Mitochondrial DNA The Journal of DNA Mapping, Sequencing, and Analysis

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Complete male mitochondrial genomes of European Mytilus edulis mussels Beata Śmietanka, Roman Wenne & Artur Burzyński To cite this article: Beata Śmietanka, Roman Wenne & Artur Burzyński (2014): Complete male mitochondrial genomes of European Mytilus edulis mussels, Mitochondrial DNA To link to this article: http://dx.doi.org/10.3109/19401736.2014.958704

Published online: 10 Sep 2014.

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Date: 14 September 2015, At: 06:36

http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–2 ! 2014 Informa UK Ltd. DOI: 10.3109/19401736.2014.958704

MITOGENOME ANNOUNCEMENT

Complete male mitochondrial genomes of European Mytilus edulis mussels Beata S´mietanka, Roman Wenne, and Artur Burzyn´ski

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Institute of Oceanology, Polish Academy of Sciences, Sopot, Poland

Abstract

Keywords

Doubly uniparental inheritance (DUI) results in the existence of two gender-specific, divergent mtDNA lineages within a single species. Under DUI, the female genome (F) is transmitted from mothers to the whole offspring, and the male genome (M) is transmitted exclusively from fathers to sons. This system was first described in a marine mussels Mytilus edulis inhabiting European coastal waters, over a decade ago. Despite that, the complete sequence of the M genome from the European M. edulis mussels remained unknown. Here we announce it for the first time. The announcement is based on the two haplotypes isolated from heteroplasmic males of European M. edulis sampled at two moderately distant locations: southern North Sea and western Baltic. The two M genomes are quite similar both in length (16,631 and 16,632 bp) and in sequence (98.3%). Furthermore, both newly sequenced genomes are closely related to the genomes described from Baltic M. trossulus.

DUI, East Atlantic, European mussels, mitogenomics

Marine mussels of the Mytilus edulis species complex, consisting of three recognized members: M. edulis, M. trossulus and M. galloprovincialis, all exhibit the unusual DUI system of mitochondrial DNA inheritance (Skibinski et al., 1994; Zouros et al., 1994). In this system, the two mitochondrial genomes are substantially divergent (420%). Consequently, there should be six mitochondrial lineages within this species complex. However, due to hybridization, introgression and isolation events, the situation is more complex, as discussed by S´mietanka et al. (2010). Two distinct M lineages exist in the Atlantic M. edulis: one in the western Atlantic (American) and the second, in the eastern Atlantic (European) (Riginos et al., 2004). The full sequence of the American M genome has been published (Breton et al., 2006), but that of the European M. edulis has not. Based on shorter fragments, it was suggested that these genomes are similar to the M genomes present at low frequencies in Baltic M. trossulus (S´mietanka et al., 2009; Zbawicka et al., 2007). Here we announce, for the first time, the complete sequences of the two mitochondrial M genomes isolated from the European M. edulis mussels. They are representative for the whole European population, based on our earlier survey (S´mietanka et al., 2009). The two male individuals were: WES36, sampled in the North Sea (The Netherlands, Western Scheldt) and MEB55 sampled in the western Baltic Sea (Germany, Mecklenburg Bight). Taxonomic identification of both individuals was performed previously by Kijewski et al. (2011). In the two diagnostic markers: ME 15/16 and EF-bis all their alleles corresponded to M. edulis. The complete M sequences were obtained in two steps: the highly specific long range PCR, followed by re-amplifications and direct sequencing of shorter Correspondence: Artur Burzyn´ski, Institute of Oceanology, Polish Academy of Sciences, Powstan´co´w Warszawy 55, 81-712 Sopot, Poland. Tel: 48587311764. E-mail: [email protected]

History Received 13 August 2014 Accepted 23 August 2014 Published online 10 September 2014

PCR products (S´mietanka et al., 2010). Sequences of all used primers are available from the authors upon request. Both annotated genomes have been deposited in GenBank under accession numbers HM489873 and HM489874. The nucleotide composition of the newly sequenced genomes has a typical bias towards A + T (63.3%), the number and order of genes is the same as in all other published M. edulis mitochondrial genomes. Both genomes have almost the same length: curiously one of the trnM genes is one bp longer in MEB55. The genetic distances between the newly sequenced European M. edulis Table 1. Genetic distances between the newly sequenced and closely related M genomes of Mytilus mussels.

EUR AME BAL

EUR

AME

BAL

0.0166 ± 0.0014 0.0416 ± 0.0032 0.0235 ± 0.0020

0.0767 ± 0.0040 0.0124 ± 0.0013 0.0287 ± 0.0026

0.0212 ± 0.0009 0.0773 ± 0.0033 0.0192 ± 0.0009

EUR – two newly sequenced European M. edulis M genomes, accession numbers HM489873 and HM489874; AME – two M genomes of American M. edulis, accession numbers: AY823623 and AY823624 (Breton et al., 2006); BAL – two M genomes of Baltic M. trossulus, accession numbers: KM192129 and DQ198225 (Zbawicka et al., 2007, 2014). The values above the diagonal and at the diagonal were calculated as the number of base substitutions per site from averaging over all sequence pairs between or within groups, using the Maximum Composite Likelihood model (Tamura et al., 2004). This analysis was based on the alignment of the complete genomes (16,563 positions), with the rate variation among sites modelled with gamma distribution (shape parameter ¼ 0.2). The values below diagonal were calculated based on concatenated alignment of all protein-coding sequences (3918 positions), using average number of amino acid differences per site as a measure of sequence divergence. All positions containing gaps were eliminated. Standard error estimates were obtained by a bootstrap procedure (500 replicates). These analyses were conducted in MEGA6 (Tamura et al., 2013).

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M genomes and the closest published M genomes were calculated (Table 1). They confirm the close relationship of the Baltic M. trossulus M genomes with the European M. edulis M genomes and the distinctiveness of European and American M. edulis M genomes. This distinction is much more pronounced at nucleotide level (47%), much less so at protein level, where all inter and intra-group comparisons yielded the values in the range of 2–4%. Taking into account that diversity in synonymous and nonsynonymous substitutions calculated for various genome comparisons consequently show elevated KA/KS ratios in all M groups (mean M KA/KS ¼ 0.092, mean F KA/KS ¼ 0.053), this suggests that stochastic processes dominate the evolution of protein-coding genes within this M lineage.

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Declaration of interest This study was partially funded by project EC ICA1-CT-2002-70022, SPB 127/E-335/SPB/5.PR UE/DIE 63/2005, Polish Ministry of Science and Higher Education to R.W., through a Grant No. NN303 418336 to A.B. and by the statutory topic IV.1 in the IO PAS. The authors are solely responsible for writing this manuscript.

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Mitochondrial DNA, Early Online: 1–2

Kijewski T, S´mietanka B, Zbawicka M, Gosling E, Hummel H, Wenne R. (2011). Distribution of Mytilus taxa in European coastal areas as inferred from molecular markers. J Sea Res 65:224–34. Riginos C, Hickerson MJ, Henzler CM, Cunningham CW. (2004). Differential patterns of male and female mtDNA exchange across the Atlantic Ocean in the blue mussel, Mytilus edulis. Evolution 58: 2438–51. Skibinski DO, Gallagher C, Beynon CM. (1994). Mitochondrial DNA inheritance. Nature 368:817–18. S´mietanka B, Burzyn´ski A, Wenne R. (2009). Molecular population genetics of male and female mitochondrial genomes in European mussels Mytilus. Marine Biol 156:913–25. S´mietanka B, Burzyn´ski A, Wenne R. (2010). Comparative genomics of marine mussels (Mytilus spp.) gender associated mtDNA: Rapidly evolving atp8. J Mol Evol 71:385–400. Tamura K, Nei M, Kumar S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–5. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–9. Zbawicka M, Burzyn´ski A, Wenne R. (2007). Complete sequences of mitochondrial genomes from the Baltic mussel Mytilus trossulus. Gene 406:191–8. Zbawicka M, Wenne R, Burzyn´ski A. (2014). Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels. Mol Genet Genomics. [Epub ahead of print]. DOI 10.1007/s00438014-0888-3. Zouros E, Ball AO, Saavedra C, Freeman KR. (1994). Mitochondrial DNA inheritance. Nature 368:818.

Complete male mitochondrial genomes of European Mytilus edulis mussels.

Doubly uniparental inheritance (DUI) results in the existence of two gender-specific, divergent mtDNA lineages within a single species. Under DUI, the...
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