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Mitochondrial Genome Rearrangements at Low Taxonomic Levels: Three Distinct Mitogenome Gene Orders in the Genus Pseudoniphargus (Crustacea: Amphipoda)

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Mitochondrial Genome Rearrangements at Low Taxonomic Levels: Three Distinct Mitogenome Gene Orders in the Genus Pseudoniphargus (Crustacea: Amphipoda) Mitochondrial DNA The Journal of DNA Mapping, Sequencing, and Analysis ISSN: 1940-1736 (Print) 1940-1744 (Online) Journal homepage: http://www.tandfonline.com/loi/imdn20 Mitochondrial genome rearrangements at low taxonomic levels: three distinct mitogenome gene orders in the genus Pseudoniphargus (Crustacea: Amphipoda) Morten Stokkan, Jose A. Jurado-Rivera, Carlos Juan, Damià Jaume & Joan Pons To cite this article: Morten Stokkan, Jose A. Jurado-Rivera, Carlos Juan, Damià Jaume & Joan Pons (2015): Mitochondrial genome rearrangements at low taxonomic levels: three distinct mitogenome gene orders in the genus Pseudoniphargus (Crustacea: Amphipoda), Mitochondrial DNA, DOI: 10.3109/19401736.2015.1079821 To link to this article: http://dx.doi.org/10.3109/19401736.2015.1079821 Published online: 02 Sep 2015. Submit your article to this journal Article views: 58 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=imdn20 Download by: [Inst Medit Estudios Avanzados] Date: 02 March 2016, At: 01:56 http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–11 ! 2015 Taylor & Francis. DOI: 10.3109/19401736.2015.1079821 RESEARCH ARTICLE Mitochondrial genome rearrangements at low taxonomic levels: three distinct mitogenome gene orders in the genus Pseudoniphargus (Crustacea: Amphipoda) Morten Stokkan1, Jose A. Jurado-Rivera1,2, Carlos Juan1,2, Damia` Jaume1, and Joan Pons1 1Department of Biodiversity and Conservation, Instituto Mediterraneo de Estudios Avanzados (IMEDEA, CSIC-UIB), Esporles, Spain and 2Departament de Biologia, Universitat de les Illes Balears, Palma, Spain Abstract Keywords A comparison of mitochondrial genomes of three species of the amphipod Pseudoniphargus Pseudoniphargidae, non-coding region, RNA revealed the occurrence of a surprisingly high level of gene rearrangement involving protein- structure, transposition and reversal events coding genes that is a rare phenomenon at low taxonomic levels. The three Pseudoniphargus mitogenomes also display a unique gene arrangement with respect to either the presumed History Pancrustacean order or those known for other amphipods. Relative long non-coding sequences appear adjacent to the putative breakage points involved in gene rearrangements of protein Received 24 April 2015 coding genes. Other details of the newly obtained mitochondrial genomes – e.g., gene content, Revised 26 July 2015 nucleotide composition and codon usage – are similar to those found in the mitogenomes of Accepted 29 July 2015 other amphipod species studied. They all contain the typical mitochondrial genome set Published online 1 September 2015 consisting of 13 protein-coding genes, 22 tRNAs, and two rRNAS, as well as a large control region. The secondary structures and characteristics of tRNA and ribosomal mitochondrial genes of these three species are also discussed. Introduction to have operated in reverse transpositions. TDRLs are more complex processes where a segment including more than one A typical metazoan mitochondrial genome (mitogenome) con- gene undergoes duplication and subsequently, suffers the deletion tains 13 protein-coding genes (PCGs), two ribosomal RNA genes of particular gene copies at random, producing novel gene (rRNA), 22 transfer RNA genes (tRNA), and a non-coding arrangements that can differ considerably from the ancestral gene control region (CR) also called the D-loop that includes the order. The latter is an interesting mechanism from a phylogenetic origin of replication (Boore, 1999). However, gene order differs point of view, since it is the only shift that can be considered remarkably across higher taxonomic ranks (family and above) with confidence to be irreversible (Chaudhuri et al., 2006). The due to the occurrence of gene rearrangements such as transpos- rearrangement events that took place in a particular mitogenome itions and reversals (Arndt & Smith, 1998; Bauza-Ribot et al., with respect to an ancestral gene order can be heuristically 2009; Bensch & Harlid, 2000; Dowton & Austin, 1999; determined using strong interval trees (Berard et al., 2007; Bernt Hickerson & Cunningham, 2000; Irisarri et al., 2014). et al., 2007; Perseke et al., 2008). The ultimate causes of Downloaded by [Inst Medit Estudios Avanzados] at 01:56 02 March 2016 Rearrangements of this kind, especially those affecting tRNA rearrangement events in the mitochondrial genome remain genes, are frequently detected when comparing animal mitogen- unclear, although nuclear substitution rate has been shown to omes belonging to different taxonomic families or even between correlate with rearrangement frequency (Shao et al., 2003). genera within the same family (Arndt & Smith, 1998; Dowton Furthermore, the origin of replication – that is located in the et al., 2009; Kurabayashi et al., 2008, 2010). But rearrangements control region – also has been postulated to be a hot-spot for within the same genus, especially those involving PCGs, are gene rearrangements (Arunkumar & Nagaraju, 2006; Kraytsberg rather rare (Matsumoto et al., 2009; Rawlings et al., 2001). et al., 2004; Macey et al., 1997; San Mauro et al., 2006). Mitochondrial gene rearrangements can occur as a product of Besides, life history and ecology traits such as founder effect and one of these four major events: reversals, transpositions, reverse parasitism have been postulated to play a role in the gene transpositions, or tandem duplications with subsequent random rearrangement rate in some animal lineages (Tsaousis et al., loss (TDRL) (Chaudhuri et al., 2006; Moritz & Brown, 1987; 2005). Despite gene content of mitogenomes is mostly conserved San Mauro et al., 2006). Reversals consist of one or several across metazoans, nucleotide and aminoacid composition, as genes that switch from one DNA strand to the other, while well as codon usage, vary largely across major taxonomic transpositions involve a shift to another location without groups. Thus, insects and other arthropods display very AT-rich changing the sense of the strand. Both processes are deduced mitogenomes with PCGs showing heavily biased codon usages (Sheffield et al., 2008; Yang, 2008), while vertebrates show lower AT-richness (Sano et al., 2005). Correspondence: Joan Pons, Department of Biodiversity and Conservation, Instituto Mediterraneo de Estudios Avanzados The amphipod crustacean family Pseudoniphargidae (IMEDEA), Miquel Marque`s 21, 07190 Esporles, Spain. Tel: +34 (Karaman, 1993) contains only two genera, Pseudoniphargus 971611332. E-mail: [email protected] (Chevreux, 1901) and Parapseudoniphargus (Notenboom, 1988), 2 M. Stokkan et al. Mitochondrial DNA, Early Online: 1–11 whereupon the latter is represented by only one species. Secondary structures of tRNAs were corroborated using Arwen Pseudoniphargus has 68 species currently described, all being (Laslett & Canba¨ck, 2008) and tRNAscan-SE (Schattner et al., obligate stygobionts (occurring exclusively in groundwaters), and 2005) search servers in parallel. Finally, annotations were checked displays a broad disjunct geographic distribution despite its with MITOS web server (Bernt et al., 2013), particularly to members presumably having a poor dispersal ability (Notenboom, estimate the secondary structures of rRNA sequences. These were 1991). Endemic island Pseudoniphargus species are found in manually refined with Mfold web server (Zuker, 2003) and Bermuda as well as in the Atlantic archipelagoes of the Canaries, graphically visualized using VARNA v3.9 (Darty et al., 2009). Madeira, and Azores. Species of the genus are also found on the Palindromes in non-coding spacer regions and the control region southern margin of the Mediterranean (e.g., Algeria, Morocco, were identified using the Mfold. Nucleotide and aminoacid and southern Spain including the Balearic Islands) as well as in composition, as well as relative synonymous codon usage northern Spain and the south coast of France (Messouli et al., (RSCU), were calculated using MEGA v5.05 (Tamura et al., 2001; Notenboom, 1986, 1987a, b; Stock, 1980, 1988; Stock & 2011). The effective number of codons (ENC) (Wright, 1990) was Abreu, 1992; Stock et al., 1986). The mitogenome of P. daviui estimated with INCA V2.1 (Supek & Vlahovicˇek, 2004). AT and (Jaume, 1991), of around 15 kb, was sequenced and used as an GT skews were estimated as described in Pons et al. (2014), and outgroup in a broad scope biogeographic study (Bauza`-Ribot ggskew options within the EMBOSS v6.6.0 package (Rice et al., et al., 2012) although its gene order, composition, and secondary 2000). structures were not addressed. Here we analyze in greater detail the characteristics of this mitogenome along with newly obtained Mitochondrial genome rearrangements mitochondrial genomes of two additional congeneric species, namely P. gorbeanus (Notenboom, 1986) and P. sorbasiensis Gene rearrangements with respect to the putative ancestral (Notenboom, 1987b), which display a different gene order, Pancrustacean and other known amphipod gene orders were particularly focusing on gene rearrangements and secondary investigated using CREx (Bernt et al., 2007). This software structures. calculates and creates ‘‘strong interval trees’’, to heuristically disentangle the possible processes involved (Berard et al., 2007; Methods Bernt et al., 2007; Perseke et al., 2008). A ‘‘common interval’’ is a subset of genes that appears successively in two or more input
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