Phylomitogenomics of Malacostraca (Arthropoda: Crustacea)
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Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 DOI: 10.1007/s13131-015-0583-1 http://www.hyxb.org.cn E-mail: [email protected] Phylomitogenomics of Malacostraca (Arthropoda: Crustacea) SHEN Xin1, 2, 3*, TIAN Mei1, YAN Binlun1, CHU Kahou3 1 Jiangsu Key Laboratory of Marine Biotechnology/College of Marine Science, Huaihai Institute of Technology, Lianyungang 222005, China 2 Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China 3 Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China Received 25 February 2014; accepted 29 August 2014 ©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2015 Abstract Along with the sequencing technology development and continual enthusiasm of researchers on the mitochondrial genomes, the number of metazoan mitochondrial genomes reported has a tremendous growth in the past decades. Phylomitogenomics—reconstruction of phylogenetic relationships based on mitochondrial genomic data—is now possible across large animal groups. Crustaceans in the class Malacostraca display a high diversity of body forms and include large number of ecologically and commercially important species. In this study, comprehensive and systematic analyses of the phylogenetic relationships within Malacostraca were conducted based on 86 mitochondrial genomes available from GenBank. Among 86 malacostracan mitochondrial genomes, 54 species have identical major gene arrangement (excluding tRNAs) to pancrustacean ground pattern, including six species from Stomatopoda, three species from Amphipoda, two krill, seven species from Dendrobranchiata (Decapoda), and 36 species from Pleocyemata (Decapoda). However, the other 32 mitochondrial genomes reported exhibit major gene rearrangements. Phylogenies based on Bayesian analyses of nucleotide sequences of the protein-coding genes produced a robust tree with 100% posterior probability at almost all nodes. The results indicate that Amphipoda and Isopoda cluster together (Edriophthalma) (BPP=100). Phylomitogenomic analyses strong support that Euphausiacea is nested within Decapoda, and closely related to Dendrobranchiata, which is also consistent with the evidence from developmental biology. Yet the taxonomic sampling of mitochondrial genome from Malacostraca is very biased to the order Decapoda, with no complete mitochondrial genomes reported from 11 of the 16 orders. Future researches on sequencing the mitochondrial genomes from a wide variety of malacostracans are necessary to further elucidate the phylogeny of this important group of animals. With the increase in mitochondrial genomes available, phylomitogenomics will emerge as an important component in the Tree of Life researches. Key words: Malacostraca, Crustacea, Phylomitogenomics, gene arrangement, mitochondrial genome Citation: Shen Xin, Tian Mei, Yan Binlun, Chu Kahou. 2015. Phylomitogenomics of Malacostraca (Arthropoda: Crustacea). Acta Oceanologica Sinica, 34(2): 84–92, doi: 10.1007/s13131-015-0583-1 1 Introduction close related species so that there is a lack of large-scale and Complete mitochondrial genomes of human (Homo sapiens) comparison in many major animal groups. As the genome data- and mouse (Mus musculus) were sequenced in 1981 (Anderson et bases now contain thousands of animal mitochondrial genomes, al., 1981; Bibb et al., 1981), which are the first ones available in it allows comprehensive analysis and evaluation of existing data Metazoa. The number of metazoan mitochondrial genomes re- in a major group based on a large number of taxa. To assess and ported reaches 127 by the end of the year 2000. However, from analyze the existing mitochondrial genomic information, which 2001 to the present, along with the sequencing technology devel- not only help to reconstruct animal phylogeny based on mito- opment and the continued enthusiasm of researchers on mito- chondrial genomes, but also help to pinpoint the gaps in the cur- chondrial genomes, the number of metazoan mitochondrial gen- rent mitochondrial genomic data, and thus provide guidance for omes reported increases tremendously. The metazoan mito- future researches. As a case study, this study examines the situ- chondrial genomes available from GenBank have reached 3 653 ation in malacostracans from the viewpoint of phylomitogenom- by the end of 2013 (Fig. 1). Phylomitogenomics, the use of mito- ics. chondrial genomic data in resolving phylogenetic relationships, The class Malacostraca is the largest of the six classes of crus- has emerged to be an important approach in phylogenetic recon- taceans, containing about 25 000 extant species, and is divided struction. into 16 orders. Malacostracans display a high diversity of body When mitochondrial genomes of one or several new species forms, and include shrimp, crabs, krill, lobsters, woodlice, mantis were obtained, the researchers often compare them with those of shrimp and many other species (Martin and Davis, 2001). Foundation item: The National Natural Science Foundation of China under contract Nos 41476146 and 40906067; Hong Kong Scholars Program under contract No. XJ2012056; China Postdoctoral Science Foundation under contract Nos 2012M510054 and 2012T50218; a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). *Corresponding author, E-mail: [email protected] SHEN Xin et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 2, P. 84–92 85 Malacostracans not only contain a wide variety of taxa, but also long time a hotly debated issue (Richter and Scholtz, 2001; von include many species with high ecological and economic values. Reumont et al., 2012). In this paper, comprehensive analyses of In the past hundreds of years, there have been many studies fo- the phylogenetic relationships within Malacostraca were con- cused on its systematic and evolutionary relationships. Literat- ducted based on 86 mitochondrial genomes available. In addi- ures exploring the malacostracan relationships based on mor- tion, the knowledge gaps of the current mitochondrial genomic phological and molecular data are numerous. Evolutionary rela- data are also noted to guide future researches. tionships among the various groups of Malacostraca was for a Fig. 1. Growth curve of metazoan mitochondrial genomes released in GenBank. 2 Materials and methods (atp6, atp8, cob, cox1-3, nad1-4, nad4L, nad5 and nad6) were separately aligned using Clustal X 1.83 (Thompson et al., 1997) 2.1 Data acquisition (default parameters) and then concatenated as a single dataset of A total of 3 653 metazoan mitochondrial genomes were 11 584 base pairs (bp) for analysis. Model selection for the nucle- downloaded (ftp://ftp.ncbi.nlm.nih.gov/genomes/). Then 86 otide acid dataset was done with jModelTest (Darriba et al., 2012) malacostracan mitochondrial genomes were obtained by self- and the best model was GTR matrix and the Gamma+Invar mod- written PERL script. The taxa are shown in Table 1, including rep- el. Phylogenetic analysis was performed using MrBayes 3.1 (Ron- resentatives from five orders, with 60 species from Decapoda quist and Huelsenbeck, 2003). Four Markov chains of 1 000 000 (Wilson et al., 2000; Yamauchi et al., 2002; Yamauchi et al., 2003; generations were run with sampling every 1 000 generations. The Miller et al., 2004; Yamauchi et al., 2004; Miller et al., 2005; Place first quarter (250 000 generations) was excluded from the analys- et al., 2005; Segawa and Aotsuka, 2005; Sun et al., 2005; Ivey and is as “burn-in”. After omitting the first 250 “burn in” trees, the re- Santos, 2007; Shen et al., 2007; Yang et al., 2008; Ki et al., 2009; maining 750 sampled trees were used to estimate the consensus Peregrino-Uriarte et al., 2009; Shen et al., 2009; Liu and Cui, tree and the Bayesian posterior probability (BPP). 2010a; Yang et al., 2010; Ma et al., 2011; Qian et al., 2011; Gene rearrangement information was indicated in the phylo- Jondeung et al., 2012; Kim et al., 2012a; Kim et al., 2011; Kim et genetic tree constructed using the protein-coding gene se- al., 2012b; Lin et al., 2012; Liu and Cui, 2011; Shi et al., 2012; Yang quences. Thus information from mitochondrial genomes as a et al., 2012; Kim et al., 2013a; Kim et al., 2013b; Ma et al., 2013; whole (including sequence information and gene arrangement) Shen et al., 2013; Yang et al., 2013; Wang et al., 2014), two from were used for exploring the phylogenetic relationships of the tar- Euphausiacea (Shen et al., 2010; Shen et al., 2011), six from Sto- get groups, which is basic requirement of phylomitogenomic matopoda (Cook, 2005; Miller and Austin, 2006; Liu and Cui, analyses. 2010b), sixteen from Amphipoda (Bauza-Ribot et al., 2009; Ito et al., 2010; Ki et al., 2010; Kilpert and Podsiadlowski, 2010b; Bauza- 3 Results and discussion Ribot et al., 2012; Krebes and Bastrop, 2012; Shin et al., 2012), and two from Isopoda (Kilpert and Podsiadlowski, 2006; Kilpert and 3.1 Characteristics of malacostracan mitochondrial genomes Podsiadlowski, 2010a). The length of decapod mitochondrial genomes ranges from 14 316 bp (H. gammarus) to 18 197 bp (G. dehaani) (Table 1). The 2.2 Comparison of major gene arrangements two krill mitochondrial genomes are 15 498 bp and 16 898 bp in Due to the high frequency of translocations and inversions of length for E. superba (incomplete) and E. pacifica, respectively. the transfer RNA (tRNA) genes in animal mitochondrial gen- The length of mantis shrimp mitochondrial genomes ranges from omes, major coding gene (protein-coding genes and ribosomal 15 714 bp (H. harpax) to 16 325 bp (L. maculata). In Amphipoda, RNA genes) arrangement may provide more reliable information the length of mitochondrial genomes varies between 14 113 bp than tRNA genes when we focus on the comparison of higher (M. longipes) and 18 424 bp (G. antarctica). The length of two iso- level taxa. In this paper, the major gene arrangement of the 86 pod mitochondrial genomes is 15 289 bp (L. oceanica) and 14 994 malacostracan mitochondrial genomes were analyzed and com- bp (E. sp.14 FK-2009), respectively. pared systematically. In Decapoda, the A + T contents of the mitochondrial heavy chain are between 60.2% (A. distinguendus) and 74.9% (G.