A New Mitochondrial Gene Order in the Banded Cusk-Eel Raneya Brasiliensis (Actinopterygii, Ophidiiformes)

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A new mitochondrial gene order in the banded cusk-eel Raneya brasiliensis (Actinopterygii, Ophidiiformes)

Amir Fromm, Stephen D. Atkinson, Gema Alama-Bermejo, Paulyn Cartwright, Jerri L. Bartholomew & Dorothée Huchon

To cite this article: Amir Fromm, Stephen D. Atkinson, Gema Alama-Bermejo, Paulyn Cartwright, Jerri L. Bartholomew & Dorothée Huchon (2019) A new mitochondrial gene order in the banded cusk-eel Raneyabrasiliensis (Actinopterygii, Ophidiiformes), Mitochondrial DNA Part B, 4:1, 1-4, DOI: 10.1080/23802359.2018.1532824 To link to this article: https://doi.org/10.1080/23802359.2018.1532824

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tmdn20 MITOCHONDRIAL DNA PART B 2019, VOL. 4, NO. 1, 1–4 https://doi.org/10.1080/23802359.2018.1532824

MITO COMMUNICATION A new mitochondrial gene order in the banded cusk-eel Raneya brasiliensis (Actinopterygii, Ophidiiformes)

Amir Fromma, Stephen D. Atkinsonb , Gema Alama-Bermejoc , Paulyn Cartwrightd , Jerri L. Bartholomewb and Dorothee Huchona,e aSchool of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel; bDepartment of Microbiology, Oregon State University, Corvallis, OR, USA; cCenter for Applied Research and Technology Transference in Marine Resources Almirante Storni (CIMAS-CCT CONICET-CENPAT), San Antonio Oeste, Argentina; dDepartment of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA; eThe Steinhardt Museum of Natural History and National Research Center, Tel Aviv University, Tel Aviv, Israel

ABSTRACT ARTICLE HISTORY The complete mitochondrial genome of the banded cusk-eel, Raneya brasilensis (Kaup, 1856), was Received 26 June 2018 obtained using next-generation sequencing approaches. The genome sequence was 16,881 bp and Accepted 31 August 2018 exhibited a novel gene order for a vertebrate. Specifically, the WANCY and the nd6 – D-loop regions KEYWORDS were re-ordered, supporting the hypothesis that these two regions are hotspots for gene rearrange- Ophidiidae; mitogenomics; ments in Actinopterygii. Phylogenetic reconstructions confirmed that R. brasiliensis is nested within next-generation Ophidiiformes. Mitochondrial genomes are required from additional ophidiins to determine whether sequencing; phylogeny the gene rearrangements that we observed are specific to the genus Raneya or to the subfam- ily Ophidiinae.

Mitochondrial (mt) gene orders are extremely conserved in were assembled using IDBA-UD as implemented in IDBA-1.1.1 vertebrates. In fish (Actinopterygii), only 35 departures from (Peng et al. 2010) and the fish mt sequence was identified the canonical mt gene order have been described, whereas using BLAST searches. Reads were mapped with Geneious over 2000 species have been sequenced (Satoh et al. 2016). Pro version 9.0.5 using ‘High Sensitivity’ and mapping only In contrast, the vertebrate sister clade – the tunicates – paired reads which ‘map nearby’. Among the 189,000,000 demonstrates extreme gene order variability, in which each reads obtained, the mean coverage of the fish mitogenome of the sequenced genera presents a different gene order was computed with Geneious Pro and estimated to be (Gissi et al. 2010; Rubinstein et al. 2013). Consequently, find- 40,000 (SD 6000; Min ¼ 22,740; Max ¼ 60,423). Annotation ing a new gene order in Actinopterygii is a rare event. The was performed with MitoAnnotator (http://mitofish.aori.u- banded cusk-eel (Raneya brasiliensis [Kaup, 1856]) is a demer- tokyo.ac.jp/annotation/input.html, last accessed 2017 Nov) sal fish present along the eastern coast of South America, (Iwasaki et al. 2013). The complete mt sequence of R. brasi- from southern Brazil to northern Argentina. We report here a liensis was submitted to the DNA databank of Japan (acces- new mt gene order for this species. sion number LC341245). The R. brasiliensis specimen we studied was collected in The fish identification to species level was confirmed by Argentina (43.374000 S 64.901944 W), as bycatch from a constructing a phylogenetic tree based on cox1 sequences, shrimp beam trawler. The sample has been deposited in the as recommended by Botero-Castro et al. (2016). All cox1 Invertebrate collection of Museo de La Plata, FCNyM-UNLP, sequences of Ophidiinae available on 7 December 2017 were Argentina, Acc. Number MLP-CRG 420. Our original aim was downloaded from The National Center for Biotechnology to characterize a myxozoan parasite of this species. DNA was Information (NCBI). Other Ophidiiforms with complete mt extracted from myxozoan-infected tissue using a DNeasy sequences were used as outgroups. Cox1 sequences were Blood & Tissue Kit (Qiagen, Germantown, MD). A dual- aligned with MAFFT 7.308 (Katoh and Standley 2013) under indexed Illumina library was created using a Wafergen the L-ins-i algorithm. A phylogenetic tree was reconstructed Biosystems Apollo 324 NGS Library Prep System (TakaraBio, with RaxML 7.4.2 (Stamatakis 2006) using codon partitions Mountain View, CA), then paired-ended sequencing (150 bp), under the GTRGAMMA model. Bootstrap percentages (BP) was performed on an Illumina HiSeq 3000 (Illumina, San were computed using the rapid bootstrap option. Diego, CA) by the Center for Genome Research and The phylogenetic position of R. brasiliensis among Biocomputing of Oregon State University (USA). DNA reads Ophidiiformes was investigated using all mt protein-coding

CONTACT Dorothee Huchon [email protected] School of Zoology, Sherman building, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel ß 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 A. FROMM ET AL.

(A) Raneya brasiliensis C Q A Y S ψP N 1 IMW S2 D H L1 E P T FV L2 KGR

12s 16S ND1 ND2 COI COII ND4 ND5 CYTB 6 ND3 ATP8 ND COIII ND4L ATP6 D-loop

(B) Standard Acnopterygii gene order

12s 16S ND1 ND2 COI COII ND4 ND5 6 CYTB ND3 ATP8 ND COIII ND4L ATP6 D-loop

FV L KGR E 2 I W Y S D H L T P Q A C 2 S 1 M N 1 (C) Carapus bermudensis

12s 16S ND1 ND2 COI COII ND4 ND5 CYTB ND3 ATP8 ND4L COIII ND6 ATP6 D-loop

FV L2 KGR E T P M I Q W Y S D H L A C 2 S 1 N 1 (D) Ophidiiformes phylogeny Bassozetus zenkevitchi 96 / 1.0 Lamprogrammus niger 73 / 0.98 Raneya brasiliensis* 100 / 1.0 Sirembo imberbis Ophidiiformes 80 / - Carapus 100 / 1.0 bermudensis Cataetyx rubrirostris 100 / 1.0 Diplacanthopoma brachysoma Dactyloptena tiltoni 77 / 1.0 Carangoides armatus Cottus reinii Outgroups 100 / 1.0 Pholis crassispina 100 / 1.0 Lycodes toyamensis 1 Figure 1. Linearized representation of Raneya brasiliensis mt gene order (A) compared with the typical Actinopterygii mt gene order (B) and with Carapus bermudensis mt gene order (C). tRNA genes are designated by single-letter amino acid codes. Genes that have undergone rearrangement in R. brasiliensis (A) and C. bermudensis (C) are connected with lines to their corresponding location in the typical Actinopterygii gene order (B). Genes encoded on the L-strand are underlined. The phylogenetic position of R. brasiliensis and C. bermudensis among Ophidiiformes was reconstructed based on mt protein-coding genes (D). All species possess the typical Actinopterygii mt gene order except R. brasiliensis and C. bermudensis, which are indicated in bold. Bootstrap supports above 50% and Bayesian posterior probabilities are indicated near the corresponding nodes, separated with a slash. The mt sequence of the specimen obtained in this work is indicated in bold and with an asterisk.

genes encoded on the H-strand. The nd6 gene and overlap- WANCY tRNA gene cluster and the nd6 – D-loop region. All ping gene regions were discarded. Each protein-coding gene rearranged genes had retained their original strand direction, was aligned separately with MAFFT, as described above. A as observed in other Ophidiiformes. In R. brasiliensis, the trnN maximum likelihood (ML) tree was reconstructed with RaxML was transposed to the end of the ‘WANCY’ region, presenting 7.4.2 as described above, with different model parameters for a gene order of WACYN (Figure 1(A)). The exact position of each codon partition of each protein-coding gene. In add- the origin of light-strand replication (OL), which is usually ition, a Bayesian reconstruction was performed using located between trnN and trnC in Actinopterygii, could not MrBayes 3.2.2 (Ronquist et al. 2012) for 12,500,000 genera- be determined. Concerning rearrangement of the nd6 – tions under default mcmc settings. The partitions and substi- D-loop region, in the standard mitochondrial gene order the tution models were the same as those for the ML analysis. cytb gene is usually flanked by the trnE and trnT on its 50- The R. brasiliensis mt genome was 16,881 bp, slightly lon- and 30-ends, respectively (Figure 1(B)). In R. brasiliensis, ger than other Ophidiiformes (16,090–16,564 bp). Surprisingly, the cytb gene was flanked by non-coding regions and the we identified that the mt gene order was rearranged com- nd6 þ trnE gene region was transposed downstream of the pared with the standard Actinopterygii gene order (Figure 1). cytb gene. The trnE is now flanked by the trnP at its 30-end. Specifically, we observed different orders in two regions: the This indicated that both nd6 þ trnE and trnT gene regions MITOCHONDRIAL DNA PART B 3

88 Bassozetus zenkevitchi AP004405 Lamprogrammus niger AP004410 Diplacanthopoma brachysoma AP004408 Outgroup 73 Sirembo imberbis AP004406 Lepophidium profundorum KC015508 Lepophidium profundorum KC015509 98 Lepophidium profundorum KC015510 Lepophidium profundorum KC015505 Lepophidium profundorum KC015504 Lepophidium Lepophidium profundorum KC015507 Lepophidium profundorum KC015506 Lepophidium profundorum KF930038 Genypterus blacodes EU074430 Genypterus blacodes HQ611137 Genypterus tigerinus EF609355 Genypterus blacodes EF609354 51 Genypterus blacodes HQ611135 Genypterus blacodes KX781854 Genypterus brasiliensis JQ365365 Genypterus brasiliensis EU074432 Genypterus brasiliensis JQ365366 Genypterus brasiliensis EU074431 Genypterus capensis JF493515 96 Genypterus capensis JF493517 Genypterus capensis HM007744 Genypterus capensis HM007740 Genypterus capensis HM007737 Genypterus capensis HM007746 Genypterus capensis HM007743 Genypterus capensis HM007742 Genypterus capensis HM007738 Genypterus capensis HM007745 Genypterus Genypterus capensis HM007739 Genypterus capensis HM007741 Genypterus capensis HM007736 Genypterus capensis HM007735 Genypterus capensis JF493518 Genypterus capensis JF493514 Genypterus capensis JF493516 Genypterus capensis GU804987 Genypterus blacodes KX781939 Genypterus blacodes KX781862 Genypterus blacodes HQ611136 Genypterus blacodes EU074427 Genypterus blacodes EU074428 Genypterus blacodes EU074429 Genypterus blacodes EU074426 Ophidion holbrookii GU702499 Ophidion holbrookii GU702415 100 Ophidion holbrookii GU702414 Ophidion holbrookii GU702496 Ophidion 62 Ophidion holbrookii GU702416 Ophidion holbrookii GU702417 Lepophidium brevibarbe FJ583626 Lepophidium brevibarbe FJ583623 100 Lepophidium brevibarbe FJ583625 Lepophidium brevibarbe FJ583622 Lepophidium Lepophidium brevibarbe FJ583624 Chilara taylori EU520651 Chilara taylori FJ164459 100 Chilara taylori KF929735 Chilara taylori GU440276 Chilara Chilara taylori KF918867 Chilara taylori JQ354041 Chilara taylori DQ027981 100 Parophidion schmidti JQ841751 Parophidion schmidti GU224999 Parophidion Parophidion schmidti JQ841750 Parophidion schmidti JQ841313 Ophidion marginatum KF930201 Ophidion scrippsae EU520652 97 Ophidion scrippsae GU440437 Ophidion Ophidion scrippsae KF930202 Otophidium dormitator JQ840958 Otophidium Raneya brasiliensis EU074577 Raneya brasiliensis EU074578 Raneya 0.1 99 Raneya brasiliensis* LC341245 Figure 2. Maximum likelihood tree of Ophidiinae cox1 sequences. The cox1 sequence of the specimen obtained in this work is indicated in bold and with an asterisk. Bootstrap supports above 50% are indicated near the corresponding node. have been transposed. The trnT is now found downstream to Our phylogenetic reconstruction based on cox1 sequences the D-loop (or control region), and is flanked at its 30-end by (Figure 2) confirmed that the obtained sequence clusters a pseudo-trnP, which suggests that the transposition of the with other R. brasiliensis (EU074577 and EU074578 trnT involved the duplication of the trnT þ trnP region (Mabragana~ et al. 2011)) with maximal support value (Figure 1(A)). (BP ¼ 100). The 652 bp cox1 sequences of the three 4 A. FROMM ET AL. specimens differed by 1–2 nucleotides only, supporting the Funding correct identification of our sample. We then investigated the This work was supported by the United States-Israel Binational Science position of R. brasiliensis within the Ophidiiformes using mt Foundation [Grant No. 2015010 to D.H. and P.C.]. protein coding sequences (Figure 1(D)). We found that Raneya (Ophidiinae) was a sister clade of the Neobythitinae Bassozetus zenkevitchi and Lamprogrammus niger with high ORCID support (BP ¼ 73; posterior probability PP ¼ 0.98). In agree- Stephen D. Atkinson http://orcid.org/0000-0002-7180-6672 ment with Miya et al. (2003), our analyses did not recover Gema Alama-Bermejo http://orcid.org/0000-0002-6452-6154 the monophyly of Ophidiidae, as Carapus bermudensis Paulyn Cartwright https://orcid.org/0000-0002-8174-6933 (Carapidae, Carapinae) is the sister clade of Sirembo imberbis Jerri L. Bartholomew https://orcid.org/0000-0002-8174-6933 (Neobythitinae) (Figure 1(D)). Dorothee Huchon http://orcid.org/0000-0002-5047-244X Mitochondrial gene order is highly conserved among vertebrates, thus finding a novel rearrangement is a rare event. In this study, we identified multiple unique rearrangements References in R. brasiliensis, a representative of the Ophidiiformes. Interestingly mt rearrangements have been described in Botero-Castro F, Delsuc F, Douzery EJP. 2016. Thrice better than once: quality control guidelines to validate new mitogenomes. another member of the Ophidiiformes – C. bermudensis (Miya Mitochondrial DNA Part A. 27:449–454. et al. 2003; Satoh et al. 2016). However, the rearrangements Gissi C, Pesole G, Mastrototaro F, Iannelli F, Guida V, Griggio F. 2010. in Carapus and Raneya differ. In Carapus, they involve the Hypervariability of ascidian mitochondrial gene order: exposing the trnP and trnM, which are located downstream of the D-loop myth of deuterostome organelle genome stability. Mol Biol Evol. 27: (Figure 1(C)). Our phylogenetic analyses (Figure 1(D)) showed 211–215. that Carapus and Raneya are not closely related, and are Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, both more closely related to species that have a standard Sado T, Mabuchi K, Takeshima H, Miya M, et al. 2013. MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an Actinopterygii gene order. These findings support the accurate and automatic annotation pipeline. Mol Biol Evol. 30: hypotheses that mt rearrangements occurred independently 2531–2540. in Carapus and Raneya, and that the Ophidiiformes constitute Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment soft- a hotspot for gene rearrangement. ware version 7: improvements in performance and usability. Mol Biol Gene rearrangements in Actinopterygii occur more fre- Evol. 30:772–780. ~ ı quently in the WANCY and the region from the nd5 to the D- Mabragana E, D az de Astarloa JM, Hanner R, Zhang J, Gonzalez Castro M. 2011. 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Research in three separate events of duplication with multiple gene Computational Molecular Biology: 14th Annual International losses, in the lineage leading to Raneya. Additional sequenc- Conference, RECOMB 2010, Lisbon, Portugal, April 25-28, 2010 ing of members of the Ophidiinae should shed light on the Proceedings. Berlin, Heidelberg: Springer Berlin Heidelberg; p. origins of the novel Raneya gene order. Additional data 426–440. € should also reveal whether the gene order we observed in Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: effi- Raneya is shared by other members of the Ophidinae or cient Bayesian phylogenetic inference and model choice across a large whether it is specific to Raneya. model space. Syst Biol. 61:539–542. Rubinstein ND, Feldstein T, Shenkar N, Botero-Castro F, Griggio F, Mastrototaro F, Delsuc F, Douzery EJP, Gissi C, Huchon D. 2013. Deep Disclosure statement sequencing of mixed total DNA without barcodes allows efficient No potential conflict of interest was reported by the authors. assembly of highly plastic ascidian mitochondrial genomes. Genome Biol Evol. 5:1185–1199. Satoh TP, Miya M, Mabuchi K, Nishida M. 2016. Structure and variation of Acknowledgements the mitochondrial genome of fishes. BMC Genomics. 17:719. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogen- We thank Naomi Paz for her help with English editing and Dayana etic analyses with thousands of taxa and mixed models. Yahalomi for her help with the assemblies. Bioinformatics. 22:2688–2690.