Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets

BMC Research Notes BioMed Central Short Report Open Access Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets Xiangyun Wu, Xiaodong Xu, Ziniu Yu* and Xiaoyu Kong Address: Key Laboratory of Marine Bio-resource Sustainable Utilization, Laboratory of Applied Marine Biology; South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou 510301, PR China Email: Xiangyun Wu - ; Xiaodong Xu - ; Ziniu Yu* - ; Xiaoyu Kong - * Corresponding author Published: 5 May 2009 BMC Research Notes 2009, 2:69 doi:10.1186/1756-0500-2-69 Received: 26 January 2009 Accepted: 5 May 2009 This article is available from: http://www.biomedcentral.com/1756-0500/2/69 © 2009 Yu et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: It can be seen from the available mollusk mitogenomes that the family Pectinidae exhibits the most variation in genome organization. In this study, comparative mitogenomic analyses were performed for three scallops from the subfamily Chlamydinae (Pectinidae), with the goal of characterizing the degree of variability of mitogenome organization and other characteristics among species from the same subfamily and exploring their possible evolution route. Findings: The complete or nearly complete mtDNA sequences of scallop Mimachlamys nobilis (17 935 bp), Mizuhopecten yessoensis (20 964 bp) and Chlamys farreri (17 035 bp) were determined using long PCR amplification and primer walking sequencing strategy. Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets. Only 21, 16, and 17 tRNA genes were detected in the mitogenomes of M. nobilis, M. yessoensis and C. farreri, respectively. Remarkably, no trnS gene could be identified in any of the three scallops. A newly-detected trnA-like sequence within the mitogenome of M. yessoensis seems to exemplify the functional loss of a tRNA gene, and the duplication of trnD in M. yessoensis raises a fundamental question of whether the retention of the tRNA gene copy of 2-tRNAs is easier than that of 4tRNAs. Analysis of putative evolutionary pathways of gene rearrangement indicates that transposition of neighboring gene blocks may play an important role in the evolution of mitogenomes in scallops. Parsimonious analysis of the genomic variations implies that the mitogenomes of M. yessoensis and C. farreri are likely to derive independently from a common ancestor that was closely related to M. nobilis. Conclusion: Comparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes. These features provide useful clues and information for evolutionary analysis of scallop mitogenomes. Page 1 of 7 (page number not for citation purposes) BMC Research Notes 2009, 2:69 Findings It can be seen from the available mollusk mitogenomes that the Pectinidae exhibits the most variation in genome organization. When we were initiating the current study, three complete or nearly complete mitogenomes, representing three subfamilies, were available from this family, i.e., Argopecten irradians (Aequipectini group, GenBank: EU023915), Mizuhopecten yessoensis (Chlamydinae, GenBank: AB271769) and Placopecten magellanicus (Palliolinae, GenBank: DQ088274). Obvious differences in mitogenome organization of three scallops were observed: 1) the sizes of three mitogenomes are distinct from each other, i.e. 16 221 bp for A. irradians, 20 414 bp for M. yessoensis and 32 115 bp for P. magellanicus [1]; 2) allegedly, the three mitogenomes have significantly different tRNA gene sets, with the numbers of 22, 32 and 9 for A. irradians, P. magellanicus and M. yessoensis, respectively; 3) the genomes show distinct gene arrangement patterns, namely unique rearrangements involving nearly every gene. The degree of gene arrangements of mitogenomes from different species in the same subfamily, Chlamydinae, is one of our concerns. Therefore, in this study the complete mtDNA sequences of Mimachlamys nobilis and M. yessoensis, and nearly complete mtDNA sequence of Chlamys farreri are determined using long PCR amplification and primer walking sequencing strategy (see Additional file 1), and used for comparative analyses. Another reason for inclusion of M. yessoensis is that its first mitogenome data deposited in GenBank (AB271769) seems to bear significant omissions and mis-annotations of tRNA genes and protein-coding gene. Apparently, these mis-annotations http://www.biomedcentral.com/1756-0500/2/69 need to be amended for further studies of gene order variation, evolution and phylogenetic analysis. Genome organization and nucleotide composition The size of the mitogenome is 17 935 bp for M. nobilis (GenBank: FJ595958). Due to technical difficulties in sequencing, a small part (up to a couple of hundreds base pairs) of the mitogenome of C. farreri was not obtained and the nearly complete genome is 17 035 bp in length (GenBank: FJ595957). Genome assembly indicated that the unfinished section is the start part of the major noncoding region (MNR). The complete mtDNA sequence of M. yessoensis obtained in this study is 20 964 bp in length (GenBank: FJ595959), which is 550 bp longer than the nearly complete genome. Genome assembly indicated that the previously unfinished section is part of the MNR. Annotation to the mitogenome obtained in the current study and a re-annotation to AB271769 revealed the following findings: 1) the "absent" cox2 gene in previous annotation is actually present, corresponding to nucleotides 14 638–15 325, with "CTG" as initiation codon and "T" as termination codon; and 2) the genome has a total of 16 tRNA genes, instead of nine identified in that nearly complete genome. Additionally, 56 transitions were detected from a comparison of mitogenomes FJ595959 and AB271769. The three mitogenomes contain 12 protein-coding genes (PCGs), lacking the atp8 gene as in most bivalves, two ribosomal RNA genes and varying numbers of tRNA gene set (see Additional file 2; Additional file 3; Additional file 4; Additional file 5; Figure 1). No obvious difference in gene length was observed among three scallops (Additional file 2); thus, what contributes to the differences in Figure Organization 1 of the mitochondrial genome of Mimachlamys nobilis (A), Mizuhopecten yessoensis (B) and Chlamys farreri (C) Organi (...truncated)