Abstract
Here, we sequenced the complete mitogenome of Parasesarma eumolpe (Brachyura: Grapsoidea: Sesarmidae) for the first time. The characteristics of this newly sequenced mitogenome were described and compared with other Sesarmidae species. The 15 646-bp mitogenome contains 13 protein-coding genes (PCGs), two ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs), and an A-T rich region. All of the PCGs are initiated by the start codon ATN and terminated by the standard TAN codon or an incomplete T. The pairwise Ka/Ks ratio analysis shows that all 13 PCGs are under purifying selection, whereas the ATP8 gene is an outlier, with pairwise comparison values ranging from neutral selection (0.000) to positive selection (1.039). The gene arrangement of P. eumolpe compared with ancestral Decapoda shows the translocation of two tRNAs (tRNA-His and tRNA-Gln), which is identical to other Sesarmidae species. Phylogenetic analyses show that all Sesarmidae species are placed into one group, and the polyphyly of Eriphioidea, Ocypodoidea, and Grapsoidea is well supported. The relationship between gaps in the QIM region and the phylogeny of Sesarmidae is analyzed. It is obvious that both the G5 (the gap between Q and I) and G6 (the gap between I and M) decrease progressively with the evolution process. These results will help to better understand the genomic evolution within Sesarmidae and provide insights into the phylogeny of Brachyura.
Similar content being viewed by others
References
Arndt A, Smith M J. 1998. Mitochondrial gene rearrangement in the sea cucumber genus Cucumaria. Molecular Biology and Evolution, 15(8): 1009–1016, doi: https://doi.org/10.1093/oxfordjournals.molbev.a025999
Basso A, Babbucci M, Pauletto M, et al. 2017. The highly rearranged mitochondrial genomes of the crabs Maja crispata and Maja squinado (Majidae) and gene order evolution in Brachyura. Scientific Reports, 7(1): 4096, doi: https://doi.org/10.1038/s41598-017-04168-9
Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27(2): 573–580, doi: https://doi.org/10.1093/nar/27.2.573
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, doi: https://doi.org/10.1016/j.ympev.2012.08.023
Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767–1780, doi: https://doi.org/10.1093/nar/27.8.1767
Boussau B, Walton Z, Delgado J A, et al. 2014. Strepsiptera, phylogenomics and the long branch attraction problem. PLoS ONE, 9(10): e107709, doi: https://doi.org/10.1371/journal.pone.0107709
Cantatore P, Gadaleta M N, Roberti M, et al. 1987. Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature, 329(6142): 853–855, doi: https://doi.org/10.1038/329853a0
Chen Jianqin, **ng Yuhui, Yao Wenjia, et al. 2018. Characterization of four new mitogenomes from Ocypodoidea & Grapsoidea, and phylomitogenomic insights into thoracotreme evolution. Gene, 675: 27–35, doi: https://doi.org/10.1016/j.gene.2018.06.088
Dierckxsens N, Mardulyn P, Smits G. 2017. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research, 45(4): e18
Evans N. 2018. Molecular phylogenetics of swimming crabs (Portunoidea Rafinesque, 1815) supports a revised family-level classification and suggests a single derived origin of symbiotic taxa. PeerJ, 6: e4260, doi: https://doi.org/10.7717/peerj.4260
Gillikin D P, Schubart C D. 2004. Ecology and systematics of mangrove crabs of the genus Perisesarma (Crustacea: Brachyura: Sesarmidae) from East Africa. Zoological Journal of the Linnean Society, 141(3): 435–445, doi: https://doi.org/10.1111/J.1096-3642.2004.00125.x
Gong Li, Jiang Hui, Zhu Kehua, et al. 2019. Large-scale mitochondrial gene rearrangements in the hermit crab Pagurus nigrofascia and phylogenetic analysis of the Anomura. Gene, 695: 75–83, doi: https://doi.org/10.1016/j.gene.2019.01.035
Gong Li, Lu **nting, Luo Hairong, et al. 2020a. Novel gene rearrangement pattern in Cynoglossus melampetalus mitochondrial genome: new gene order in genus Cynoglossus (Pleuronectiformes: Cynoglossidae). International Journal of Biological Macromolecules, 149: 1232–1240, doi: https://doi.org/10.1016/j.ijbiomac.2020.02.017
Gong Li, Lu **nting, Wang Zhifu, et al. 2020b. Novel gene rearrangement in the mitochondrial genome of Coenobita brevimanus (Anomura: Coenobitidae) and phylogenetic implications for Anomura. Genomics, 112(2): 1804–1812, doi: https://doi.org/10.1016/j.ygeno.2019.10.012
Gong Li, Shi Wei, Si Lizhen, et al. 2013. Rearrangement of mitochondrial genome in fishes. Zoological Research, 34(6): 666–673
Guo **nhong, Liu Shaojun, Liu Yun. 2003. Comparative analysis of the mitochondrial DNA control region in cyprinids with different ploidy level. Aquaculture, 224(1–4): 25–38, doi: https://doi.org/10.1016/S0044-8486(03)00168-6
Gyllensten U, Wharton D, Josefsson A, et al. 1991. Paternal inheritance of mitochondrial DNA in mice. Nature, 352(6332): 255–257, doi: https://doi.org/10.1038/352255a0
Hebert P D N, Ratnasingham S, De Waard J R. 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences, 270(S1): S96–S99
Kumar S, Stecher G, Li M, et al. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547–1549, doi: https://doi.org/10.1093/molbev/msy096
Kumazawa Y, Nishida M. 1995. Variations in mitochondrial tRNA gene organization of reptiles as phylogenetic markers. Molecular Biology and Evolution, 12(5): 759–772
Larkin M A, Blackshields G, Brown N P, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21): 2947–2948, doi: https://doi.org/10.1093/bioinformatics/btm404
Lavrov D V, Boore J L, Brown W M. 2002. Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Molecular Biology and Evolution, 19(2): 163–169, doi: https://doi.org/10.1093/oxfordjournals.molbev.a004068
Lee S Y. 1998. Ecological role of grapsid crabs in mangrove ecosystems: a review. Marine and Freshwater Research, 49(4): 335–343, doi: https://doi.org/10.1071/MF97179
Liu Qiuning, **n Zhaozhe, Zhu **aoyu, et al. 2017. A transfer RNA gene rearrangement in the lepidopteran mitochondrial genome. Biochemical and Biophysical Research Communications, 489(2): 149–154, doi: https://doi.org/10.1016/j.bbrc.2017.05.115
Lowe T M, Chan P P. 2016. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research, 44(W1): W54–W57, doi: https://doi.org/10.1093/nar/gkw413
Lu **nting, Gong Li, Zhang Ying, et al. 2020. The complete mitochon-drial genome of Calappa bilineata: the first representative from the family Calappidae and its phylogenetic position within Brachyura. Genomics, 112(3): 2516–2523, doi: https://doi.org/10.1016/j.ygeno.2020.02.003
Lü Zhenming, Zhu Kehua, Jiang Hui, 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, doi: https://doi.org/10.1016/j.ijbiomac.2019.05.139
Luo Hairong, Kong **aoyu, Chen Shixi, et al. 2019. Mechanisms of gene rearrangement in 13 bothids based on comparison with a newly completed mitogenome of the threespot flounder, Grammatobothus polyophthalmus (Pleuronectiformes: Bothidae). BMC Genomics, 20(1): 792, doi: https://doi.org/10.1186/s12864-019-6128-9
Ma Kayan, Qin **g, Lin Chia-Wei, et al. 2019. Phylogenomic analyses of brachyuran crabs support early divergence of primary freshwater crabs. Molecular Phylogenetics and Evolution, 135: 62–66, doi: https://doi.org/10.1016/j.ympev.2019.02.001
Ma Zhihong, Yang Xuefen, Bercsenyi M, et al. 2015. Comparative mitogenomics of the genus Odontobutis (Perciformes: Gobioidei: Odontobutidae) revealed conserved gene rearrangement and high sequence variations. International Journal of Molecular Sciences, 16(10): 25031–25049, doi: https://doi.org/10.3390/ijms161025031
Macey J R, Larson A, Ananjeva N B, et al. 1997. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Molecular Biology and Evolution, 14(1): 91–104, doi: https://doi.org/10.1093/oxfordjournals.molbev.a025706
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal, 17(1): 10–12
McKnight M L, Shaffer H B. 1997. Large, rapidly evolving intergenic spacers in the mitochondrial DNA of the salamander family Ambystomatidae (Amphibia: Caudata). Molecular Biology and Evolution, 14(11): 1167–1176, doi: https://doi.org/10.1093/oxfordjournals.molbev.a025726
Moritz C, Dowling T E, Brown W M. 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18: 269–292, doi: https://doi.org/10.1146/annurev.es.18.110187.001413
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, doi: https://doi.org/10.1093/molbev/msu300
Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature, 290(5806): 470–474, doi: https://doi.org/10.1038/290470a0
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, doi: https://doi.org/10.1007/BF01215182
Philippe H. 2000. Opinion: long branch attraction and protist phylogeny. Protist, 151(4): 307–316, doi: https://doi.org/10.1078/S1434-4610(04)70029-2
Poulton J, Deadman M E, Bindoff L, et al. 1993. Families of mtDNA re-arrangements can be detected in patients with mtDNA deletions: duplications may be a transient intermediate form. Human Molecular Genetics, 2(1): 23–30, doi: https://doi.org/10.1093/hmg/2.1.23
Ray D A, Densmore L. 2002. The crocodilian mitochondrial control region: general structure, conserved sequences, and evolutionary implications. Journal of Experimental Zoology, 294(4): 334–345, doi: https://doi.org/10.1002/jez.10198
Ren Lipin, Zhang **angyan, Li Yi, et al. 2020. Comparative analysis of mitochondrial genomes among the subfamily Sarcophaginae (Diptera: Sarcophagidae) and phylogenetic implications. International Journal of Biological Macromolecules, 161: 214–222, doi: https://doi.org/10.1016/j.ijbiomac.2020.06.043
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, doi: 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, doi: https://doi.org/10.1093/molbev/msx248
Ruan Huiting, Li Min, Li Zhenhai, et al. 2020. Comparative analysis of complete mitochondrial genomes of three Gerres fishes (Perciformes: Gerreidae) and primary exploration of their evolution history. International Journal of Molecular Sciences, 21(5): 1874, doi: https://doi.org/10.3390/ijms21051874
Sanchez G, Tomano S, Yamashiro C, et al. 2016. Population genetics of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) in the northern Humboldt Current system based on mitochondrial and microsatellite DNA markers. Fisheries Research, 175: 1–9, doi: https://doi.org/10.1016/j.fishres.2015.11.005
Sato M, Sato K. 2013. Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1833(8): 1979–1984, doi: https://doi.org/10.1016/j.bbamcr.2013.03.010
Shahdadi A, Ng P K L, Schubart C D. 2018. Morphological and phylogenetic evidence for a new species of Parasesarma De Man, 1895 (Crustacea: Decapoda: Brachyura: Sesarmidae) from the Malay Peninsula, previously referred to as Parasesarma indiarum (Tweedie, 1940). Raffles Bulletin of Zoology, 66: 739–762
Shahdadi A, Schubart C D. 2015. Evaluating the consistency and taxonomic importance of cheliped and other morphological characters that potentially allow identification of species of the genus Perisesarma De Man, 1895 (Brachyura, Sesarmidae). Crustaceana, 88(10–11): 1079–1095, doi: https://doi.org/10.1163/15685403-00003473
Shahdadi A, Schubart C D. 2018. Taxonomic review of Perisesarma (Decapoda: Brachyura: Sesarmidae) and closely related genera based on morphology and molecular phylogenetics: new classification, two new genera and the questionable phylogenetic value of the epibranchial tooth. Zoological Journal of the Linnean Society, 182(3): 517–548, doi: https://doi.org/10.1093/zoolinnean/zlx032
Stothard P, Wishart D S. 2005. Circular genome visualization and exploration using CGView. Bioinformatics, 21(4): 537–539, doi: https://doi.org/10.1093/bioinformatics/bti054
Sun Ziqiang, Liu Yingqi, Wilson J J, et al. 2019. Mitochondrial genome of Phalantus geniculatus (Hemiptera: Reduviidae): trnT duplication and phylogenetic implications. International Journal of Biological Macromolecules, 129: 110–115, doi: https://doi.org/10.1016/j.ijbiomac.2019.01.205
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, doi: https://doi.org/10.1080/10635150701472164
Tan M H, Gan Hanming, Lee Y P, et al. 2018. ORDER within the chaos: insights into phylogenetic relationships within the Anomura (Crustacea: Decapoda) from mitochondrial sequences and gene order rearrangements. Molecular Phylogenetics and Evolution, 127: 320–331, doi: https://doi.org/10.1016/j.ympev.2018.05.015
Thyagarajan B, Padua R A, Campbell C. 1996. Mammalian mitochondria possess homologous DNA recombination activity. Journal of Biological Chemistry, 271(44): 27536–27543, doi: https://doi.org/10.1074/jbc.271.44.27536
Tsang L M, Schubart C D, Ahyong S T, et al. 2014. Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs. Molecular Biology and Evolution, 31(5): 1173–1187, doi: https://doi.org/10.1093/molbev/msu068
Tsaousis A D, Martin D P, Ladoukakis E D, et al. 2005. Widespread recombination in published animal mtDNA sequences. Molecular Biology and Evolution, 22(4): 925–933, doi: https://doi.org/10.1093/molbev/msi084
Tweedie M W F. 1954. Notes on grapsoid crabs from the Raffles Museum, Nos. 3, 4 and 5. Bulletin of the Raffles Museum, 25: 118–128
Wang Yuan, Chen **g, Jiang Liyun, et al. 2015. Hemipteran mitochondrial genomes: features, structures and implications for phylogeny. International Journal of Molecular Sciences, 16(6): 12382–12404
Wang Ziqian, Shi Xuejia, Guo Huayun, et al. 2020a. Characterization of the complete mitochondrial genome of Uca lacteus and comparison with other Brachyuran crabs. Genomics, 112(1): 10–19, doi: https://doi.org/10.1016/j.ygeno.2019.06.004
Wang Zhengfei, Shi Xuejia, Tao Yitao, et al. 2019. The complete mitochondrial genome of Parasesarma pictum (Brachyura: Grapsoidea: Sesarmidae) and comparison with other Brachyuran crabs. Genomics, 111(4): 799–807, doi: https://doi.org/10.1016/j.ygeno.2018.05.002
Wang Qi, Tang Dan, Guo Huayun, et al. 2020b. Comparative mitochondrial genomic analysis of Macrophthalmus pacificus and insights into the phylogeny of the Ocypodoidea & Grapsoidea. Genomics, 112(1): 82–91, doi: https://doi.org/10.1016/j.ygeno.2019.12.012
Wang Zhengfei, Wang Ziqian, Shi Xuejia, et al. 2018. Complete mitochondrial genome of Parasesarma affine (Brachyura: Sesarmidae): Gene rearrangements in Sesarmidae and phylogenetic analysis of the Brachyura. International Journal of Biological Macromolecules, 118: 31–40, doi: https://doi.org/10.1016/j.ijbiomac.2018.06.056
Wu **angyun, Li **aoling, Li Lu, et al. 2012. New features of Asian Crassostrea oyster mitochondrial genomes: a novel alloaccept- or tRNA gene recruitment and two novel ORFs. Gene, 507(2): 112–118, doi: https://doi.org/10.1016/j.gene.2012.07.032
**, et al. 2018. A comprehensive phylogenetic analysis of Grapsoidea crabs (Decapoda: Brachyura) based on mitochondrial cytochrome oxidase subunit 1 (CO1) genes. Turkish Journal of Zoology, 42: 46–52, doi: https://doi.org/10.3906/zoo-1703-46
Yang Ziheng. 2006. Computational Molecular Evolution. Oxford: Oxford University Press, 259–292
Yang Zhihui, Yang Tingting, Liu Yu, et al. 2019. The complete mitochondrial genome of Sinna extrema (Lepidoptera: Nolidae) and its implications for the phylogenetic relationships of Noctuoidea species. International Journal of Biological Macromolecules, 137: 317–326, doi: https://doi.org/10.1016/j.ijbiomac.2019.06.238
Zhang Zhiqiang. 2011. Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148: 1–237, doi: https://doi.org/10.11646/zootaxa.3148.1.1
Zhang Dong, Gao Fangluan, Jakovlić I, et al. 2020a. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20(1): 348–355, doi: https://doi.org/10.1111/1755-0998.13096
Zhang Bo, Wu Yingying, Wang **n, et al. 2020b. 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, doi: https://doi.org/10.1007/s00343-019-8364-x
Zhang Zhan, **ng Yuhui, Cheng Jiajia, et al. 2020c. Phylogenetic implications of mitogenome rearrangements in East Asian potamiscine freshwater crabs (Brachyura: Potamidae). Molecular Phylogenetics and Evolution, 143: 106669, doi: https://doi.org/10.1016/j.ympev.2019.106669
Zhao Ling, Zheng Zheming, Huang Yuan, et al. 2011. Comparative analysis of the mitochondrial control region in Orthoptera. Zoological Studies, 50(3): 385–393
Zhuang Xuan, Cheng C H C. 2010. ND6 gene “lost” and found: evolution of mitochondrial gene rearrangement in Antarctic notothenioids. Molecular Biology and Evolution, 27(6): 1391–1403, doi: https://doi.org/10.1093/molbev/msq026
Author information
Authors and Affiliations
Corresponding author
Additional information
Foundation item: The National Natural Science Foundation of China under contract No. 41706176; the Basic Scientific Research Operating Expenses of Zhejiang Provincial Universities under contract No. 2019J00022.
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Zhang, Y., Meng, L., Wei, L. et al. Comparative mitochondrial genome analysis of Sesarmidae and its phylogenetic implications. Acta Oceanol. Sin. 41, 62–73 (2022). https://doi.org/10.1007/s13131-021-1911-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13131-021-1911-2