Cite this paper:
Mei YANG, Jixing SUI, Xinzheng LI. The first complete mitogenome of Acharax sp. (Protobranchia, Solemyida, Solemyidae): comparisons with other Solemyidae bivalves and deep-sea adaptive characteristics[J]. Journal of Oceanology and Limnology, 2023, 41(6): 2374-2390

The first complete mitogenome of Acharax sp. (Protobranchia, Solemyida, Solemyidae): comparisons with other Solemyidae bivalves and deep-sea adaptive characteristics

Mei YANG1,2, Jixing SUI1,2, Xinzheng LI1,2,3,4
1 Department of Marine Organism Taxonomy&Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
3 University of Chinese Academy of Sciences, Beijing 100049, China;
4 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
Abstract:
Solemyidae is an ancient group of protobranch bivalves, and most solemyids are symbiotic with chemoautotrophic and gill-hosted bacteria, enabling them to survive in unusual habitats such as deep-sea chemosynthetic environments. However, evolution of the mitogenomes in this family and their phylogenetic relationships remain poorly understood. The complete mitogenome of Acharax sp. was determined and compared with other available mitogenomes of solemyids. The mitogenome of Acharax sp. is 18 970 bp in length and consists of 13 protein-coding genes, 2 ribosomal RNA genes, and 22 transfer RNA genes. The gene arrangement was identical to those of other sequenced solemyids. For the present five mitogenomes of Solemyidae species, all protein-coding genes were initiated with the typical ATD (ATA, ATG, and ATT) codon and terminated with the TAA/TAG codon. Furthermore, the incomplete termination codon was detected. The Ka/Ks ratio analyses indicated that 13 protein-coding genes of five Solemyidae mitogenomes suffered strong purifying selection. Compared to 45 existing shallow water equivalents, the 18 available mitogenomes from the deep-sea, including the Acharax sp. in this study, show significantly more nonpolar amino acids in the 13 protein-coding genes, which indicates the adaptation to the deep-sea environment. The phylogenetic tree based on 48 Bivalvia complete mitogenomes provided further information to support the scientific classification of protobranchs. The relationships among Solemyidae were assessed based on 2 mitochondrial (16S rRNA and COX1) and 3 nuclear (18S rRNA, 28S rRNA, and histone H3) gene sequences from 17 in-group species. The two genera Acharax and Solemya formed a monophyletic clade each, and Acharax sp. clustered with previously reported Acharax bivalves with high support values.
Key words:    Solemyidae|Acharax|mitogenome|deep sea|adaptation|phylogeny   
Received: 2022-05-07   Revised:
Tools
PDF (7475 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Mei YANG
Articles by Jixing SUI
Articles by Xinzheng LI
References:
Anisimova M, Gil M, Dufayard J F et al.2011.Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes.Systematic Biology, 60(5):685-699, https://doi.org/10.1093/sysbio/syr041.
Barrientos A, Barros M H, Valnot I et al.2002.Cytochrome oxidase in health and disease.Gene, 286(1):53-63, https://doi.org/10.1016/S0378-1119(01)00803-4.
Bernt M, Donath A, Jühling F et al.2013.MITOS:improved de novo metazoan mitochondrial genome annotation.Molecular Phylogenetics and Evolution, 69(2):313-319, https://doi.org/10.1016/j.ympev.2012.08.023.
Bernt M, Merkle D, Ramsch K et al.2007.CREx:inferring genomic rearrangements based on common intervals.Bioinformatics, 23(21):2957-2958, https://doi.org/10.1093/bioinformatics/btm468.
Bieler R, Mikkelsen P M, Giribet G.2013.Bivalvia-A discussion of known unknowns.American Malacological Bulletin, 31(1):123-133, https://doi.org/10.4003/006.031.0105.
Boore J L.1999.Animal mitochondrial genomes.Nucleic Acids Research, 27(8):1767-1780, https://doi.org/10.1093/nar/27.8.1767.
Chan P P, Lowe T M.2019.tRNAscan-SE:searching for tRNA genes in genomic sequences.In:Kollmar M ed.Gene Prediction:Methods and Protocols.Humana, New York.p.1-14, https://doi.org/10.1007/978-1-4939-9173-0_1.
Conway N M, Howes B L, McDowell Capuzzo J E et al.1992.Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis.Marine Biology, 112(4):601-613, https://doi.org/10.1007/BF00346178.
Cunha R L, Grande C, Zardoya R.2009.Neogastropod phylogenetic relationships based on entire mitochondrial genomes.BMC Evolutionary Biology, 9:210, https://doi.org/10.1186/1471-2148-9-210.
da Fonseca R R, Johnson W E, O'Brien S J et al.2008.The adaptive evolution of the mammalian mitochondrial genome.BMC Genomics, 9:119, https://doi.org/10.1186/1471-2164-9-119.
Dreyer H, Steiner G.2006.The complete sequences and gene organisation of the mitochondrial genomes of the heterodont bivalves Acanthocardia tuberculata and Hiatella arctica-and the first record for a putative Atpase subunit 8 gene in marine bivalves.Frontiers in Zoology, 3:13, https://doi.org/10.1186/1742-9994-3-13.
Fisher C R, Childress J J.1986.Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi.Marine Biology, 93(1):59-68, https://doi.org/10.1007/BF00428655.
Fujiwara Y.2003.Symbiotic adaptation for deeper habitats in chemosynthetic environments.Journal of Geography (Chigaku Zasshi), 112(2):302-308, https://doi.org/10.5026/jgeography.112.2_302.
Fukasawa Y, Matsumoto H, Beppu S et al.2017.Molecular phylogenetic analysis of chemosymbiotic Solemyidae and Thyasiridae.Open Journal of Marine Science, 7(1):124-141, https://doi.org/10.4236/ojms.2017.71010.
Guerra D, Bouvet K, Breton S.2018.Mitochondrial gene order evolution in Mollusca:inference of the ancestral state from the mtDNA of Chaetopleura apiculata (polyplacophora, chaetopleuridae).Molecular Phylogenetics and Evolution, 120:233-239, https://doi.org/10.1016/j.ympev.2017.12.013.
Hao J S, Sun Q Q, Zhao H B et al.2012.The complete mitochondrial genome of Ctenoptilum vasava (Lepidoptera:Hesperiidae:Pyrginae) and its phylogenetic implication.Comparative and Functional Genomics, 2012:328049, https://doi.org/10.1155/2012/328049.
Hassanin A, Ropiquet A, Couloux A et al.2009.Evolution of the mitochondrial genome in mammals living at high altitude:new insights from a study of the tribe Caprini (Bovidae, Antilopinae).Journal of Molecular Evolution, 68(4):293-310, https://doi.org/10.1007/s00239-009-9208-7.
Hoang D T, Chernomor O, von Haeseler A et al.2018.UFBoot2:improving the ultrafast bootstrap approximation.Molecular Biology and Evolution, 35(2):518-522, https://doi.org/10.1093/molbev/msx281.
Kamenev G M.2009.North Pacific species of the genus Solemya Lamarck, 1818 (Bivalvia:Solemyidae), with notes on Acharax johnsoni (Dall, 1891).Malacologia, 51(2):233-261, https://doi.org/10.4002/040.051.0202.
Katoh K, Rozewicki J, Yamada K D.2019.MAFFT online service:multiple sequence alignment, interactive sequence choice and visualization.Briefings in Bioinformatics, 20(4):1160-1166, https://doi.org/10.1093/bib/bbx108.
Kou Q, Xu P, Poore G C B et al.2020.A new species of the deep-sea sponge-associated genus Eiconaxius (Crustacea:Decapoda:Axiidae), with new insights into the distribution, speciation, and mitogenomic phylogeny of axiidean shrimps.Frontiers in Marine Science, 7:469, https://doi.org/10.3389/fmars.2020.00469.
Kück P, Meid S A, Groß C et al.2014.AliGROOVE-visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support.BMC Bioinformatics, 15(1):294, https://doi.org/10.1186/1471-2105-15-294.
Kumar S, Stecher G, Tamura K.2016.MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets.Molecular Biology and Evolution, 33(7):1870-1874, https://doi.org/10.1093/molbev/msw054.
Lanfear R, Frandsen P B, Wright A M et al.2016.PartitionFinder 2:new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Molecular Biology and Evolution, 34:772-773, https://doi.org/10.1093/molbev/msw260.
Lavrov D V, Brown W M, Boore J L.2000.A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus.Proceedings of the National Academy of Sciences of the United States of America, 97(25):13738-13742, https://doi.org/10.1073/pnas.250402997.
Lemer S, Bieler R, Giribet G.2019.Resolving the relationships of clams and cockles:dense transcriptome sampling drastically improves the bivalve tree of life.Proceedings of the Royal Society B:Biological Sciences, 286(1896):20182684, https://doi.org/10.1098/rspb.2018.2684.
Letunic I, Bork P.2007.Interactive tree of life (iTOL):an online tool for phylogenetic tree display and annotation.Bioinformatics, 23(1):127-128, https://doi.org/10.1093/bioinformatics/btl529.
Li J, Zhao Y Q, Lin R R et al.2019a.Mitochondrial genome characteristics of Somena scintillans (Lepidoptera:Erebidae) and comparation with other Noctuoidea insects.Genomics, 111(6):1239-1248, https://doi.org/10.1016/j.ygeno.2018.08.003.
Li J Y, Song Z L, Yan G Y et al.2019b.The complete mitochondrial genome of the largest amphipod, Alicella gigantea:insight into its phylogenetic relationships and deep sea adaptive characters.International Journal of Biological Macromolecules, 141:570-577, https://doi.org/10.1016/j.ijbiomac.2019.09.050.
Liu H Y, Yang Y, Sun S E et al.2020.Mitogenomic phylogeny of the Naticidae (Gastropoda:Littorinimorpha) reveals monophyly of the Polinicinae.Zoologica Scripta, 49(3):295-306, https://doi.org/10.1111/zsc.12412.
Lohse M, Drechsel O, Bock R.2007.OrganellarGenomeDRAW (OGDRAW):a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes.Current Genetics, 52(5):267-274, https://doi.org/10.1007/s00294-007-0161-y.
Luo Y J, Gao W X, Gao Y Q et al.2008.Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation.Mitochondrion, 8(5-6):352-357, https://doi.org/10.1016/j.mito.2008.07.005.
Lü Z M, Zhu K H, Jiang H et al.2019.Complete mitochondrial genome of Ophichthus brevicaudatus reveals novel gene order and phylogenetic relationships of Anguilliformes.International Journal of Biological Macromolecules, 135:609-618, https://doi.org/10.1016/j.ijbiomac.2019.05.139.
Metpally R P R, Reddy B V B.2009.Comparative proteome analysis of psychrophilic versus mesophilic bacterial species:insights into the molecular basis of cold adaptation of proteins.BMC Genomics, 10:11, https://doi.org/10.1186/1471-2164-10-11.
Mu W D, Liu J, Zhang H B.2018.The first complete mitochondrial genome of the Mariana Trench Freyastera benthophila (Asteroidea:Brisingida:Brisingidae) allows insights into the deep-sea adaptive evolution of Brisingida.Ecology and Evolution, 8(22):10673-10686, https://doi.org/10.1002/ece3.4427.
Neulinger S C, Sahling H, Süling J et al.2006.Presence of two phylogenetically distinct groups in the deep-sea mussel Acharax (Mollusca:Bivalvia:Solemyidae).Marine Ecology Progress Series, 312:161-168, https://doi.org/10.3354/meps312161.
Nguyen L T, Schmidt H A, von Haeseler A et al.2015.IQ-TREE:a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Molecular Biology and Evolution, 32(1):268-274, https://doi.org/10.1093/molbev/msu300.
Oliver G, Rodrigues C F, Cunha M R.2011.Chemosymbiotic bivalves from the mud volcanoes of the Gulf of Cadiz, NE Atlantic, with descriptions of new species of Solemyidae, Lucinidae and Vesicomyidae.ZooKeys, 113:1-38, https://doi.org/10.3897/zookeys.113.1402.
Perna N T, Kocher T D.1995.Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes.Journal of Molecular Evolution, 41(3):353-358, https://doi.org/10.1007/BF00186547.
Plazzi F, Ribani A, Passamonti M.2013.The complete mitochondrial genome of Solemya velum (Mollusca:Bivalvia) and its relationships with Conchifera.BMC Genomics 14:409, https://doi.org/10.1186/1471-2164-14-409.
Pojeta J J.1988.The origin and Paleozoic diversification of Solemyoid Pelecypods.New Mexico Bureau of Mines and Mineral Resources, Memoir, 44:201-271.
Rahuman S, Jeena N S, Asokan P K et al.2020.Mitogenomic architecture of the multivalent endemic black clam (Villorita cyprinoides) and its phylogenetic implications.Scientific Reports, 10(1):15438, https://doi.org/10.1038/s41598-020-72194-1.
Rex M A.1981.Community structure in the deep-sea Benthos.Annual Review of Ecology and Systematics, 12:331-353.
Rodrigues C F, Webster G, Cunha M R et al.2010.Chemosynthetic bacteria found in bivalve species from mud volcanoes of the Gulf of Cadiz.FEMS Microbiology Ecology, 73(3):486-499, https://doi.org/10.1111/j.1574-6941.2010.00913.x.
Ronquist F, Teslenko M, van der Mark P et al.2012.MrBayes 3.2:efficient Bayesian phylogenetic inference and model choice across a large model space.Systematic Biology, 61(3):539-542, https://doi.org/10.1093/sysbio/sys029.
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio J C et al.2017.DnaSP 6:DNA sequence polymorphism analysis of large data sets.Molecular Biology and Evolution, 34(12):3299-3302, https://doi.org/10.1093/molbev/msx248.
Russell S L, McCartney E, Cavanaugh C M.2018.Transmission strategies in a chemosynthetic symbiosis:detection and quantification of symbionts in host tissues and their environment.Proceedings of the Royal Society B:Biological Sciences, 285(1890):20182157, https://doi.org/10.1098/rspb.2018.2157.
Saether K P, Sha J G, Little C T S et al.2016.New records and a new species of bivalve (Mollusca:Bivalvia) from Miocene hydrocarbon seep deposits, North Island, New Zealand.Zootaxa, 4154(1):1-26, https://doi.org/10.11646/zootaxa.4154.1.1.
Salvato P, Simonato M, Battisti A et al.2008.The complete mitochondrial genome of the bag-shelter moth Ochrogaster lunifer (Lepidoptera, Notodontidae).BMC Genomics, 9:331, https://doi.org/10.1186/1471-2164-9-33.
Sato K, Kano Y, Setiamarga D H E et al.2020.Molecular phylogeny of protobranch bivalves and systematic implications of their shell microstructure.Zoologica Scripta, 49(4):458-472, https://doi.org/10.1111/zsc.12419.
Sato K, Nakashima R, Majima R et al.2013.Shell microstructures of five recent solemyids from Japan (Mollusca:Bivalvia).Paleontological Research, 17(1):69-90, https://doi.org/10.2517/1342-8144-17.1.69.
Satoh T P, Miya M, Mabuchi K et al.2016.Structure and variation of the mitochondrial genome of fishes.BMC Genomics, 17:719, https://doi.org/10.1186/s12864-016-3054-y.
Seike K, Jenkins R G, Watanabe H et al.2012.Novel use of burrow casting as a research tool in deep-sea ecology.Biology Letters, 8(4):648-651, https://doi.org/10.1098/rsbl.2011.1111.
Sharma P P, Zardus J D, Boyle E E et al.2013.Into the Deep:a phylogenetic approach to the bivalve subclass Protobranchia.Molecular Phylogenetics and Evolution, 69(1):188-204, https://doi.org/10.1016/j.ympev.2013.05.018.
Sun S E, Sha Z L, Wang Y R.2018.Complete mitochondrial genome of the first deep-sea spongicolid shrimp Spongiocaris panglao (Decapoda:Stenopodidea):novel gene arrangement and the phylogenetic position and origin of Stenopodidea.Gene, 676:123-138, https://doi.org/10.1016/j.gene.2018.07.026.
Talavera G, Castresana J.2007.Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Systematic Biology, 56(4):564-577, https://doi.org/10.1080/1063515 0701472164.
Taylor J D, Glover E A, Williams S T.2008.Ancient chemosynthetic bivalves:systematics of Solemyidae from eastern and southern Australia (Mollusca:Bivalvia).Memoirs Queensland Museum-Nature, 54(1):75-104.
Tomasco I H, Lessa E P.2011.The evolution of mitochondrial genomes in subterranean caviomorph rodents:adaptation against a background of purifying selection.Molecular Phylogenetics and Evolution, 61(1):64-70, https://doi.org/10.1016/j.ympev.2011.06.014.
Uribe J E, Zardoya R, Puillandre N.2018.Phylogenetic relationships of the conoidean snails (Gastropoda:Caenogastropoda) based on mitochondrial genomes.Molecular Phylogenetics and Evolution, 127:898-906, https://doi.org/10.1016/j.ympev.2018.06.037.
Walton K.2015.New Zealand living Solemyidae (Bivalvia:Protobranchia).Molluscan Research, 35(4):246-261, https://doi.org/10.1080/13235818.2015.1053168.
Wang K, Shen Y J, Yang Y Z et al.2019.Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation.Nature Ecology & Evolution, 3(5):823-833, https://doi.org/10.1038/s41559-019-0864-8.
Wang Y, Shen Y J, Feng C G et al.2016a.Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude.Scientific Reports, 6:29690, https://doi.org/10.1038/srep29690.
Wang Z L, Li C, Fang W Y et al.2016b.The complete mitochondrial genome of two Tetragnatha spiders (Araneae:Tetragnathidae):severe truncation of tRNAs and novel gene rearrangements in Araneae.International Journal of Biological Sciences, 12(1):109-119, https://doi.org/10.7150/ijbs.12358.
Wei S J, Shi M, Chen X X et al.2010.New views on strand asymmetry in insect mitochondrial genomes.PLoS One, 5(9):e12708, https://doi.org/10.1371/journal.pone.0012708.
Xu F S.1999.Fauna Sinica:Phylum Mollusca:Class Bivalvia:Subclass Protobranchia and Anomalodesmata.Science Press, Beijing, China.p.1-244.(in Chinese)
Xu S Q, Luosang J, Hua S et al.2007.High altitude adaptation and phylogenetic analysis of Tibetan horse based on the mitochondrial genome.Journal of Genetics and Genomics, 34(8):720-729, https://doi.org/10.1016/S1673-8527(07)60081-2.
Xu S Q, Yang Y Z, Zhou J et al.2005.A mitochondrial genome sequence of the Tibetan antelope (Pantholops hodgsonii).Genomics, Proteomics & Bioinformatics, 3(1):5-17, https://doi.org/10.1016/S1672-0229(05)03003-2.
Yang L L, Tang S K, Huang Y et al.2015.Low temperature adaptation is not the opposite process of high temperature adaptation in terms of changes in amino acid composition.Genome Biology and Evolution, 7(12):3426-3433, https://doi.org/10.1093/gbe/evv232.
Yang M, Dong D, Li X Z.2021.The complete mitogenome of Phymorhynchus sp.(Neogastropoda, Conoidea, Raphitomidae) provides insights into the deep-sea adaptive evolution of Conoidea.Ecology and Evolution, 11(12):7518-7531, https://doi.org/10.1002/ece3.7582.
Yang M, Gong L, Sui J X et al.2019.The complete mitochondrial genome of Calyptogena marissinica (Heterodonta:Veneroida:Vesicomyidae):insight into the deep-sea adaptive evolution of vesicomyids.PLoS One, 14(9):e0217952, https://doi.org/10.1371/journal.pone.0217952.
Yang Z H, Bielawski J P.2000.Statistical methods for detecting molecular adaptation.Trends in Ecology & Evolution, 15(12):496-503, https://doi.org/10.1016/S0169-5347(00)01994-7.
Yu L, Wang X P, Ting N et al.2011.Mitogenomic analysis of Chinese snub-nosed monkeys:evidence of positive selection in NADH dehydrogenase genes in high-altitude adaptation.Mitochondrion, 11(3):497-503, https://doi.org/10.1016/j.mito.2011.01.004.
Zardus J D.2002.Protobranch bivalves.Advances in Marine Biology, 42:1-65, https://doi.org/10.1016/S0065-2881 (02)42012-3.
Zhang B, Wu Y Y, Wang X et al.2020a.Comparative analysis of mitochondrial genome of a deep-sea crab Chaceon granulates reveals positive selection and novel genetic features.Journal of Oceanology and Limnology, 38(2):427-437, https://doi.org/10.1007/s00343-019-8364-x.
Zhang B, Zhang Y H, Wang X et al.2017a.The mitochondrial genome of a sea anemone Bolocera sp.exhibits novel genetic structures potentially involved in adaptation to the deep-sea environment.Ecology and Evolution, 7(13):4951-4962, https://doi.org/10.1002/ece3.3067.
Zhang D, Gao F L, Jakovlić I et al.2020b.PhyloSuite:an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies.Molecular Ecology Resources, 20(1):348-355, https://doi.org/10.1111/1755-0998.13096.
Zhang K, Sun J, Xu T et al.2021.Phylogenetic relationships and adaptation in deep-sea mussels:insights from mitochondrial genomes.International Journal of Molecular Sciences, 22(4):1900, https://doi.org/10.3390/ijms22041900.
Zhang Y J, Sun J, Chen C et al.2017b.Adaptation and evolution of deep-sea scale worms (Annelida:Polynoidae):insights from transcriptome comparison with a shallow-water species.Scientific Reports, 7:46205, https://doi.org/10.1038/srep46205.
Zhu K C, Liang Y Y, Wu N et al.2017.Sequencing and characterization of the complete mitochondrial genome of Japanese Swellshark (Cephalloscyllium umbratile).Scientific Reports, 7:15299, https://doi.org/10.1038/s41598-017-15702-0.
Copyright © Haiyang Xuebao