Volume 45 Issue 1
Jan.  2024
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Zhan-Fei Wei, Kai-Wen Ta, Nan-Nan Zhang, Shan-Shan Liu, Liang Meng, Kai-Qiang Liu, Chong-Yang Cai, Xiao-Tong Peng, Chang-Wei Shao. Molecular phylogenetic relationships based on mitochondrial genomes of novel deep-sea corals (Octocorallia: Alcyonacea): Insights into slow evolution and adaptation to extreme deep-sea environments. Zoological Research, 2024, 45(1): 215-225. doi: 10.24272/j.issn.2095-8137.2023.039
Citation: Zhan-Fei Wei, Kai-Wen Ta, Nan-Nan Zhang, Shan-Shan Liu, Liang Meng, Kai-Qiang Liu, Chong-Yang Cai, Xiao-Tong Peng, Chang-Wei Shao. Molecular phylogenetic relationships based on mitochondrial genomes of novel deep-sea corals (Octocorallia: Alcyonacea): Insights into slow evolution and adaptation to extreme deep-sea environments. Zoological Research, 2024, 45(1): 215-225. doi: 10.24272/j.issn.2095-8137.2023.039

Molecular phylogenetic relationships based on mitochondrial genomes of novel deep-sea corals (Octocorallia: Alcyonacea): Insights into slow evolution and adaptation to extreme deep-sea environments

doi: 10.24272/j.issn.2095-8137.2023.039
The raw data and mitochondrial genomes in this study were submitted to NCBI (PRJNA951866), Science Data Bank (10.57760/sciencedb.j00139.00051), and GSA (PRJCA016049).
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
The project was conceived by S.S.L., X.T.P., and C.W.S.. Sample collection, DNA extraction, and DNA library preparation were carried out by N.N.Z., C.Y.C. and L.M. Morphological examination and sclerite scanning were carried out by K.W.T. Pipeline assembly, including data cleaning, genome assembly, annotation, and all downstream analyses, was carried out by Z.F.W. and K.Q.L. The manuscript was written by Z.F.W. with contributions from all authors. All authors edited the manuscript before submission. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work
Funds:  This study was supported by the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2022QNLM030004), Hainan Science and Technology Department (ZDKJ2019011), Open Project Fund of Key Laboratory of Sustainable Development of Polar Fisheries, Ministry of Agriculture and Rural Affairs of PRC (2022OPF02), State Key R&D Project (2021YFF0502500), and Qingdao Postdoctoral Applied Research Project (JZ2223j06100)
More Information
  • A total of 10 specimens of Alcyonacea corals were collected at depths ranging from 905 m to 1 633 m by the manned submersible Shenhai Yongshi during two cruises in the South China Sea (SCS). Based on mitochondrial genomic characteristics, morphological examination, and sclerite scanning electron microscopy, the samples were categorized into four suborders (Calcaxonia, Holaxonia, Scleraxonia, and Stolonifera), and identified as 9 possible new cold-water coral species. Assessments of GC-skew dissimilarity, phylogenetic distance, and average nucleotide identity (ANI) revealed a slow evolutionary rate for the octocoral mitochondrial sequences. The nonsynonymous (Ka) to synonymous (Ks) substitution ratio (Ka/Ks) suggested that the 14 protein-coding genes (PCGs) were under purifying selection, likely due to specific deep-sea environmental pressures. Correlation analysis of the median Ka/Ks values of five gene families and environmental factors indicated that the genes encoding cytochrome b (cyt b) and DNA mismatch repair protein (mutS) may be influenced by environmental factors in the context of deep-sea species formation. This study highlights the slow evolutionary pace and adaptive mechanisms of deep-sea corals.
  • The raw data and mitochondrial genomes in this study were submitted to NCBI (PRJNA951866), Science Data Bank (10.57760/sciencedb.j00139.00051), and GSA (PRJCA016049).
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    The project was conceived by S.S.L., X.T.P., and C.W.S.. Sample collection, DNA extraction, and DNA library preparation were carried out by N.N.Z., C.Y.C. and L.M. Morphological examination and sclerite scanning were carried out by K.W.T. Pipeline assembly, including data cleaning, genome assembly, annotation, and all downstream analyses, was carried out by Z.F.W. and K.Q.L. The manuscript was written by Z.F.W. with contributions from all authors. All authors edited the manuscript before submission. All authors read and approved the final version of the manuscript.
    #Authors contributed equally to this work
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  • [1]
    Andrews S. 2014. FastQC a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
    [2]
    Baillon S, Hamel JF, Wareham Hayes V, et al. 2012. Deep cold-water corals as nurseries for fish larvae. Frontiers in Ecology and the Environment, 10(7): 351−356. doi: 10.1890/120022
    [3]
    Beaton MJ, Roger AJ, Cavalier-Smith T. 1998. Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. Journal of Molecular Evolution, 47(6): 697−708. doi: 10.1007/PL00006429
    [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]
    Bilewitch JP, Degnan SM. 2011. A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function. BMC Evolutionary Biology, 11(1): 228. doi: 10.1186/1471-2148-11-228
    [6]
    Boore JL. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767−1780. doi: 10.1093/nar/27.8.1767
    [7]
    Brockman S, McFadden C. 2012. The mitochondrial genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes. Genome Biology and Evolution, 4(9): 994−1006. doi: 10.1093/gbe/evs074
    [8]
    Brugler MR, France SC. 2008. The mitochondrial genome of a deep-sea bamboo coral (Cnidaria, Anthozoa, Octocorallia, Isididae): genome structure and putative origins of replication are not conserved among octocorals. Journal of Molecular Evolution, 67(2): 125−136. doi: 10.1007/s00239-008-9116-2
    [9]
    Cairns SD. 2009. Review of octocorallia (Cnidaria: Anthozoa) from Hawai‘i and adjacent seamounts. Part 2: Genera Paracalyptrophora; Candidella; and Calyptrophora. Pacific Science, 63(3): 413–448.
    [10]
    Cairns SD. 2012. The Marine Fauna of New Zealand: New Zealand Primnoidae (Anthozoa, Alcyonacea) - Part 1. Genera Narella, Narelloides, Metanarella, Calyptrophora, and Helicoprimnoa. Wellington: NIWA.
    [11]
    Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25(15): 1972−1973. doi: 10.1093/bioinformatics/btp348
    [12]
    Carapelli A, Fanciulli P P, Frati F, et al. 2019. Mitogenomic data to study the taxonomy of Antarctic springtail species (Hexapoda: Collembola) and their adaptation to extreme environments. Polar Biology, 42(4): 715−732. doi: 10.1007/s00300-019-02466-8
    [13]
    Chen SF, Zhou YQ, Chen Y, et al. 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884−i890. doi: 10.1093/bioinformatics/bty560
    [14]
    Donath A, Jühling F, Al-Arab M, et al. 2019. Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes. Nucleic Acids Research, 47(20): 10543−10552. doi: 10.1093/nar/gkz833
    [15]
    Fryer P, Wheat CG, Williams T, et al. 2020. Mariana serpentinite mud volcanism exhumes subducted seamount materials: implications for the origin of life. Philosophical Transactions of the Royal Society A:Mathematical, Physical and Engineering Sciences, 378(2165): 20180425. doi: 10.1098/rsta.2018.0425
    [16]
    Gao H, Kong J. 2005. Distribution characteristics and biological function of tandem repeat sequences in the genomes of different organisms. Zoological Research, 26(5): 555−564. (in Chinese)
    [17]
    Greiner S, Lehwark P, Bock R. 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3. 1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research, 47(W1): W59−W64. doi: 10.1093/nar/gkz238
    [18]
    Hebbeln D, Wienberg C, Dullo WC, et al. 2020. Cold-water coral reefs thriving under hypoxia. Coral Reefs, 39(4): 853−859. doi: 10.1007/s00338-020-01934-6
    [19]
    Heestand Saucier E, France SC, Watling L. 2021. Toward a revision of the bamboo corals: part 3, deconstructing the Family Isididae. Zootaxa, 5047(3): 247−272. doi: 10.11646/zootaxa.5047.3.2
    [20]
    Hellberg ME. 2006. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology, 6: 24. doi: 10.1186/1471-2148-6-24
    [21]
    Horvath EA. 2019. A review of gorgonian coral species (Cnidaria, Octocorallia, Alcyonacea) held in the Santa Barbara Museum of Natural History research collection: focus on species from Scleraxonia, Holaxonia, and Calcaxonia - Part I: introduction, species of Scleraxonia and Holaxonia (Family Acanthogorgiidae). ZooKeys, 860: 1−66. doi: 10.3897/zookeys.860.19961
    [22]
    Hsieh HM, Chiang HL, Tsai LC, et al. 2001. Cytochrome b gene for species identification of the conservation animals. Forensic Science International, 122(1): 7−18. doi: 10.1016/S0379-0738(01)00403-0
    [23]
    Katoh K, Toh H. 2010. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics, 26(15): 1899−1900. doi: 10.1093/bioinformatics/btq224
    [24]
    Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nature Medicine, 6(5): 513−519. doi: 10.1038/74994
    [25]
    Kumar V, Tyagi K, Chakraborty R, et al. 2020. The complete mitochondrial genome of endemic giant tarantula, Lyrognathus crotalus (Araneae: Theraphosidae) and comparative analysis. Scientific Reports, 10(1): 74. doi: 10.1038/s41598-019-57065-8
    [26]
    Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    [27]
    Li DH, Liu CM, Luo RB, et al. 2014. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31(10): 1674−1676.
    [28]
    Li F, Lv YY, Wen ZY, et al. 2021. The complete mitochondrial genome of the intertidal spider (Desis jiaxiangi) provides novel insights into the adaptive evolution of the mitogenome and the evolution of spiders. BMC Ecology and Evolution, 21(1): 72. doi: 10.1186/s12862-021-01803-y
    [29]
    Li JR, Wang PX. 2019. Discovery of deep-water bamboo coral forest in the South China Sea. Scientific Reports, 9(1): 15453. doi: 10.1038/s41598-019-51797-3
    [30]
    Li Y, Zhan ZF, Xu KD. 2020. Morphology and molecular phylogenetic analysis of deep-sea purple gorgonians (Octocorallia: Victorgorgiidae) from seamounts in the Tropical Western Pacific, with description of three new species. Frontiers in Marine Science, 7: 701. doi: 10.3389/fmars.2020.00701
    [31]
    Lowe TM, Chan PP. 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]
    Lv YY, Li YP, Ruan ZQ, et al. 2018. The complete mitochondrial genome of Glyptothorax macromaculatus provides a well-resolved molecular phylogeny of the Chinese sisorid catfishes. Genes, 9(6): 282. doi: 10.3390/genes9060282
    [33]
    McFadden CS, France SC, Sánchez JA, et al. 2006. A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Molecular Phylogenetics and Evolution, 41(3): 513−527. doi: 10.1016/j.ympev.2006.06.010
    [34]
    McFadden CS, Sánchez JA, France SC. 2010. Molecular phylogenetic insights into the evolution of octocorallia: a review. Integrative and Comparative Biology, 50(3): 389−410. doi: 10.1093/icb/icq056
    [35]
    Moore KM, Alderslade P, Miller KJ. 2017. A taxonomic revision of Anthothela (Octocorallia: Scleraxonia: Anthothelidae) and related genera, with the addition of new taxa, using morphological and molecular data. Zootaxa, 4304(1): 1.
    [36]
    Mueller RL, Boore JL. 2005. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Molecular Biology and Evolution, 22(10): 2104−2112. doi: 10.1093/molbev/msi204
    [37]
    Muthye V, Mackereth CD, Stewart JB, et al. 2022. Large dataset of octocoral mitochondrial genomes provides new insights into mt-mutS evolution and function. DNA Repair, 110: 103273. doi: 10.1016/j.dnarep.2022.103273
    [38]
    Nguyen LT, Schmidt HA, 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
    [39]
    Nielsen R. 2005. Molecular signatures of natural selection. Annual Review of Genetics, 39: 197−218. doi: 10.1146/annurev.genet.39.073003.112420
    [40]
    Niu WT, Xiao JG, Tian P, et al. 2020. Characterization of the complete mitochondrial genome sequences of three Merulinidae corals and novel insights into the phylogenetics. PeerJ, 8: e8455. doi: 10.7717/peerj.8455
    [41]
    Noll D, Leon F, Brandt D, et al. 2022. Positive selection over the mitochondrial genome and its role in the diversification of gentoo penguins in response to adaptation in isolation. Scientific Reports, 12(1): 3767. doi: 10.1038/s41598-022-07562-0
    [42]
    Nurk S, Bankevich A, Antipov D, et al. 2013. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. Journal of Computational Biology, 20(10): 714−737. doi: 10.1089/cmb.2013.0084
    [43]
    Ogata H, Ray J, Toyoda K, et al. 2011. Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment. The ISME Journal, 5(7): 1143−1151. doi: 10.1038/ismej.2010.210
    [44]
    Park E, Hwang DS, Lee JS, et al. 2012. Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Molecular Phylogenetics and Evolution, 62(1): 329−345. doi: 10.1016/j.ympev.2011.10.008
    [45]
    Richter M, Rosselló-Móra R, Oliver Glöckner F, et al. 2016. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics, 32(6): 929−931. doi: 10.1093/bioinformatics/btv681
    [46]
    Roberts JM, Wheeler AJ, Freiwald A. 2006. Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science, 312(5773): 543−547. doi: 10.1126/science.1119861
    [47]
    Sánchez JA. 2005. Systematics of the bubblegum corals (Cnidaria: Octocorallia: Paragorgiidae) with description of new species from New Zealand and the Eastern Pacific. Zootaxa, 1014(1): 1−72. doi: 10.11646/zootaxa.1014.1.1
    [48]
    Schaack S, Ho EKH, Macrae F. 2020. Disentangling the intertwined roles of mutation, selection and drift in the mitochondrial genome. Philosophical Transactions of the Royal Society B:Biological Sciences, 375(1790): 20190173. doi: 10.1098/rstb.2019.0173
    [49]
    Shearer TL, Van Oppen MJH, Romano S, L et al. 2002. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology, 11(12): 2475−2487. doi: 10.1046/j.1365-294X.2002.01652.x
    [50]
    Shtolz N, Mishmar D. 2019. The mitochondrial genome-on selective constraints and signatures at the organism, cell, and single mitochondrion levels. Frontiers in Ecology and Evolution, 7: 342. doi: 10.3389/fevo.2019.00342
    [51]
    Small I, Maréchal-Drouard L, Masson J, et al. 1992. In vivo import of a normal or mutagenized heterologous transfer RNA into the mitochondria of transgenic plants: Towards novel ways of influencing mitochondrial gene expression?. The EMBO Journal, 11(4): 1291−1296. doi: 10.1002/j.1460-2075.1992.tb05172.x
    [52]
    Sokolova I. 2018. Mitochondrial adaptations to variable environments and their role in Animals’ stress tolerance. Integrative and Comparative Biology, 58(3): 519−531. doi: 10.1093/icb/icy017
    [53]
    Sun Z, Hamel JF, Edinger E, et al. 2010. Reproductive biology of the deep-sea octocoral Drifa glomerata in the Northwest Atlantic. Marine Biology, 157(4): 863−873. doi: 10.1007/s00227-009-1369-9
    [54]
    Taanman JW. 1999. The mitochondrial genome: structure, transcription, translation and replication. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1410(2): 103−123. doi: 10.1016/S0005-2728(98)00161-3
    [55]
    Thierens M, Browning E, Pirlet H, et al. 2013. Cold-water coral carbonate mounds as unique palaeo-archives: the plio-pleistocene challenger Mound record (NE Atlantic). Quaternary Science Reviews, 73: 14−30. doi: 10.1016/j.quascirev.2013.05.006
    [56]
    Tillich M, Lehwark P, Pellizzer T, et al. 2017. GeSeq-Versatile and accurate annotation of organelle genomes. Nucleic Acids Research, 45(W1): W6−W11. doi: 10.1093/nar/gkx391
    [57]
    Tu TH, Dai CF, Jeng MS. 2016. Taxonomic revision of Coralliidae with descriptions of new species from New Caledonia and the Hawaiian Archipelago. Marine Biology Research, 12(10): 1003−1038. doi: 10.1080/17451000.2016.1241411
    [58]
    Uda K, Komeda Y, Koyama H, et al. 2011. Complete mitochondrial genomes of two Japanese precious corals, Paracorallium japonicum and Corallium konojoi (Cnidaria, Octocorallia, Coralliidae): Notable differences in gene arrangement. Gene, 476(1-2): 27−37. doi: 10.1016/j.gene.2011.01.019
    [59]
    Van De Water JAJM, Allemand D, FerrierPagès C. 2018. Host-microbe interactions in octocoral holobionts - recent advances and perspectives. Microbiome, 6(1): 64. doi: 10.1186/s40168-018-0431-6
    [60]
    Van Der Ham JL, Brugler MR, France SC. 2009. Exploring the utility of an indel-rich, mitochondrial intergenic region as a molecular barcode for bamboo corals (Octocorallia: Isididae). Marine Genomics, 2(3-4): 183−192. doi: 10.1016/j.margen.2009.10.002
    [61]
    Wang DP, Zhang YB, Zhang Z, et al. 2010. KaKs_Calculator 2.0: a toolkit incorporating Gamma-series methods and sliding window strategies. Genomics, Proteomics & Bioinformatics, 8(1): 77−80.
    [62]
    Wang ZF, Shi XJ, Sun LX, et al. 2017. Evolution of mitochondrial energy metabolism genes associated with hydrothermal vent adaption of Alvinocaridid shrimps. Genes & Genomics, 39(12): 1367−1376.
    [63]
    Xu Y, Zhan ZF, Xu KD. 2021. Morphological and molecular characterization of five species including three new species of golden gorgonians (Cnidaria: Octocorallia) from seamounts in the Western Pacific. Biology, 10(7): 588. doi: 10.3390/biology10070588
    [64]
    Yan CJ, Duanmu XY, Zeng X, et al. 2019. Mitochondrial DNA: distribution, mutations, and elimination. Cells, 8(4): 379. doi: 10.3390/cells8040379
    [65]
    Zhang B, Zhang YH, Wang X, et al. 2017. 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. doi: 10.1002/ece3.3067
    [66]
    Zhou Y, Feng CG, Pu YJ, et al. 2021. The first draft genome of a cold-water coral Trachythela sp. (Alcyonacea: Stolonifera: Clavulariidae). Genome Biology and Evolution, 13(2): evaa265. doi: 10.1093/gbe/evaa265
    [67]
    Zhu KC, Liang YY, Wu N, et al. 2017. Sequencing and characterization of the complete mitochondrial genome of Japanese Swellshark (Cephalloscyllium umbratile). Scientific Reports, 7(1): 15299. doi: 10.1038/s41598-017-15702-0
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