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Molecular Phylogenetics and Evolution 65 (2012) 323–328

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Molecular Phylogenetics and Evolution 65 (2012) 323–328 Molecular Phylogenetics and Evolution 65 (2012) 323–328 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Short Communication Novel organization of the mitochondrial genome in the deep-sea coral, Madrepora oculata (Hexacorallia, Scleractinia, Oculinidae) and its taxonomic implications Mei-Fang Lin a,c,g, Marcelo Visentini Kitahara b, Hiroyuki Tachikawa d, Hironobu Fukami e, ⇑ David John Miller c,g, Chaolun Allen Chen a,f,h, a Biodiversity Research Center, Academia Sinica, Nangang, Taipei 115, Taiwan b Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião 11600-970, Brazil c School of Pharmacy and Molecular Sciences, James Cook University, Townsville 4810, Australia d Natural History Museum and Institute, Chiba 955-2, Japan e Department of Marine Biology and Environmental Science, University of Miyazaki, Miyazaki 889-2192, Japan f Institute of Oceanography, National Taiwan University, Taipei 106, Taiwan g ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville 4810, Australia h Taiwan International Graduate Program (TIGP)-Biodiversity, Academia Sinica, Nangang, Taipei 115, Taiwan article info abstract Article history: Madrepora is one of the most ecologically important genera of reef-building scleractinians in the deep sea, Received 25 January 2012 occurring from tropical to high-latitude regions. Despite this, the taxonomic affinities and relationships Revised 29 May 2012 within the genus Madrepora remain unclear. To clarify these issues, we sequenced the mitochondrial Accepted 4 June 2012 (mt) genome of the most widespread Madrepora species, M. oculata, and compared this with data for Available online 1 July 2012 other scleractinians. The architecture of the M. oculata mt genome was very similar to that of other scle- ractinians, except for a novel gene rearrangement affecting only cox2 and cox3. This pattern of gene orga- Keywords: nization was common to four geographically distinct M. oculata individuals as well as the congeneric Scleractinian species M. minutiseptum, but was not shared by other genera that are closely related on the basis of Madrepora Mitochondrial genome cox1 sequence analysis nor other oculinids, suggesting that it might be unique to Madrepora. Gene rearrangement Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction 2007), and comprises five recent species (Cairns, 2009). M. oculata is the type species and is probably the most-widespread scleractin- Almost half of extant scleractinians are azooxanthellate (i.e. live ian species, being essentially ubiquitous in deep water except in without dinoflagellate symbionts) and are often referred to as cold- the polar seas (Cairns and Zibrowius, 1997). M. oculata is highly or deep-water corals because they generally occur in waters polymorphic, six forms being recognized (alpha, beta, gamma, deeper than 50 m (Cairns et al., 1999; Cairns, 2007). Although less galapagensis, vitiae, and formosa; Cairns, 1991, 1995; Cairns et al., obvious than the shallow water coral reefs of tropical waters, the 1999) based on variations in color, branching patterns, the texture deep sea reefs constructed by some azooxanthellate scleractinians of the coenosteum and the size of septa; however, note that these serve as habitat, feeding, recruitment, and nursery grounds for characters are variable even within sympatric specimens (e.g., numerous marine organisms (Roberts et al., 2009) and have Galápagos specimens; Cairns, 1991). recently attracted the attention of both the scientific community Although traditionally classified in the Family Oculinidae and the general public, particularly the fishing industry. However, (Cairns et al., 1999; Cairns, 2009), recent molecular phylogenetic relatively few deep-water scleractinians – representatives of the analyses suggest that the family is polyphyletic (representatives genera Lophelia, Solenosmilia, Goniocorella, Madrepora, Oculina, were scattered across four different clades, these most likely repre- and Enallopsammia – are considered to fulfill the ecological and senting four different families; Kitahara et al., 2010), and that the geological criteria of true reef-building species (Stolarski and genus Madrepora should be elevated to a higher taxonomic level Vertino, 2007; Roberts et al., 2009). (Le Goff-Vitry et al., 2004; Kitahara et al., 2010). Molecular phylog- Of the deep-sea reef-builders, Madrepora has a fossil record dat- enetics based on partial cox1 data suggests that Madrepora oculata ing from the Lower Cretaceous (ca. 70 Mya; Stolarski and Vertino, may be more closely related to Caryophyllia (family Caryophyllii- dae) and pocilloporids than to other oculinids (Kitahara et al., 2010; Stolarski et al., 2011). ⇑ Corresponding author at: Biodiversity Research Center, Academia Sinica, Nangang, Taipei 115, Taiwan. Fax: +886 2 28958059. Comparison of mitochondrial (mt) genomes has contributed to E-mail address: [email protected] (C.A. Chen). the clarification of phylogenetic relationships among animals (Boore, 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.06.011 324 M.-F. Lin et al. / Molecular Phylogenetics and Evolution 65 (2012) 323–328 1999; van Oppen et al., 2002; Chen et al., 2008a,b), gene arrangement reported, each with important phylogenetic implications. These vari- has been generally the most informative mt character (reviewed in ations include the presence of an idiosyncratic atp8 in Seriatopora and Boore et al., 2005). Several well-established evolutionary lineages a duplicated trnW in some pocilloporids (Chen et al., 2008b), the are defined by common organization of mt genes (reviewed in Boore insertion of a distinct group I intron in the cox1 gene of some ‘‘robust’’ and Brown, 1998) and unique arrangements distinguish subgroups corals (Fukami et al., 2007) and the extended 30-end found of the cox1 within nematodes, mollusks (reviewed in Boore and Brown (1998)) gene of Euphyllia (Lin et al., 2011). and cnidarians (Hexacorallia; Beagley et al., 1998; Medina et al., To clarify the phylogenetic status of Madrepora, the complete 2006; Brugler and France, 2007). In terms of mt gene order, many mt genome of M. oculata was sequenced, revealing a novel gene scleractinians conform to a consensus first reported in rearrangement that constitutes only the second known deviation Acropora tenuis (van Oppen et al., 2002;seeFig. 2A upper). Within from the scleractinian consensus. This pattern of mt genome the Scleractinia, only one example of apparent gene reorganization organization appears to be common across Madrepora, but is is known – the case of Lophelia pertusa (Emblem et al., 2011; see not shared by genera that are closely related on the basis of Fig. 2A lower) – but a number of minor variations have also been cox1 data (i.e. pocilloporids and some caryophyllids) or other Fig. 1. Madrepora oculata branch fragment and calicular views of the specimen used for determination of the complete sequence of the mitochondrial genome, and the sampling locations examined in this study. Collection sites are indicated by solid black squares. M.-F. Lin et al. / Molecular Phylogenetics and Evolution 65 (2012) 323–328 325 members of Oculinidae, the Family in which Madrepora is classi- 94 °C, 45 s at 52 °C, and 1.5 min at 68 °C, followed by a final exten- cally placed. Madrepora apparently represents a distinct lineage, sion step at 68 °C for 3 min. PCR products from the gene rearrange- but whether it merits family status is as yet unclear. ment survey and cox1 region from each sample were directly sequenced using the same method described above. 2. Materials and methods 2.3. Mitochondrial genome annotation 2.1. Coral sample collections Nucleotide sequences were verified and assembled using The M. oculata colony fragment used for complete mt genome SeqManII (DNAstar vers. 5.0) and then analyzed in Vector NTI vers. sequencing (Fig. 1 upper, the colony fragment and the corallite) 9.0 (InforMax, Invitrogen Life Science). Open reading frames (ORFs) was collected from a deep-sea expedition in the South China Sea of considerable length (>50 amino acids) were initially translated (21°3502400N, 117°1702400E, at 353 m in depth) by an otter trawl of using a cnidarian mt genetic code (NCBI translation Table 4) and the research vessel Fisheries Researcher I, of the Taiwan Fishery Re- compared to sequences in the GenBank database using BLAST X search Institute (TFRI), Council of Agriculture. Pacific M. oculata (Gish and States, 1993). Alignment of identical putative ORFs and specimens were collected in New Caledonian waters (23°010S, rRNA genes was performed using MEGA vers. 4.0 (Tamura et al., 168°170E, at 550 m in depth) during the Norfolk 2 expedition 2007) with a weighted matrix of Clustal W (Thompson et al., (sta. DW 2142), and off Katsuura, Chiba, Japan. The Indian Ocean 1994). Transfer (t)RNAs structures were predicted by tRNAscan- specimen was collected near Western Australia (between SE search server vers. 1.21 (Lowe and Eddy, 1997). The 31°5705400S, 115°0601800E at 928 m and 31°5605900S, 115°0700500E, arrangement of the protein-coding gene, tRNAs, rRNA, and at 1170 m in depth) (Fig. 1). A colony fragment of M. minutiseptum intergenic spacers was illustrated using Vector NTI vers. 9.0 examined herein was also collected in Japanese waters, near le- (InforMax, Invitrogen Life Science). channel. All samples were preserved in CHAOS solution as de- scribed in Fukami
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