: apache ou O. apache (Mill-
e , 1972) MW300342, cu h oa ou O. cla kii ( icha -
son, 1836) KP013107, gila ou O. gilae (Mille , 1950)
MW300335, chum salmon O. ke a (Walbaum, 1792)
AP010773, coho salmon O. kisu ch MF621749, masu salm-
on O. masou (B e oo , 1856) KU523579, ainbow ou
O. mykiss KP013084, sockeye salmon O. ne ka (Walbaum,
1792) MH003639 and chinook salmon O. shawy scha
AF392054 plus a sequence o b own ou Salmo u a Lin-
naeus, 1758 MF621761, a c ic cha Sal elinus alpinus Lin-
naeus, 1758 Mn530962 and eu opean g ayling Thymallus
hymallus (Linnaeus, 1758) Mn852233 we e e ie ed om
GenBank.
sequences alignmen was pe o med using he Clus al
W plugin in Geneious 11.2.2, as well as nucleo ide di e -
si y and pai wise dis ances. he bes e olu iona y model
was in e ed in jModel es (Da iba e al., 2012) and was
G +i+G o bo h Akaike and Bayesian in o ma ion c i e i-
on. Phylogene ic analysis was in e ed by Maximum Likeli-
hood (ML) using RAxML-HPC2 Wo k low on XSEDE ( e -
sion 8.2.10) (s ama akis, 2014) wi h he in e ed subs i u ion
model and 1,000 boo s ap i e a ions on he CiP es science
Ga eway (Mille e al., 2010) online pla o m.
Compa ison o me aba code ma ke s
nine me aba coding ma ke s om ou loci (12s, 16s,
Coi and Cy b) we e es ed ( able ii). Fo each locus, we
able i. – s a is ics abou he assembly o he mi ogenome Onco-
hynchus go buscha (GenBank Accession numbe PP272106) o
he h ee long PC s.
M 1 M 2 M 3
Leng h (bp) 6748 5385 5382
n eads 44685 14709 20150
Co e age
min-max
(a e age; sD)
913-3561
(1702.1; 369.4) 438-1489
(695.4; 220.8) 455-1902
(871.0; 226.4)
eads leng hs
min-max
(a e age; sD)
221-251
(249.2; 6.4) 224-251
(248.9; 8.1) 224-251
(248.1; 8.1)
able ii. – Me aba coding p ime s commonly used in he li e a u e and es ed in his s udy o disc imina e Onco hynchus go buscha om
o he in oduced Onco hynchus species.
Locus P ime s sequence 5’-> 3’ Amplicon
leng h (bp) e e ence
12s
MiFish Fo wa d: G CGG AAAAC CG GCCAGC
e e se: CA AG GGGG A C AA CCCAG G 170 Miya e al. (2015)
eleo Fo wa d: ACACCGCCCG CAC C
e e se: C CCGG ACAC ACCA G 63 Valen ini e al. (2016)
eleo2 Fo wa d: AAAC CG GCCAGCCACC
e e se: GGG A C AA CCCAG G 166 abe le e al. (2018)
12s-V5 Fo wa d: AGA ACCCCAC A GC
e e se: AGAACAGGC CC C AG 99 iaz e al. (2011)
16s
Fish16sFD/16s2 Fo wa d: GACCC A GGAGC AGAC
e e se: CGC G A CCC AD G AAC 205 Be y e al. (2017)
16sa /16sb Fo wa d: CGCC G A CAAAAACA
e e se: CCGG C GAAC CAGA CACG 581 Duke and Bu on (2020)
Coi
FishF1/Fish 1 Fo wa d: C CAACCAACCACAAAGACA GG
e e se: AGAC C GGG GGCCAAAGAA CA 658 Wa d e al. (2005)
mlCoiin F/jgHCo2198 Fo wa d:
GGWACWGGW GAACWG W AyCCyCC
e e se: AiACy CiGG GiCC AA AAyCA
313 Le ay e al. (2013)
Cy B L14912-CyB/H15149-
CyB Fo wa d: CC AGCCA ACAy AyAC
e e se:
GG GGCKCC CAGAAGGACA GKCCyCA
234 Minamo o e al. (2012)
Mi ogenome o onco hynchus go buscha De n y s e a l .
114 Cybium 2024, 48(2)
compa ed ou sequence wi h hose o he ou Onco hyn-
chus species in oduced in F ance a ailable on GenBank and
associa ed wi h a ouche (Appendix 2). Diagnos ic si es
cha ac e izing species we e hen iden i ied wi h he QUID-
DiCH package (Kühn and Hasse, 2019) o ( Co e eam,
2022).
RESULTS AND DISCUSSION
Sequence desc ip ion and phylogene ic analysis
he newly ob ained mi ogenome has a o al leng h o
16,695 bp and ollows he s anda d e eb a e o de , simi-
la o al eady published mi ogenome o O. go buscha: 13
p o ein-coding genes including six coding wi h an incom-
ple e codon s op (Coii, A P6, Coiii, nADH3, nADH4
and Cy b), 22 ans e nA genes including wo nA-Leu
and 2 nA-se , wo ibosomal nA genes and a con ol
egion (Fig. 2; Appendix 3). in e genic spaces and o e lap-
ping sequences we e ound. he base composi ion o he
en i e genome was 27.9% o A, 26.4% o T, 28.7% o C
and 17.0% o G. As o he wo sequences o O. go buscha
a ailable on GenBank, he mi ogenome CM029873 is
e e sed in he da abase and had o be e e se complemen ed
o align wi h he da ase in s anda d o de . he con ol egion
o he mi ogenome eF455489 does no ha e he same leng h
(1131 bp s. 1041 bp). P e ious gene ic s udies al eady high-
ligh ed leng h he e oplasmy among pink salmon popula ions
wi h his ma ke wi h inse ions and dele ions (B yko e al.,
1999; Chu iko and Gha e , 2002; sa o and U awa, 2017).
Alignmen o ou sequence wi h all C sequences om Gen-
Bank p o ided a 100% ma ch wi h he haplo ype OGDL-8
(sequence LC191999), one o he haplo ypes widesp ead in
Japan (sa o and U awa, 2017).
he ML phylogeny (Fig. 3) is consis en wi h shedko
e al. (2013) on mi ochond ial da a showing gene ally high
suppo alues o nodes as well as wi h he nuclea AG1
ma ke opology (shedko e al., 2012). i di e s om phylo-
gene ic ees o Ho eo (2017) and Gong e al. (2017) by he
posi ion o O. masou, which is no a a basal posi ion wi hin
he Onco hynchus spp. bu wi h a weak obus ness. C espi
and Ful on (2004) al eady demons a ed ha he posi ion o
O. masou depends o he ma ke s analysed and he phyloge-
ne ic econs uc ion me hod. ou O. go buscha mi ogenome
g oups well wi h he wo o he sequences a ailable on Gen-
Bank, co obo a ing i s iden i ica ion.
Finally, we es ed me aba coding ma ke s o ou genes
(12s, 16s, Coi, Cy b) in o de o know i O. go buscha can
easily be dis inguished om he ou o he Onco hynchus
species used o es ocking in non-Ame ican a eas. O. go -
buscha is dis inguished o e hese ou genes by 10 diagnos-
ic si es on he 12s ( able iii), 34 on he 16s ( able iV), 82
on he Coi ( able V) and 61 on he Cy b ( able Vi). MiFish
(Miya e al., 2015) and eleo2 p ime s ( abe le e al., 2018)
be ween he posi ions 246/250 and 416 di e en ia e all 4
species ( able iii). Howe e , he agmen s co esponding o
he 12V-5 p ime s ( iaz e al., 2011) be ween he posi ions
444 and 543 and he eleo p ime s (Valen ini e al., 2016)
be ween he posi ions 849 and 912, while hey disc imina e
well O. go buscha om o he Onco hynchus species, ha e
Figu e 3. – Maximum Likelihood phylogene -
ic ee o Onco hynchus mi ogenomes; boo -
s ap alues beside he nodes.
De n y s e a l . Mi ogenome o onco hynchus go buscha
Cybium 2024, 48(2) 115
able iii. – Diagnos ic si es de e mined on he 12s ma ke o Onco hynchus go buscha, O. kisu ch, O. mykiss and O. shawy scha. Diag-
nos ic si es a e in bold. he MiFish and eleo2 agmen s (Miya e al., 2015; abe le e al., 2018) be ween he posi ions 246/250 and 416,
he 12V-5 agmen ( iaz e al., 2011) be ween he posi ions 444 and 543 as well as he eleo agmen (Valen ini e al., 2016) be ween he
posi ions 849 and 912 a e highligh ed in g ey.
MiFish / eleo2 12V-5 eleo
32 38 63 118 122 128 197 307 349 355 370 390 463 490 561 592 643 662 699 730 736 738 747 788 795 864 882 936 947
O. go buscha A G A A A A A G G C G G C G CA c A
O. kisu ch . G c. C G G G C . cC G A . . . A . . C A C G G C
O. mykiss cG . AC G . . C . . . G A . c. . A. . C A C . G G C
O. shawy scha . G . . C G . . C G. C . . A . c C A C G G C
able iV. – Diagnos ic si es de e mined on he 16s ma ke o Onco hynchus go buscha, O. kisu ch, O. mykiss and O. shawy scha. Diag-
nos ic si es a e in bold. he Fish16sFD/16s2 agmen s (Be y e al., 2017) be ween he posi ions 1170 and 1357 and he 16sa /16sb
agmen (Duke and Bu on, 2020) be ween he posi ions 931 and 1512 a e highligh ed espec i ely in da k and ligh g ey.
18 19 20 29 38 40 44 52 57 59 70 98 114 115 117 118 121 132 149 162 163 164 171 176 180 189 193
O. go buscha C C A C c G A CG A – – G – – G A – cA
O. kisu ch A . . . C A A C G . A G . – c– . – – . . . – .
O. mykiss . A c . . C A A C G GA G . – . – . – – . . c– G
O. shawy scha . A . . –. C A A C G . A G c A .A A A G A c . .
241 245 265 266 267 300 309 315 425 427 444 465 470 545 549 550 617 619 648 669 718 721 751 757 759 773 795
O. go buscha Ac c CGAc G A A G G AA c –G G A AG A
O. kisu ch . . A . . . C G A A . C . . C A A . . C . A C
O. mykiss c A . c. C G A A GCc cC . .cCcA C
O. shawy scha . . A G . AC G A A . C . . C . . G. C . A C
16sa /16sb 16sa /16sb + Fish16sFD/16s2
808 816 819 823 831 844 864 881 949 1087 1131 1169 1182 1186 1194 1263 1292 1294 1308 1312 1340 1351 1352 1562 1665
O. go buscha A G G C A C G GC c A/– AA C G A A GAA
O. kisu ch .GA A . . . . A . C A C C G C .A. . A G
O. mykiss c. A A . c A . A . C A C C . C . . . G A . G
O. shawy scha . . A A . . AA C A C C . C . c. . . A . G
able V. – Diagnos ic si es de e mined on he Coi ma ke o Onco hynchus go buscha, O. kisu ch, O. mykiss and O. shawy scha. Diag-
nos ic si es a e in bold. he FishF1/Fish 1 agmen s (Wa d e al., 2005) be ween he posi ions 48 and 706 and he mlCoiin F/jgCo2198
agmen (Le ay e al., 2013) be ween he posi ions 393 and 706 a e highligh ed espec i ely in ligh and da k g ey.
FishF1/Fish 1
21 99 102 108 114 117 123 132 144 148 153 156 159 162 174 210 213 228 258 267 270 276 282 285 294 315
O. go buscha cAc A GAAAAAC G C CAA G A A A A c G
O. kisu ch . G A.GG . G . c C . G . . C G C
O. mykiss G G . G. G GG . A. . C . G G A C G C
O. shawy scha G . . . G . G . . . . C G . . C G C
FishF1/Fish 1 FishF1/Fish 1 + mlCoiin F/jgCo2198
318 327 339 348 354 363 366 372 378 384 402 408 423 426 429 432 438 468 480 498 507 516 519 525 546 552
O. go buscha c c C/ cC C G G A c c c A G GcAAAA
O. kisu ch G A G. . A . C C C A . C A . GC . .
O. mykiss G A . G AACCC . C A . . c c c
O. shawy scha A A C A. . A cCAC A GC A . C . .
FishF1/Fish 1 + mlCoiin F/jgCo2198
561 564 568 579 586 591 594 603 615 618 627 643 651 666 669 672 675 729 738 744 747 756 783 789 792 804
O. go buscha G A A CAC c G A G G c A/G AcC GC
O. kisu ch . . G . C . C A C C G A C G C GCc . A .
O. mykiss c. G C .cC A C C G A C G C cC . . cA .
O. shawy scha .AG C . C . . C A C C G A C G C . C . . . A
813 819 822 831 834 843 846 861 873 885 888 891 909 915 930 957 993 1005 1017 1024 1029 1035 1044 1053 1062 1065
O. go buscha G A AAG c G cC G GCc A AG G c CA c c G c
O. kisu ch . . C . A A A c . A . G GA A . G . AA
O. mykiss A G C . A G. . A. A A/ G . A A G c A
O. shawy scha . . C GA A . A . AA . G . A A . G . A
1068 1083 1098 1099 1122 1125 1146 1152 1188 1194 1208 1209 1212 1215 1224 1227 1275 1278 1287 1293 1299 1302 1305 1326 1332 1344
O. go buscha c c c G A A c C C GAcCc A C A G C G G
O. kisu ch C cC C G. G A . . . A G . . . A A
O. mykiss C . C .GG A . . cA . . . . . . A A
O. shawy scha C . C C . . G A A . A . . G. . A. A A
1347 1359 1368 1380 1384 1443 1459 1470 1491 1500 1506 1515 1518 1524 1527 1536 1541 1546
O. go buscha AG C C A A AGC C G A GAG
O. kisu ch G . . . . G A GA . . . A . A A
O. mykiss GA.A c GcA . A . A . A . A A
O. shawy scha G . . . G A . A . . . GAGA A

Mi ogenome o onco hynchus go buscha De n y s e a l .
116 Cybium 2024, 48(2)
he exac same sequence o wo (12V-5) o all h ee ( eleo)
o he species making hei dis inc ion impossible. Fo he
o he ma ke s used o 16s, Coi and Cy b genes, all species
a e dis inguishable ( ables iV-Vi).
hus, his mi ogenome can be used as a sequence o e -
e ence o di e en molecula expe ise using mul iple ma k-
e s such as eDnA o con ol o mislabelling ood (Wang e
al., 2021).
Acknowledgemen s. – his wo k was suppo ed by he Muséum
na ional d’His oi e na u elle (MnHn), he UA Pa ina 2006, he
UM Bo eA 8067 and he F ench Biodi e si y Agency (oFB).
We hank he eam om he Long e m obse a o y o he B esle
esponsible o he cap u e o he specimen used in his s udy and
also he cu a ion s a o he INRAE ish collec ions (COLISA) o
sending in clip, as well as Lau en Beaula on (OFB/INRAE) who
suppo s his s udy. Labo a o y access and assis ance was p o ided
by he “Se ice de Sys éma ique Moléculai e” o he MNHN (UAR
2AD 2700). he au ho s hank wo anonymous e iewe s o hei
use ul commen s.
REFERENCES
A izono n., yamada M., nakamu a-Uchiyama F. & ohnishi K.,
2009. Diphyllobo h iasis associa ed wi h ea ing aw Paci ic
salmon. Eme g. In ec . Dis., 15(6): 866-870. h ps://doi.
o g/10.3201/eid1506.090132
A ms ong J. D., Bean C. W. & Wells A., 2018. he sco ish in a-
sion o pink salmon in 2017. J. Fish Biol., 93: 8-11. h ps://doi.
o g/10.1111/j b.13680
Bagliniè e J.-L., Josse Q. & Beaula on L., 2020. Le saumon à
bosse ou saumon ose. In: Kei h P., Poule n., Denys G., Chan-
geux ., Feun eun e. & Pe sa H. (eds), Les Poissons d’eau
douce de F ance. Mèze, Bio ope édi ions ; Pa is, Publica ions
scien i iques du Muséum na ional d’His oi e na u elle: 512-
513.
Beaula on L., Josse Q. & Bagliniè e J.-L., 2021. Le saumon ose
(Onco hynchus go buscha, Walbaum, 1792) – Condui e à eni
e élémen s d’écologie. epo oFB, in Ae, AG oCAMPUs
oUes , Uni e si é de Pau e des pays de l’Adou /e2s UPPA:
25 p.
Be y . e., os e iede s. K., Mu ay D. C., Coghlan M. L., ich-
a ds on A. J., G ealy A. K., s a M., Beide L. & Bunce M.,
2017. DnA me aba coding o die analysis and biodi e si y: A
case s udy using he endange ed Aus alian sea lion (Neophoca
cine ea). Ecol. E ol., 7: 5435-5453. h ps://doi.o g/10.1002/
ece3.3123
Bonnyaud M. & Denys G., 2021. P emiè e occu ence de deux
espèces in asi es de poissons dans le leu e Somme : le Sau-
mon ose du Paci ique e le Gobie demi-lune. L’A oce e, 45(2):
27-35.
B yko V. A., Polyako a n., sku ikhina L. A., Kukhle sky A. D.,
Ki illo a o. n., Chu iko D., Pudo kin A. i. & Gha e A. J.,
1999. Analysis o m DnA indica es weak empo al gene ic he -
e ogenei y in pink salmon spawning uns in wo i e s on
sakhalin island. J. Fish Biol., 55: 617-635. h ps://doi.
o g/10.1111/j.1095-8649.1999. b00703.x
Chu iko D. & Gha e A. J., 2002. Compa a i e phylogeog aphy
o he wo pink salmon b oodlines: an analysis based on a mi o-
chond ial DnA genealogy. Mol. Ecol., 11: 1077-1101. h ps://
doi.o g/10.1046/j.1365-294X.2002.01506.x
C espi B. J. & Ful on M. J., 2004. Molecula sys ema ics o salmo-
nidae: combined nuclea da a yields a obus phylogeny. Mol.
Phylogene . E ol., 31: 658-679. h ps://doi.o g/10.1016/j.
ympe .2003.08.012
able Vi. – Diagnos ic si es de e mined on he Cy b ma ke o Onco hynchus go buscha, O. kisu ch, O. mykiss and O. shawy scha.
Diagnos ic si es a e in bold. he L14912-CyB/H15149-CyB agmen s (Minamo o e al., 2012) be ween he posi ions 48 and 706 is high-
ligh ed in g ey.
L14912-CyB/H15149-CyB
24 72 78 81 108 115 120 121 126 147 165 168 189 198 204 207 219 222 234 240 243 252 258 276 288 300 309 315
O. go buscha ACCC c c CA c C C C c c A C A G /G G/A
O. kisu ch . C . . . C . C C . . . C A . A . . A A . C
O. mykiss c .AC C C c . . C A . A . cA A cC
O. shawy scha . C . . C . C C . . . C A AG. A A . C
L14912-CyB/H15149-CyB
318 324 341 345 378 381 384 387 390 414 417 447 450 453 462 465 468 471 489 492 498 501 513 522 549 558 567 573
O. go buscha AA G C A c A C G c c C G c G c A c c
O. kisu ch . C A . . C G A A . C C . A C A A A . . G C C C .
O. mykiss GC A . . C . . A AC C AC/A C A A A . G c C C C c
O. shawy scha C A c C . . A . C C . GC A A A c. G C C C
579 591 624 627 630 639 645 657 660 663 666 684 690 693 708 711 714 717 723 729 732 744 748 750 774 777 783 786
O. go buscha Ac G A G C C G C c c G A A c A C A C A G
O. kisu ch . A G. . . C C . . A A . C . GC . C . . C C .
O. mykiss G . . A C . . A A c A c . C C . C C A
O. shawy scha . A . c. . C C c A A . C . . C . C G. C C .
789 795 804 816 819 825 831 840 849 852 876 891 903 906 912 915 918 927 943 945 960 970 975 978 981 982 984 987
O. go buscha CGC A A C C c G C C A AA A A A
O. kisu ch . A . GCG c C . . . G . . A A CcCG.ccG C . G G
O. mykiss GA . C . . C c. Gc. . . C C /A c. . G C . . .
O. shawy scha . A . . C . . C . . G . A C C . G. . G C c. .
1003 1017 1026 1029 1035 1038 1044 1047 1053 1057 1059 1065 1068 1071 1083 1090 1098 1116 1119
O. go buscha C A C A G C C G AA C G A A
O. kisu ch G .GC A . . . . . G.C.AC .
O. mykiss . . . C c . /A .c . C . cC .
O. shawy scha . . . . C A . c.A. . . C A G CG
De n y s e a l . Mi ogenome o onco hynchus go buscha
Cybium 2024, 48(2) 117
Da iba D., aboada G. L., Doallo . & Posada D., 2012. jModel-
es 2: mo e models, new heu is ics and pa allel compu ing.
Na . Me hods, 9: 772. h ps://doi.o g/10.1038/nme h.2109
Denys G. P. J., secci-Pe e o G. & Gomes Dos san os A., 2020.
he comple e mi ochond ial genome o Thymallus hymallus
(Linnaeus, 1758) (Ac inop e ygii, salmonidae) ob ained by
long ange PC s and double mul iplexing. Cybium, 44(2):
91-94. h ps://doi.o g/10.26028/cybium/2020-442-001
Duda J. J., Hoy M. s., Chase D. M., Pess G. ., B enkman s. J.,
Mchen y M. M. & os be g C. o., 2021. en i onmen al DnA is
an e ec i e ool o ack ecolonizing mig a o y ish ollowing
la ge-scale dam emo al. En i on. DNA, 3: 121-141. h ps://
doi.o g/10.1002/edn3.134
Duke E. M. & Bu on R. S., 2020. E icacy o me aba coding o
iden i ica ion o ish eggs e alua ed wi h mock communi ies.
Ecol. E ol., 10: 3463-3476. h ps://doi.o g/10.1002/ece3.6144
Dunlop K., Elo an a A. P., Schoen E., Wip li M., Jensen J. L. A.,
Muladal . & Ch is ense G. n., 2021. e idence o ene gy and
nu ien ans e om in asi e pink salmon (Onco hynchus
go buscha) spawne s o ju enile A lan ic salmon (Salmo sala )
and b own ou (Salmo u a) in no he n no way. Ecol.
F eshw. Fish, 30: 270-283. h ps://doi.o g/10.1111/e .12582
F oese . & Pauly D., 2022. FishBase. Wo ld Wide Web elec onic
publica ion. www. ishbase.o g, e sion (02/2022).
Ga gan L. M., Mo . A., Ca lsson J. e. L., Ball B., Fossøy F. &
Ca lsson J., 2022. De elopmen o an en i onmen al DnA
assay and ield alida ion o he de ec ion o in asi e pink
salmon Onco hynchus go buscha. En i on. DNA, 4: 284-290.
h ps://doi.o g/10.1002/edn3.250
Gong L., Liu L.-Q., Guo B.-y., ye y.-y. & Lü Z.-M., 2017. he
comple e mi ochond ial genome o Onco hynchus masou o -
mosanus (salmoni o mes: salmonidae) and phylogene ic s ud-
ies o salmoninae. Conse . Gene . Resou ., 9: 281-284. h ps://
doi.o g/10.1007/s12686-016-0673-1
Hea d W. ., 1991. Li e his o y o Pink salmon Onco hynchus go -
buscha. In: G oo C. & Ma colis (eds), Paci ic salmon Li e
His o ies. Vancou e , UBC P ess: 119-230.
Hebe P. D. n., a nasingham s. & De Waa d J. ., 2003. Ba cod-
ing animal li e: cy och ome c oxidase subuni 1 di e gences
among closely ela ed species. P oc. R. Soc. Lond. B., 270:
s96-s99. h ps://doi.o g/10.1098/ sbl.2003.0025
Hinsinge D. D., Deb uyne ., homas M., Denys G. P. J., Men-
nesson M., U ge M. & De ai A., 2015. Fishing o ba codes in
he o en : om Coi o comple e mi ogenomes on nGs pla -
o ms. DNA Ba codes, 3: 170-186. h ps://doi.o g/10.1515/dna-
2015-0019
Ho eo J. L., 2017. e isi ing he mi ogenomic phylogeny o sal-
moninae: new insigh s hanks o ecen sequencing ad ances.
Pee J, 5: e3828. h ps://doi.o g/10.7717/pee j.3828
iwasaki W., Fukunaga ., isagozawa ., yamada K., Maeda y.,
sa oh . P., sado ., Mabuchi K., akeshima H., Miya M. &
nishida M., 2013. Mi oFish and Mi oAnno a o : A mi ochon-
d ial genome da abase o ish wi h an accu a e and au oma ic
anno a ion pipeline. Mol. Biol. E ol., 30: 2531-2540. h ps://
doi.o g/10.1093/molbe /ms 141
Josse Q., Flesselle A., Be na din A., Macque . & Pe i L., 2021.
appo d’ac i i é de l’obse a oi e Long e me de la B esle –
Année 2020. echnical epo o he Pôle Ges ion des Mig a-
eu s Amphihalins dans leu en i onnemen : 49 p.
Kea se M., Moi ., Wilson A., s ones-Ha as s., Cheunung M.,
s u ock s., Bux on s., Coope A., Ma kowi z s., Du an C.,
hie e ., Ash on B., Mein jes P. & D ummond A., 2012.
Geneious Basic: an in eg a ed and ex endable desk op so wa e
pla o m o he o ganiza ion and analysis o sequence da a.
Bioin o ma ics, 28: 1647-1649. h ps://doi.o g/10.1093/bioin-
o ma ics/b s199
Kühn A.L. & Haase M., 2019. QUIDDICH: QUick IDen i ica ion
o Diagnos ic CHa ac e s. J. Zool. Sys . E ol. Res., 58(1):
22-26. h ps://doi.o g/10.1111/jzs.12347
Le ay M., yang J. y., Meye C. P., Mills s. C., Agudelo n., anwez
V., Boehm J. & Machida . J., 2013. A new e sa ile p ime se
a ge ing a sho agmen o he mi ochond ial Coi egion o
me aba coding me azoan di e si y: applica ion o cha ac e iz-
ing co al ee ish gu con en s. F on . Zool., 10: 34. h ps://doi.
o g/10.1186/1742-9994-10-34
Ma chand F., Aymes J.-C., Gue aud F., Domaizon i., Goulon C.,
Hamele V., Lange F., P e os e., Bagliniè e J.-L., Beaula on
L., Penil C., Josse Q., Flesselle A., s a ck A., Jeanno n., He -
a d n., Ma ignon M. & Azam D., 2018 Colisa, he collec ion
o ich hyological samples. h ps://colisa. /. h ps://doi.
o g/10.15454/D3oDJM
Mille M. A., P ei e W. & schwa z ., 2010. C ea ing he
CiP es science Ga eway o in e ence o la ge phylogene ic
ees. In: 2010 Ga eway Compu ing en i onmen s Wo kshop
(GCe). ieee: p. 1-8. h ps://doi.o g/10.1109/GCe.2010.
5676129
Minamo o ., yamanaka H., akaha a ., Honio M. n. & Kawaba a
Z., 2012. Su eillance o ish species composi ion using en i-
onmen al DnA. Limnology, 13: 193-197. h ps://doi.
o g/10.1007/s10201-011-0362-4
Miya M., sa o y., Fukunaga ., sado ., Poulsen J. y., sa o K.,
Minamo o ., yamamo o s., yamanaka H., A aki H., Kondoh
M. & iwasaki W., 2015. MiFish, a se o uni e sal PC p ime s
o me aba coding en i onmen al DNA om ishes: de ec ion
o mo e han 230 sub opical ma ine species. R. Soc. Open Sci.,
2: 150088. h ps://doi.o g/10.1098/ sos.150088
Mizumo o H., U abe H., Kanbe ., Fukushima M. & A aki H.,
2018. es ablishing an en i onmen al DnA me hod o de ec
and es ima e he biomass o sakhalin aimen, a c i ically endan-
ge ed Asian salmonid. Limnology, 19: 219-2277. h ps://doi.
o g/10.1007/s10201-017-0535-x
Mo . A., ho s ad e. B., sandlund o. ., Be n sen H. H., Fiske P.
& Uglem i., 2018. he pink salmon in asion: a no wegian pe -
spec i e. J. Fish Biol., 93: 5-7. h ps://doi.o g/10.1111/
j b.13682
Pe sa H., Kei h P. & Denys G., 2020. Biogéog aphie e his o ique
de la mise en place des peuplemen s ich yologiques de F ance
mé opoli aine. In: Kei h P., Poule n., Denys G., Changeux .,
Feun eun e. & Pe sa H., (eds), Les Poissons d’eau douce de
F ance. Mèze, Bio ope édi ions ; Pa is, Publica ions scien i i-
ques du Muséum na ional d’His oi e na u elle: 43-97.
Podlesnykh A. V., Kukhle sky A. D. & B yko V. A., 2020. A com-
pa a i e analysis o mi ochond ial DnA gene ic a ia ion and
demog aphic his o y in popula ions o e en- and odd-yea
b oodline pink salmon, Onco hynchus go buscha (Walbaum,
1792), om sakhalin island. En i on. Biol. Fish, 103: 1553-
1564. h ps://doi.o g/10.1007/s10641-020-01040-0
Co e eam, 2022. : A language and en i onmen o s a is ical
compu ing. Vienna: De elopmen Co e eam. A ailable a
h p://www. -p ojec .o g/
aspu ina e. n., shus o y. A. & y kin i. A., 2016. eggs o pink
salmon Onco hynchus go buscha as addi ional non- adi ional
ood o ju enile A lan ic salmon Salmo sala in i e s o he
Kola Peninsula. Russ. J. Biol. In asions, 7: 294-296. h ps://
doi.o g/10.1134/s2075111716030115
iaz ., shehzad W., Via i A., Pompanon F., abe le P., Coissac e.,
2011. ecoP ime s: in e ence o new DnA ba code ma ke s
om whole genome sequence analysis. Nucleic Acids Res.,
39(21): e145. h ps://doi.o g/10.1093/na /gk 732
Mi ogenome o onco hynchus go buscha De n y s e a l .
118 Cybium 2024, 48(2)
sa o s. & U awa s., 2017. Gene ic a ia ion o Japanese pink salm-
on popula ions in e ed om nucleo ide sequence analysis on
he mi ochond ial DnA con ol egion. En i on. Biol. Fish,
100: 1355-1375. h ps://doi.o g/10.1007/s10641-017-0648-4
sch oe e J. C., Maloy A. P., ees C. B. & Ba on M. L., 2020.
Fish mi ochond ial genome sequencing: expanding gene ic
esou ces o suppo species de ec ion and biodi e si y moni-
o ing using en i onmen al DnA. Conse . Gene . Resou ., 12:
433-446. h ps://doi.o g/10.1007/s12686-019-01111-0
sco W. B. & C ossman e. J., 1973. F eshwa e Fishes o Canada.
o awa, Fishe ies esea ch Boa d o Canada: 966 p.
sepul eda A. J., nelson n. M., Je de C. L. & Luika G., 2020. A e
en i onmen al DnA me hods eady o aqua ic in asi e spe-
cies managemen ? T ends Ecol. E ol., 35: 668-678. h ps://doi.
o g/10.1016/j. ee.2020.03.011
shedko s. V., Mi oschnichenko i. L. & namko a G. A., 2012. Phy-
logeny o salmonids (salmoni o mes: salmonidae) and i s
molecula da ing: analysis o nuclea AG1 gene. Rus. J.
Gene ., 48: 575-579. h ps://doi.o g/10.1134/
s1022795412050201
shedko s. V., Mi oschnichenko i. L. & namko a G. A., 2013. Phy-
logeny o salmonids (salmoni o mes: salmonidae) and i s
molecula da ing: analysis o m DnA da a. Rus. J. Gene ., 49:
718-734. h ps://doi.o g/10.1134/s1022795413060112
s ama akis A., 2014. AxML e sion 8: a ool o phylogene ic
analysis and pos -analysis o la ge phylogenies. Bioin o ma -
ics, 30(9): 1312-1313. h ps://doi.o g/10.1093/bioin o ma ics/
b u033
s ohm J. H. ., Gwiazdowski . A. & Hanne ., 2016. nex -gen-
e a ion moni o ing o aqua ic biodi e si y using en i onmen al
DnA me aba coding. Mi ochond ial DNA, 27: 3263-3269.
h ps://doi.o g/10.3109/19401736.2015.1015003
abe le P., Bonin A., Coissac e. & Zinge L., 2018. en i onmen al
DnA: Fo Biodi e si y esea ch and Moni o ing. ox o d,
ox o d Uni e si y P ess: 253 p. h ps://doi.o g/10.1093/
oso/9780198767220.001.0001
Valen ini A., abe le P., Miaud C., Ci ade ., He de J., homsen
P. F., Bellemain e., Besna d A., Coissac e., Boye F., Gabo i-
aud C., Jean P., Poule n., ose n., Copp G. H., Geniez P.,
Pon D., A gillie C., Baudoin J. M., Pe oux ., C i elli A. J.,
oli ie A., Acquebe ge M., Le B un M., Mølle P. ., Will-
e sle e. & Dejean ., 2016. nex -gene a ion moni o ing o
aqua ic biodi e si y using en i onmen al DnA me aba coding.
Mol. Ecol., 25(4): 929-942. h ps://doi.o g/10.1111/mec.13428
Van De Vee G. & nen wig W., 2015. en i onmen al and econom-
ic impac assessmen o alien and in asi e ish species in
eu ope using he gene ic impac sco ing sys em. Ecol. F eshw.
Fish, 24: 646-656. h ps://doi.o g/10.1111/e .12181
Wang N., Xing R.-R., Zhou M.-Y., Sun R.-X., Han J.-X., Zhang
J.-K., Zheng W.-J. & Chen y., 2021. Applica ion o DnA ba -
coding and me aba coding o species iden i ica ion in salmon
p oduc s. Food Addi . Con am. Pa A Chem. Anal. Con ol
Expo. Risk Assess., 38(5): 754-768. h ps://doi.o g/10.1080/194
40049.2020.1869324
Wa d . D., Zemlak . s., innes B. H., Las P. . & Hebe P. D. n.,
2005. DNA ba coding Aus alia’s ish species. Philos. T ans. R.
Soc. B Biol. Sci., 360: 1847-1857. h ps://doi.o g/10.1098/
s b.2005.1716
De n y s e a l . Mi ogenome o onco hynchus go buscha
Cybium 2024, 48(2) 119
Appendix 2. – GenBank accession numbe s o he sequences used as compa ison ma e ial o he ou loci used in me aba code s udies
(12s, 16s, Coi, Cy B) o Onco hynchus go buscha, O. kisu ch, O. mykiss and O. shawy scha.
O. go buscha: PP272106, CM029873, eF455489; O. kisu ch: eF126369, MF621749, MF621751, MH003640; O. mykiss: AF392054,
DQ288268 o DQ288271, HQ167664, HQ167694, HQ167682, KP013084, KP085590, Ky798500, MF621750, M 410879, M 667254,
MZ2567214; O. shawy scha: AF392054, HQ167665
Appendix 1. – sc een cap u es o he p oblema ic map o e e ence mapping a ound posi ion 15985 o sequence eF455489. wo sc een
cap u es o eads o he same a ea a e p esen ed (second is simply sc olled down om he i s ), as he high numbe o eads did no allow
o a clea single pic u e. no ead o e laps bo h sides a once wi hou misma ch, causing co e age o d op o his mapping. Allowing ee
econs uc ion using elonga ion om one o he sides eco e s a di e en sequence wi h high, unambiguous co e age.