Volume 41 Issue 6
Jun.  2022
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Ying Zhang, Li Gong, Xinting Lu, Zengliang Miao, Lihua Jiang, Bingjian Liu, Liqin Liu, Pengfei Li, Xu Zhang, Zhenming Lü. Comparative mitochondrial genome analysis of Varunidae and its phylogenetic implications[J]. Acta Oceanologica Sinica, 2022, 41(6): 119-131. doi: 10.1007/s13131-021-1927-7
Citation: Ying Zhang, Li Gong, Xinting Lu, Zengliang Miao, Lihua Jiang, Bingjian Liu, Liqin Liu, Pengfei Li, Xu Zhang, Zhenming Lü. Comparative mitochondrial genome analysis of Varunidae and its phylogenetic implications[J]. Acta Oceanologica Sinica, 2022, 41(6): 119-131. doi: 10.1007/s13131-021-1927-7

Comparative mitochondrial genome analysis of Varunidae and its phylogenetic implications

doi: 10.1007/s13131-021-1927-7
Funds:  The Natural Science Foundation of Zhejiang Province under contract No. LY21C190007.
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  • Corresponding author: nblzmnb@163.com
  • Received Date: 2021-02-07
  • Accepted Date: 2021-03-29
  • Available Online: 2022-03-16
  • Publish Date: 2022-06-16
  • Complete mitochondrial genomes (mitogenomes) can indicate phylogenetic relationships, as well as useful information for gene rearrangement mechanisms and molecular evolution. Currently, the phylogenetic location of the genus Varuna (Brachyura: Varunidae) has not been well resolved mainly because of limited representatives (only two extant species). Here, we determined a new mitogenome of this genus (Varuna litterata) and added the published mitogenomes to reconstruct the phylogeny of Varunidae. The 16 368-bp mitogenome contains the entire set of 37 genes and a putative control region. The characteristics of this newly sequenced mitogenome were described and compared with the other 15 Varunidae mitogenomes. All 16 analyzed mitogenomes have identical gene order and similar molecular features. The sliding window and genetic distance analyses demonstrate highly variable nucleotide diversity, with comparatively low variability of COI and COII, and high variability of ND6. The nonsynonymous/synonymous substitution rates (dN/dS ratio) analysis shows that all 13 PCGs are under purifying selection and ATP8 gene evolves under the least selective pressure. Twelve tRNA genes, two rRNAs, one PCG, and the putative control region are found to be rearranged with respect to the pancrustacean ground pattern gene order. Tandem duplication/random loss model is adopted to explain the large-scale gene rearrangement events occurring in Varunidae mitogenomes. Phylogenetic analyses show that all Varunidae species are placed into one group, and form a sister clade with Macrophthalmidae. Nevertheless, the phylogenetic relationships within Varunidae are not completely consistent based on the two different datasets used in this study. These findings will contribute to a better understanding of gene rearrangement and molecular evolution in Varunidae mitogenomes, as well as provide insights into the phylogenetic studies of Brachyura.
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  • [1]
    Alcock A W. 1900. Materials for a carcinological fauna of India. No. 6: The Brachyura Catometopa or Grapsoidea. Journal of the Asiatic Society of Bengal, 69(3): 279–456
    [2]
    Arndt A, Smith M J. 1998. Mitochondrial gene rearrangement in the sea cucumber genus Cucumaria. Molecular Biology and Evolution, 15(8): 1009–1016. doi: 10.1093/oxfordjournals.molbev.a025999
    [3]
    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: 10.1038/s41598-017-04168-9
    [4]
    Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27(2): 573–580. doi: 10.1093/nar/27.2.573
    [5]
    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: 10.1016/j.ympev.2012.08.023
    [6]
    Bernt M, Merkle D, Ramsch K, et al. 2007. CREx: inferring genomic rearrangements based on common intervals. Bioinformatics, 23(21): 2957–2958. doi: 10.1093/bioinformatics/btm468
    [7]
    Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767–1780. doi: 10.1093/nar/27.8.1767
    [8]
    Boore J L, Lavrov D V, Brown W M. 1998. Gene translocation links insects and crustaceans. Nature, 392(6677): 667–668. doi: 10.1038/33577
    [9]
    Camargo T R, Wolf M R, Mantelatto F L, et al. 2020. Ultrastructure of spermatozoa of members of Calappidae, Aethridae and Menippidae and discussion of their phylogenetic placement. Acta Zoologica, 101(1): 89–100. doi: 10.1111/azo.12273
    [10]
    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: 10.1038/329853a0
    [11]
    Chen Jianqin, Xing 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: 10.1016/j.gene.2018.06.088
    [12]
    Chen Jianqin, Xing Yuhui, Yao Wenjia, et al. 2019. Phylomitogenomics reconfirm the phylogenetic position of the genus Metaplax inferred from the two grapsid crabs (Decapoda: Brachyura: Grapsoidea). PLoS ONE, 14(1): e0210763. doi: 10.1371/journal.pone.0210763
    [13]
    Dai Aiyun,Yang Siliang. 1991. Crabs of the China Seas. Beijing: China Ocean Press, 473
    [14]
    Davie P J F, Guinot D, Ng P K L. 2015. Systematics and classification of Brachyura. In: Castro P, et al. eds. Treatise on Zoology Antomy, Taxonomy, Biology. Decapoda: The Crustacea. Leiden: Koninklijke Brill NV, 1049–1130
    [15]
    Dierckxsens N, Mardulyn P, Smits G. 2017. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research, 45(4): e18
    [16]
    Gong Li, Liu Bingjian, Liu Liqin, et al. 2019. The complete mitochondrial genome of Terapon jarbua (Centrarchiformes: Terapontidae) and comparative analysis of the control region among eight Centrarchiformes species. Russian Journal of Marine Biology, 45(2): 137–144. doi: 10.1134/S1063074019020068
    [17]
    Gong Li, Lu Xinting, Wang Zhifu, et al. 2020. Novel gene rearrangement in the mitochondrial genome of Coenobita brevimanus (Anomura: Coenobitidae) and phylogenetic implications for Anomura. Genomics, 112(2): 1804–1812. doi: 10.1016/j.ygeno.2019.10.012
    [18]
    Gyllensten U, Wharton D, Josefsson A, et al. 1991. Paternal inheritance of mitochondrial DNA in mice. Nature, 352(6332): 255–257. doi: 10.1038/352255a0
    [19]
    Jacobs H T, Herbert E R, Rankine J. 1989. Sea urchin egg mitochondrial DNA contains a short displacement loop (D-loop) in the replication origin region. Nucleic Acids Research, 17(22): 8949–8965. doi: 10.1093/nar/17.22.8949
    [20]
    Jamieson B G M, Guinot D, De Forges B R. 1996. Contrasting spermatozoal ultrastructure in two thoracotreme crabs, Cardisoma carnifex (Gecarcinidae) and Varunu litterata (Grapsidae) (Crustacea: Brachyura). Invertebrate Reproduction & Development, 29(2): 111–126
    [21]
    Kalyaanamoorthy S, Minh B Q, Wong T K F, et al. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587–589. doi: 10.1038/nmeth.4285
    [22]
    Katoh K, Misawa K, Kuma K I, et al. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14): 3059–3066. doi: 10.1093/nar/gkf436
    [23]
    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: 10.1093/molbev/msy096
    [24]
    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: 10.1093/oxfordjournals.molbev.a004068
    [25]
    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. doi: 10.1073/pnas.250402997
    [26]
    Li Ning, Hu Guilin, Hua Baozhen. 2019. Complete mitochondrial genomes of Bittacus strigosus and Panorpa debilis and genomic comparisons of Mecoptera. International journal of biological macromolecules, 140: 672–681. doi: 10.1016/j.ijbiomac.2019.08.152
    [27]
    Li Kui, Liang Aiping. 2018. Hemiptera mitochondrial control region: new sights into the structural organization, phylogenetic utility, and roles of tandem repetitions of the noncoding segment. International Journal of Molecular Sciences, 19(5): 1292. doi: 10.3390/ijms19051292
    [28]
    Li Yuetian, Xin Zhaozhe, Tang Yingyu, et al. 2020. Comparative mitochondrial genome analyses of sesarmid and other brachyuran crabs reveal gene rearrangements and phylogeny. Frontiers in Genetics, 11: 536640. doi: 10.3389/fgene.2020.536640
    [29]
    Lin Fan, Xie Zhuofan, Fazhan H, et al. 2018. The complete mitochondrial genome of Varuna yui (Decapoda: Brachyura: Varunidae) and its phylogeny. Mitochondrial DNA Part B, 3(1): 263–264. doi: 10.1080/23802359.2018.1443043
    [30]
    Liu Yuan, Cui Zhaoxia. 2010. Complete mitochondrial genome of the Asian paddle crab Charybdis japonica (Crustacea: Decapoda: Portunidae): gene rearrangement of the marine brachyurans and phylogenetic considerations of the decapods. Molecular Biology Reports, 37(5): 2559–2569. doi: 10.1007/s11033-009-9773-2
    [31]
    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: 10.1093/nar/gkw413
    [32]
    Lu Xinting, Gong Li, Zhang Ying, et al. 2020. The complete mitochondrial genome of Calappa bilineata: the first representative from the family Calappidae and its phylogenetic position within Brachyura. Genomics, 112(3): 2516–2523. doi: 10.1016/j.ygeno.2020.02.003
    [33]
    Lunt D H, Hyman B C. 1997. Animal mitochondrial DNA recombination. Nature, 387(6630): 247. doi: 10.1038/387247a0
    [34]
    Ma Kayan, Qin Jing, 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: 10.1016/j.ympev.2019.02.001
    [35]
    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: 10.3390/ijms161025031
    [36]
    Martin J W, Davis G E. 2001. An updated classification of the recent Crustacea. In: Heyning J, Harris M J, Brown V B, eds. Natural History Museum of Los Angeles County: Science Series 39, 1–124
    [37]
    Masta S E, Boore J L. 2004. The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Molecular Biology and Evolution, 21(5): 893–902. doi: 10.1093/molbev/msh096
    [38]
    Moritz C, Brown W M. 1987. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proceedings of the National Academy of Sciences of the United States of America, 84(20): 7183–7187. doi: 10.1073/pnas.84.20.7183
    [39]
    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: 10.1146/annurev.es.18.110187.001413
    [40]
    Muse S V. 2000. Examining rates and patterns of nucleotide substitution in plants. Plant Molecular Biology, 42(1): 25–43. doi: 10.1023/A:1006319803002
    [41]
    Ng N K. 2006. The Systematics of the Crabs of the Family Varunidae (Brachyura, Decapoda). Singapore: National University of Singapore
    [42]
    Ng P K L, Guinot D, Davie P J F. 2008. Systema brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology, 17: 1–286
    [43]
    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: 10.1093/molbev/msu300
    [44]
    Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature, 290(5806): 470–474. doi: 10.1038/290470a0
    [45]
    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: 10.1007/BF01215182
    [46]
    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: 10.1093/sysbio/sys029
    [47]
    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: 10.1093/molbev/msx248
    [48]
    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: 10.1016/j.fishres.2015.11.005
    [49]
    Sato M, Sato K. 2013. Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochimica et Biophysica Acta-Molecular Cell Research, 1833(8): 1979–1984. doi: 10.1016/j.bbamcr.2013.03.010
    [50]
    Schubart C D, Cuesta J A, Diesel R, et al. 2000. Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution, 15(2): 179–190. doi: 10.1006/mpev.1999.0754
    [51]
    Schubart C D, Cuesta J A, Felder D L. 2002. Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea. Journal of Crustacean Biology, 22(1): 28–44. doi: 10.1163/20021975-99990206
    [52]
    Stothard P, Wishart D S. 2005. Circular genome visualization and exploration using CGView. Bioinformatics, 21(4): 537–539. doi: 10.1093/bioinformatics/bti054
    [53]
    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: 10.1080/10635150701472164
    [54]
    Tan Munhua, Gan Hanming, Lee Yinpeng, 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: 10.1016/j.ympev.2018.05.015
    [55]
    Tan Munhua, Gan Hanming, Lee Yinpeng, et al. 2019. Comparative mitogenomics of the Decapoda reveals evolutionary heterogeneity in architecture and composition. Scientific Reports, 9(1): 10756. doi: 10.1038/s41598-019-47145-0
    [56]
    Tang Boping, Liu Yu, Xin Zhaozhe, et al. 2018. Characterisation of the complete mitochondrial genome of Helice wuana (Grapsoidea: Varunidae) and comparison with other Brachyuran crabs. Genomics, 110(4): 221–230. doi: 10.1016/j.ygeno.2017.10.001
    [57]
    Tu Chin-Hung. 1992. Studies on the larval culture of Varuna litterata [dissertation]. Kaohsiung, China: National Sun Yat-Sen University
    [58]
    Wang Xiaoyan, Huang Yuan, Liu Nian, et al. 2015. Seven complete mitochondrial genome sequences of bushtits (Passeriformes, Aegithalidae, Aegithalos): the evolution pattern in duplicated control regions. Mitochondrial DNA, 26(3): 350–356. doi: 10.3109/19401736.2014.1003821
    [59]
    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: 10.1016/j.ygeno.2018.05.002
    [60]
    Wang Qi, Tang Dan, Guo Huayun, et al. 2020. Comparative mitochondrial genomic analysis of Macrophthalmus pacificus and insights into the phylogeny of the Ocypodoidea & Grapsoidea. Genomics, 112(1): 82–91. doi: 10.1016/j.ygeno.2019.12.012
    [61]
    Xin Zhaozhe, Liu Yu, Zhang Daizhen, et al. 2017. Mitochondrial genome of Helice tientsinensis (Brachyura: Grapsoidea: Varunidae): gene rearrangements and higher-level phylogeny of the Brachyura. Gene, 627: 307–314. doi: 10.1016/j.gene.2017.06.036
    [62]
    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: 10.1111/1755-0998.13096
    [63]
    Zhang Bo, Wu Yingying, Wang Xin, 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: 10.1007/s00343-019-8364-x
    [64]
    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: 10.1093/molbev/msq026
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