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Comparative analysis of mitochondrial genome of a deep-sea crab Chaceon granulates reveals positive selection and novel genetic features

  • Biology
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Abstract

Deep-sea organisms survive in an extremely harsh environment. There must be some genetic adaptation mechanisms for them. We systematically characterized and compared the complete mitochondrial genome (mitogenome) of a deep-sea crab (Chaceon granulates) with those of shallow crabs. The mitogenome of the crab was 16 126 bp in length, and encoded 37 genes as most of a metazoan mitogenome, including 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, and 2 ribosomal RNA (rRNA) genes. The gene arrangement and orientation was conserved in the crabs. However, a unique mitogenome element regulator, the origin of light-strand replication (OL), was firstly predicted in the present crab mitogenome. In addition, further positive selection analysis showed that two residues (33S in ND3 and 502I in ND5) in C. granulates mitogenome were positively selected, indicated the selective evolution of the deep-sea crab. Therefore, the mitogenome of deep-sea C. granulates showed a unique OL element and positive selection. These special features would influence the mitochondrial energy metabolism, and be involved in the adaptation of deep-sea environment, such as oxygen deficits and low temperatures.

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Data Availability Statement

The authors declare that all data supporting the findings of this study are available within the article and its supplementary files.

References

  • Bernt M, Braband A, Schierwater B, Stadler P F. 2013. Genetic aspects of mitochondrial genome evolution. Molecular Phylogenetics and Evolution, 69(2): 328–338.

    Google Scholar 

  • Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1 767–1 780.

    Google Scholar 

  • Boore J L. 2001. Complete mitochondrial genome sequence of the polychaete annelid Platynereis dumerilii. Molecular Biology and Evolution, 18(7): 1 413–1 416.

    Google Scholar 

  • Burkenroad M D. 1981. The higher taxonomy and evolution of Decapoda (Crustacea). Transactions of the San Diego Society of Natural History, 19(17): 251–268.

    Google Scholar 

  • Clayton D A. 1991. Replication and transcription of vertebrate mitochondrial-DNA. Annual Review of Cell Biology, 7(1): 453–478.

    Google Scholar 

  • Coscia I, Castilho R, Massa-Gallucci A, Sacchi C, Cunha R L, Stefanni S, Helyar S J, Knutsen H, Mariani S. 2018. Genetic homogeneity in the deep-sea grenadier Macrourus berglax across the North Atlantic Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 132: 60–67.

    Google Scholar 

  • Da Fonseca R R, Johnson W E, O’Brien S J, Ramos M J, Antunes A. 2008. The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics, 9: 119.

    Google Scholar 

  • Etter R J, Rex M A, Chase M C, Quattro J M. 1999. A genetic dimension to deep-sea biodiversity. Deep Sea Research Part I: Oceanographic Research Papers, 46(6): 1 095–1 099.

    Google Scholar 

  • Fernández-Silva P, Enriquez J A, Montoya J. 2003. Replication and transcription of mammalian mitochondrial DNA. Experimental Physiology, 88(1): 41–56.

    Google Scholar 

  • Flot J F, Tillier S. 2007. The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: The putative D-loop and a novel ORF of unknown function. Gene, 401(1–2): 80–87.

    Google Scholar 

  • Green D R, Reed J C. 1998. Mitochondria and apoptosis. Science, 281(5381): 1 309–1 312.

    Google Scholar 

  • Gu M L, Dong X Q, Shi L, Shi L, Lin K Q, Huang X Q, Chu J Y. 2012. Differences in mtDNA whole sequence between Tibetan and Han populations suggesting adaptive selection to high altitude. Gene, 496(1): 37–44.

    Google Scholar 

  • Guo X H, Liu S J, Liu Y. 2003. Comparative analysis of the mitochondrial DNA control region in cyprinids with different ploidy level. Aquaculture, 224(1–4): 25–38.

    Google Scholar 

  • Hassanin A, Léger N, Deutsch J. 2005. Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of metazoa, and consequences for phylogenetic inferences. Systematic Biology, 54(2): 277–298.

    Google Scholar 

  • Hassanin A, Ropiquet A, Couloux A, Cruaud C. 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.

    Google Scholar 

  • Hui M, Cheng J, Sha Z L. 2018. Adaptation to the deep-sea hydrothermal vents and cold seeps: Insights from the transcriptomes of Alvinocaris longirostris in both environments. Deep Sea Research Part I: Oceanographic Research Papers, 135: 23–33.

    Google Scholar 

  • Jacobsen M W, Da Fonseca R R, Bernatchez L, Hansen M M. 2016. Comparative analysis of complete mitochondrial genomes suggests that relaxed purifying selection is driving high nonsynonymous evolutionary rate of the NADH2 gene in whitefish (Coregonus ssp.). Molecular Phylogenetics and Evolution, 95: 161–170.

    Google Scholar 

  • Jebbar M, Franzetti B, Girard E, Oger P. 2015. Microbial diversity and adaptation to high hydrostatic pressure in deep-sea hydrothermal vents prokaryotes. Extremophiles, 19(4): 721–740.

    Google Scholar 

  • Jiang L C, Wang G C, Tan S, Gong S A, Yang M, Peng Q K, Peng R, Zou F D. 2013. The complete mitochondrial genome sequence analysis of Tibetan argali (Ovis ammon hodgsoni): implications of Tibetan argali and Gansu argali as the same subspecies. Gene, 521(1): 24–31.

    Google Scholar 

  • Jin X X, Wang R X, Wei T, Tang D, Xu T J. 2015. Complete mitochondrial genome sequence of Tridentiger bifasciatus and Tr dent ger barbatus (Perciformes, Gobiidae): a mitogenomic perspective on the phylogenetic relationships of Gobiidae. Molecular BiologyReports, 42(1): 253–265.

    Google Scholar 

  • Kawaguchi A, Miya M, Nishida M. 2001. Complete mitochondrial DNA sequence of Aulopus japonicus (Teleostei: Aulopiformes), a basal Eurypterygii: longer DNA sequences and higher-level relationships. Ichthyological Research, 48(3): 213–223.

    Google Scholar 

  • 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): 13 738–13 742.

    Google Scholar 

  • Liao F, Wang L, Wu S, Li Y P, Zhao L, Huang G M, Niu C J, Liu Y Q, Li M G. 2010. The complete mitochondrial genome of the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae). International Journal of Biological Sciences, 6(2): 172–186.

    Google Scholar 

  • Liao Y Y, Mo G D, Sun J L, Wei F Y, Liao D J. 2016. Genetic diversity of Guangxi chicken breeds assessed with microsatellites and the mitochondrial DNA D-loop region. Molecular Biology Reports, 43(5): 415–425.

    Google Scholar 

  • Liu Y, Cui Z X. 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 BiologyReports, 37(5): 2 559–2 569.

    Google Scholar 

  • Lowe T M, Eddy S R. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25(5): 955–964.

    Google Scholar 

  • Luo Y J, Gao W X, Gao Y Q, Tang S, Huang Q Y, Tan X L, Chen J, Huang T S. 2008. Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation. Mitochondrion, 8(5–6): 352–357.

    Google Scholar 

  • Ma H Y, Ma C Y, Li C H, Lu J X, Zou X, Gong Y Y, Wang W, Chen W, Ma L B, Xia L J. 2015. First mitochondrial genome for the red crab (Charybdis feriata) with implication of phylogenomics and population genetics. Scientific Reports, 5: 11 524.

    Google Scholar 

  • Ma H Y, Ma C Y, Li X C, Xu Z, Feng N N, Ma L B. 2013. The complete mitochondrial genome sequence and gene organization of the mud crab (Scylla paramamosain) with phylogenetic consideration. Gene, 519(1): 120–127.

    Google Scholar 

  • Marshall H D, Baker A J. 1997. Structural conservation and variation in the mitochondrial control region of fringilline finches (Fringilla spp.) and the greenfinch (Carduelis chloris). Molecular Biology and Evolution, 14(2): 173–184.

    Google Scholar 

  • Miller A D, Murphy N P, Burridge C P, Austin C M. 2005. Complete mitochondrial DNA sequences of the decapod crustaceans Pseudocarcinus gigas (Menippidae) and Macrobrachium rosenbergii (Palaemonidae). Marine Biotechnology, 7(4): 339–349.

    Google Scholar 

  • Newmeyer D D, Ferguson-Miller S. 2003. Mitochondria: releasing power for life and unleashing the machineries of death. Cell, 112(4): 481–490.

    Google Scholar 

  • Ning T, Xiao H, Li J, Hua S, Zhang Y P. 2010. Adaptive evolution of the mitochondrial ND6 gene in the domestic horse. Genetics and Molecular Research, 9(1): 144–150.

    Google Scholar 

  • Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature, 290(5806): 470–474.

    Google Scholar 

  • 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.

    Google Scholar 

  • Posada D, Crandall K A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14(9): 817–818.

    Google Scholar 

  • Rex M A. 1981. Community structure in the deep-sea Benthos. Annual Review of Ecology and Systematics, 12(1): 331–353.

    Google Scholar 

  • Sanders H L, Hessler R R. 1969. Ecology of the deep-sea benthos. Science, 163(3874): 1 419–1 424.

    Google Scholar 

  • Sbisa E, Tanzariello F, Reyes A, Pesole G, Saccone C. 1997. Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene, 205(1–2): 125–140.

    Google Scholar 

  • Shen X, Ren J F, Cui Z X, Sha Z L, Wang B, Xiang J H, Liu B. 2007. The complete mitochondrial genomes of two common shrimps (Litopenaeus vannamei and Fenneropenaeus chinensis) and their phylogenomic considerations. Gene, 403(1–2): 98–109.

    Google Scholar 

  • Sogin M L, Morrison H G, Huber J A, Welch D M, Huse S M, Neal P R, Arrieta J M, Herndl G J. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America, 103(32): 12 115–12 120.

    Google Scholar 

  • Sun S E, Hui M, Wang M X, Sha Z L. 2018. The complete mitochondrial genome of the alvinocaridid shrimp Shinkaicaris leurokolos (Decapoda, Caridea): insight into the mitochondrial genetic basis of deep-sea hydrothermal vent adaptation in the shrimp. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 25: 42–52.

    Google Scholar 

  • Tang B P, Liu Y, Xin Z Z, Zhang D Z, Wang Z F, Zhu X Y, Wang Y, Zhang H B, Zhou C L, Chai X Y, Liu Q N. 2017. Characterisation of the complete mitochondrial genome of Helice wuana (Grapsoidea: Varunidae) and comparison with other Brachyuran crabs. Genomics, 110(4): 221–230.

    Google Scholar 

  • Tsang L M, Ma K Y, Ahyong S T, Chan T Y, Chu K H. 2008. Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Molecular Phylogenetics and Evolution, 48(1): 359–368.

    Google Scholar 

  • Umetsu K, Iwabuchi N, Yuasa I, Saitou N, Clark P F, Boxshall G, Osawa M, Igarashi K. 2002. Complete mitochondrial DNA sequence of a tadpole shrimp (Triops cancriformis) and analysis of museum samples. Electrophoresis, 23(24): 4 080–4 084.

    Google Scholar 

  • Valverde J R, Batuecas B, Moratilla C, Marco R, Garesse R. 1994. The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. Journal of Molecular Evolution, 39: (4).

    Google Scholar 

  • Wang Z L, Li C, Fang W Y, Yu X P. 2016. 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.

    Google Scholar 

  • Yamauchi M M, Miya M U, Nishida M. 2003. Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura). Gene, 311: 129–135.

    Google Scholar 

  • Yu L, Wang X P, Ting N, Zhang Y P. 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.

    Google Scholar 

  • Zhang B, Zhang Y H, Wang X, Zhang H X, Lin Q. 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): 4 951–4 962.

    Google Scholar 

  • Zhang D X, Szymura J M, Hewitt G M. 1995. Evolution and structural conservation of the control region of insect mitochondrial DNA. Journal of Molecular Evolution, 40(4): 382–391.

    Google Scholar 

  • Zhang Q L, Zhang L, Zhao T X, Wang J, Zhu Q H, Chen J Y, Yuan M L. 2017b. Gene sequence variations and expression patterns of mitochondrial genes are associated with the adaptive evolution of two Gynaephora species (Lepidoptera: Lymantriinae) living in different high-elevation environments. Gene, 610: 148–155.

    Google Scholar 

  • Zhang Y, Li X G, Bartlett D H, Xiao X. 2015. Current developments in marine microbiology: high-pressure biotechnology and the genetic engineering of piezophiles. Current Opinion in Biotechnology, 33: 157–164.

    Google Scholar 

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Author information

Author notes

  1. ZHANG Bo and WU Yingying contributed equally to this work and should be regarded as co-first authors.

Authors and Affiliations

  1. Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510275, China

    Bo Zhang, Yingying Wu, Xin Wang, Jianping Yin & Qiang Lin

  2. Institution of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences, Guangzhou, 510275, China

    Bo Zhang, Xin Wang, Jianping Yin & Qiang Lin

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Bo Zhang & Yingying Wu

  4. Beijing Advanced Sciences and Innovation Center of Chinese Academy of Sciences, Beijing, 100049, China

    Yingying Wu

  5. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Wei Jiang

Authors
  1. Bo Zhang
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  2. Yingying Wu
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  4. Wei Jiang
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Corresponding author

Correspondence to Qiang Lin.

Additional information

Supported by the Strategic Priority Research Program of Chinese Academy of Sciences (Nos. XDA13020103, XDA19060301), the National Science & Technology Fundamental Resources Investigation Program of China (No. 2018FY100106), and the National Key Research and Development Program “Marine Environment Security Project” (Nos. 2017YFC0506302, 2018YFC1406503)

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Comparative analysis of mitochondrial genome of a deep-sea crab Chaceon granulates reveals positive selection and novel genetic features

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Zhang, B., Wu, Y., Wang, X. et al. Comparative analysis of mitochondrial genome of a deep-sea crab Chaceon granulates reveals positive selection and novel genetic features. J. Ocean. Limnol. 38, 427–437 (2020). https://doi.org/10.1007/s00343-019-8364-x

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