Abstract
The extant marine mussels which belong to the Mytiloidea are widespread species inhabiting mostly coastal waters, with some distributed in the deep sea. To clarify the classification systems and phylogenetic relationships range from genus to family level within Mytiloidea, new sequence was used in a phylogenetic analysis including all the available Mytiloidea mitochondrial genomes. In this study, the complete mitochondrial genome of Vignadula atrata is 15,624 bp in length and contains 12 protein-coding genes (PCGs, atp8 is absent), two ribosomal RNA genes, and 22 transfer RNA genes. Phylogenetic analysis based on 12 PCGs showed that it has a close relationship to Bathymodiolus. The analysis of gene rearrangements in the Pteriomorphia showed that the arrangements are highly variable across species, novel gene rearrangements were found within Mytiloidea. The V. atrata mitogenome was provided in detail, with notes on the sequence and a key to the species of Vignadula. This study provides a perspective on the taxonomic histories of the marine mussels and refines the unclear relationship between the origin and evolution of species in Mytiloidea within Bivalvia.
Similar content being viewed by others
Data Avalibility
The data supporting the findings of this study are freely available in GenBank (accession number: ON153190).
References
Ahmed MS, Barua A, Datta SK, Saha T, Antu DR, Ahmed S (2022) Characterization of spiny lobsters from Bangladesh waters using morphology, COI and 16S rRNA sequences. Heliyon 8(2):e08846
Alexandre H, Nelly L, Jean D (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst Biol 54(2):277–298
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Narnia 25(22):4692–4693
Altschul SF, Madden TL, Schffer AA, Jinghui Z, Zheng Z, Webb M, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389
Amler MRW (1999) Synoptical classification of fossil and recent bivalvia. Geol Palaeontol 33:237–248
Beagley CT, Okimoto R, Wolstenholme DR (1998) The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics 148(3):1091–1108
Bergstrom P, Hallmark N, Larsson KJ, Lindegarth M (2019) Biodeposits from Mytilus edulis: a potentially high-quality food source for the polychaete. Hediste Diversicolor Aquacult Int 27(1):89–104
Bernard FR, Cai YY, Morton B (1993). A Catalogue of the living marine bivalve molluscs of China. HKU.
Bernt M, Donath A, Juhling F (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69(2):313–319
Beu AG (2006) Marine mollusca of oxygen isotope stages of the last 2 million years in New Zealand part 2 biostratigraphically useful and new Pliocene to recent bivalves. J Roy Soc New Zeal 36(4):151–338
Beu AG, Marshall BA, Reay MB (2014) Mid-Cretaceous (Albian–Cenomanian) freshwater mollusca from the clarence valley, marlborough, New Zealand, and their biogeographical significance. Cretaceous Res 49:134–151
Bieler R, Carter JG, Coan E (2010) Classification of Bivalve Families. In: Bouchet, P., Rocroi, J.-P. (Eds.), Nomenclator of Bivalve Families. Malacologia. 52(2):113–133.
Bieler R, Mikkelsen PM (2006) Bivalvia – a look at the Branches. Zool J Linn Soc-Lond 148(3):223–235
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Bonen L (1998) Mitochondrial genomes: a paradigm of organizational diversity. Advances in Genome Biology 5:415–461
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27(8):1767–1780
Boore JL (2000) The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. Springer 1:133–147
Breton S, Stewart DT, Hoeh WR (2010) Characterization of a mitochondrial ORF from the gender-associated mtDNAs of Mytilus spp (Bivalvia: Mytilidae): identification of the “missing” ATPase 8 gene. Mar Genom 3(1):11–18
Carter JG, Campbell DC, Campbell MR (2000) Cladistic perspectives on early bivalve evolution. J Geol Soc London. https://doi.org/10.1144/GSL.SP.2000.177.01.04
Carter JG, Altaba CR, Anderson LC, Araujo R, Yancey T (2011) A synoptical classification of the bivalvia (Mollusca). Paleontological Contributions 4:1–47
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552
Colgan DJ, Costa PD (2013) Invasive and non-invasive lineages in Xenostrobus (Bivalvia: Mytilidae). Molluscan Res 33(4):272–280
Devloo-Delva F, Miralles L, Ardura A, Borrell YLJ, Pejovic I, Tsartsianidou V, Garcia-Vazquez E (2016) Detection and characterisation of the biopollutant Xenostrobus securis (Lamarck 1819) asturian population from DNA Barcoding and eBarcoding. Mar Pollut Bull 105(1):23–29
Distel DL (2000) Phylogenetic Relationships among Mytilidae (Bivalvia): 18S rRNA data suggest convergence in mytilid body plans. Mol Phylogenet Evol 15(1):25–33
Dowton M, Castro LR, Austin AD (2002) Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: the examination of genome ‘morphology.’ Invertebr Syst 16(3):345–356
Dreyer H, Steiner G (2004) The complete sequence and gene organization of the mitochondrial genome of the gadilid scaphopod Siphonodentalium lobatum (Mollusca). Mol Phylogenet Evol 31(2):605–617
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 17. Mol Biol Evol 22(8):1185–1192
Faure B, Schaeffer SW, Fisher CR (2015) Species distribution and population connectivity of deep-sea mussels at hydrocarbon seeps in the Gulf of Mexico. PLoS ONE 10(4):e0118460
Génio L, Kiel S, Cunha MR, Grahame J, Little CTS (2012) Shell microstructures of mussels (Bivalvia: Mytilidae: Bathymodiolinae) from deep-sea chemosynthetic sites: do they have a phylogenetic significance? Deep-Sea Res Pt I 64:86–103
Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of metazoa as exemplified by comparison of congeneric species. Heredity 101(4):301–320
Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res. 36(suppl_2): 81–4
Holland BS, Gallagher DS, Hicks DW, Davis SK (1999) Cytotaxonomic verification of a non-indigenous marine mussel in the gulf of Mexico. Veliger 42(3):280–283
Janke A, Gemmell NJ, Feldmaier-Fuchs G, Ha Eseler A, Pbo S (1996) The mitochondrial genome of a monotreme—the platypus (Ornithrohynchus anatinus). J Mol Evol 42:153–159
Kalyaanamoorthy S, Minh BQ, Wong T, Haeseler AV, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589
Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 30(14):3059–3066
Kong L, Li Y, Kocot KM, Yang Y, Qi L, Li Q, Halanych KM (2020) Mitogenomics reveals phylogenetic relationships of arcoida (mollusca, bivalvia) and multiple independent expansions and contractions in mitochondrial genome size. Mol Phylogenet Evol 150:106857
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549
Kuroda T, Habe T, Oyama K (1971) The sea shells of Sagami Bay. Collected by His Majesty the Emperor of Japan.
Lam-Tung N, Schmidt HA, Arndt VH, Quang MB (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Phylogenet Evol 32(1):268–274
Laslett D, Canbck AB (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. BMC Bioinformatics 24:5–172
Lee Y, Kwak H, Shin J, Kim S, Kim T, Park J (2019) A mitochondrial genome phylogeny of mytilidae (Bivalvia: Mytilida). Mol Phylogenet Evol 139:106533
Lin Z, Fan X, Huang J, Chen R, Tan Q (2020) Intertidal mussels do not stop metal bioaccumulation even when out of water: cadmium toxicokinetics in Xenostrobus atratus under influences of simulated tidal exposure. Environ Pollut 261:114192
Little C, Vrijenhoek RC (2003) Are hydrothermal vent animals living fossils? Trends Ecol Evol 18(11):582–588
Liu J, Liu H, Zhang H (2018) Phylogeny and evolutionary radiation of the marine mussels (Bivalvia: Mytilidae) based on mitochondrial and nuclear genes. Mol Phylogenet Evol 126:233–240
Lorion J, Kiel S, Faure B, Kawato M, Fujiwara Y (2014) Adaptive radiation of chemosymbiotic deep-sea mussels. Proceedings of the Royal Society B Biological Sciences. 280(1770):20131243.
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):955–964
Matsumoto M (2003) Phylogenetic analysis of the subclass pteriomorphia (Bivalvia) from mtDNA COI sequences. Mol Phylogenet Evol 27(3):429–440
Miao J, Feng J, Liu X, Yan C, Ye Y, Li J, Xu K, Guo B, Lü Z (2022) Sequence comparison of the mitochondrial genomes of five brackish water species of the family neritidae: phylogenetic implications and divergence time estimation. Ecol Evol 12(6):e8984
Miyazaki J, de Oliveira ML, Fujita Y, Matsumoto H, Fujiwara Y (2010) Evolutionary process of deep-sea bathymodiolus mussels. PLoS ONE 5(4):e10363
Morton B (2015) Evolution and adaptive radiation in the mytiloidea (bivalvia): clues from the pericardial–posterior byssal retractor musculature complex. Molluscan Res 35(4):227–245
Morton B, Dinesen GE (2010) Colonization of Asian freshwaters by the Mytilidae (Bivalvia): a comparison of Sinomytilus harmandi from the Tonle-Sap river, phnom penh, cambodia, with Limnoperna fortunei. Molluscan Res 30(2):57–72
Nicolas D, Patrick M, Guillaume S (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 4(4):e18
Ozawa G, Shimamura S, Takaki Y, Yokobori SI, Ohara Y, Takishita K, Maruyama T, Fujikura K, Yoshida T (2016) Updated mitochondrial phylogeny of pteriomorph and heterodont bivalvia, including deep-sea chemosymbiotic bathymodiolus mussels, vesicomyid clams and the thyasirid clam conchocele cf. bisecta. Mar Genomics 43:43–52
Pääbo S, Thomas WK, Whitfield KM, Kumazawa Y, Wilson AC (1991) Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol 33(5):426
Pei H, Peng Q, Lan C, Chi LB (2016) Variations in mitochondrial tRNA(Thr) gene may not be associated with coronary heart disease. Mitochondrial DNA 27(1):565–568
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Rambaut A, Drummond AJ (2013) Tracer V1.6.
Rokas A, Ladoukakis E, Zouros E (2003) Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18(8):411–417
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542
Scarlato OA, Starobogatov YI (1978) Phylogenetic relations and the early evolution of the class bivalvia. Philos Trans R Soc Lond B Biol Sci 284(1001):217–224
Searle JB (2000) Phylogeography—the history and formation of species. Heredity 85(2):201–201
Shen X, Chu KH, Chan BKK, Tsang LM (2016) The complete mitochondrial genome of the fire coral-inhabiting barnacle Megabalanus ajax (Sessilia: Balanidae): gene rearrangements and atypical gene content. Mitochondrial DNA Part A 27(2):1173–1174
Simison WB, Lindberg DR, Boore JL (2006) Rolling circle amplification of metazoan mitochondrial genomes. Mol Phylogenet Evol 39(2):562–567
Skibinski DOF, Gallagher C, Beynon CM (1994) Mitochondrial DNA inheritance. Nature 368(6474):817–818
Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36(6):545–554
Soot-Ryen T (1955) A report on the family mytilidae (Pelecypoda). Report Allan Hancock Pacific Expedition 20:174
Soot-Ryen T (1969) Superfamily Mytilacea Rafinesque, 1815. 271-280.
Starobogatov YI (1992) Morphological basis for phylogeny and classification of Bivalvia. Ruthenica 2:1–25
Sun W, Gao L (2017) Phylogeny and comparative genomic analysis of Pteriomorphia (Mollusca: Bivalvia) based on complete mitochondrial genomes. Mar Ar Biol Res 13(3):255–268
Sun SE, Li Q, Kong L, Yu H (2017) Multiple reversals of strand asymmetry in molluscs mitochondrial genomes, and consequences for phylogenetic inferences. Mol Phylogenet Evol 118:222–231
Swofford D, Swofford T, Swofford DL, (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods).
Tan KS, Tan SHM, Sanpanich K, Duangdee T, Ambarwati R (2022) Xenostrobus or Vignadula (Bivalvia: Mytilidae)? A taxonomic re-evaluation of small black mussels inhabiting the upper intertidal zone of the estuaries of Southeast Asia. Zool J Linn Soc-Lond.
Vakily JM (1989) The Biology and Culture of Mussels of the Genus Perna. The WorldFish Center, Penang
Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295(5558):1253–1257
Wang ZR (1997) Fauna Sinica: Phylum Mollusca. Order Mytiloida Science Press, Beijing
Wei ZP (2008) Analysis of the COI gene fragment of the Perna viridis and the complete mitochondrial genome of the Crassostrea hongkongensis.
Wilson BR, Hodgkin EP (1967) A comparative account of the reproductive cycles of five species of marine mussels (Bivalvia: Mytilidae) in the vicinity of fremantle Western Australia. Mar Freshwater Res 18(2):175–204
Wood AR, Apte S, MacAvoy ES, Gardner JPA (2007) A molecular phylogeny of the marine mussel genus Perna (Bivalvia: Mytilidae) based on nuclear (ITS1&2) and mitochondrial (COI) DNA sequences. Mol Phylogenet Evol 44(2):685–698
Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 32:371–373
Xia X, Zheng X, Salemi M, Lu C, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26(1):1–7
Xin Z, Liu Y, Li C, Zhang D, Jiang S, Zhang H, Zhou C, Tang B, Liu Q, Dai L (2018) Mitochondrial genome of Argopecten irradians reveals higher-level phylogenetic relationships in anisomyaria. Int J Biol Macromol 117:1089–1092
Xu T, Feng D, Tao J, Qiu J (2019) A new species of deep-sea mussel (Bivalvia: Mytilidae: Gigantidas) from the South China Sea: morphology, phylogenetic position, and gill-associated microbes. Deep Sea Res Part I 146:79–90
Yokobori S, Ueda T (1999) Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi. Genetics 153(4):1851
Yuan Y, Qi L, Hong Y, Kong L, Ouzounis CA (2012) The complete mitochondrial genomes of six heterodont bivalves (tellinoidea and solenoidea): variable gene arrangements and phylogenetic implications. PLoS ONE 7(2):e32353
Funding
This work was financially supported by the National Key R&D Program of China (2019YFD0901204), NSFC Projects of International Cooperation and Exchanges (42020104009), and the National Natural Science Foundation of China (42107301).
Author information
Authors and Affiliations
Contributions
YYY and XJY: leading—interpreted the results, provided funds for this study. MHX: writing—acquisition the data, analyzed the data, wrote the manuscript, collected samples, and prepared genomic DNA. KDX, BYGuo, and JJL: supporting—analyzed the data, wrote the manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
All authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethical Approval
The study was conducted by the guidelines and regulations of the government. No endangered or protected species were involved. Sampling also did not require specific permissions for the location.
Consent to Publish
Agree.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Xu, M., Li, J., Guo, B. et al. Insights into the Deep Phylogeny and Novel Gene Rearrangement of Mytiloidea from Complete Mitochondrial Genome. Biochem Genet 61, 1704–1726 (2023). https://doi.org/10.1007/s10528-023-10338-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-023-10338-4