Lophelia pertusa corals from the Ionian and Barents seas share identical nuclear ITS2 and near-identical mitochondrial genome sequences

BMC Research Notes

Carl André¹  Mikael Dahl¹  Jean-François Flot² 

[1] Department of Biological and Environmental Sciences – Tjärnö, University of Gothenburg, Strömstad, 452 96, Sweden;Max Planck Institute for Dynamics and Self-Organization, Biological Physics and Evolutionary Dynamics, Göttingen, 37077, Germany

关键词: Mediterranean outflow water;    Phylogeography;    Haploweb;    Internal transcribed spacer;    Control region;    Mitogenomics;   

Others  :  1142960
DOI  :  10.1186/1756-0500-6-144

 received in 2012-11-27, accepted in 2013-03-22,  发布年份 2013

【 摘 要 】

Background

Lophelia pertusa is a keystone cold-water coral species with a widespread distribution. Due to the lack of a mitochondrial marker variable enough for intraspecific analyses, the population structure of this species has only been studied using ITS and microsatellites so far. We therefore decided to sequence and compare complete mitochondrial genomes from two distant L. pertusa populations putatively isolated from each other (in the Barents Sea off Norway and in the Mediterranean Sea off Italy) in the hope of finding regions variable enough for population genetic and phylogeographic studies.

Results

The mitogenomes of two L. pertusa individuals collected in the Mediterranean and Barents seas differed at only one position, which was a non-synonymous substitution, but comparison with another recently published L. pertusa mitochondrial genome sequence from Norway revealed 18 nucleotide differences. These included two synonymous and nine non-synonymous substitutions in protein-coding genes (dN/dS > 1): hence, the mitogenome of L. pertusa may be experiencing positive selection. To test for the presence of cryptic species, the mitochondrial control region and the nuclear ITS2 were sequenced for five individuals from each site: Italian and Norwegian populations turned out to share haplotypes of both markers, indicating that they belonged to the same species.

Conclusions

L. pertusa corals collected 7,500 km apart shared identical nuclear ITS2 and near-identical mitogenomes, supporting the hypothesis of a recent connection between Lophelia reefs in the Mediterranean and in the Northern Atlantic. Multi-locus or population genomic approaches will be required to shed further light on the genetic connectivity between L. pertusa reefs across Europe; nevertheless, ITS2 and the mitochondrial control region may be useful markers for investigating the phylogeography and species boundaries of the keystone genus Lophelia across its worldwide area of distribution.

【 授权许可】

   
2013 Flot et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Shearer TL, van Oppen MJH, Romano SL, Wörheide G: Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 2002, 11:2475-2487.
• [2]Huang D, Meier R, Todd P, Chou L: Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 2008, 66:167-174.
• [3]Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL: Naked corals: skeleton loss in Scleractinia. Proc Natl Acad Sci USA 2006, 103:9096-9100.
• [4]Chen C, Chiou C-Y, Dai C-F, Chen CA: Unique mitogenomic features in the scleractinian family Pocilloporidae (Scleractinia: Astrocoeniina). Marine Biotechnol 2008, 10:538-553.
• [5]Chen C, Dai C-F, Plathong S, Chiou C-Y, Chen CA: The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinia: Pocilloporidae): an idiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations. Mol Phylogenet Evol 2008, 46:19-33.
• [6]Flot J-F, Licuanan W, Nakano Y, Payri C, Cruaud C, Tillier S: Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs 2008, 27:789-794.
• [7]Fukami H, Chen C, Chiou C-Y, Knowlton N: Novel group I introns encoding a putative homing endonuclease in the mitochondrial cox1 gene of scleractinian corals. J Mol Evol 2007, 64:591-600.
• [8]Flot J-F, Tillier S: The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: the putative D-loop and a novel ORF of unknown function. Gene 2007, 401:80-87.
• [9]Linnaeus C: Systema naturae per regna tria naturæ secundum classes, ordines, genera, species, cum characteribus, differentilis, synonymis, locis. Edited by Tomus I. Stockholm: Laurentius Salvius; 1758. Editio decima, reformata
• [10]Emblem Å, Karlsen BO, Evertsen J, Johansen SD: Mitogenome rearrangement in the cold-water scleractinian coral Lophelia pertusa (Cnidaria, Anthozoa) involves a long-term evolving group I intron. Mol Phylogenet Evol 2011, 61:495-503.
• [11]Rogers AD: The biology of Lophelia pertusa (Linnaeus 1758) and other deep-water reef-forming corals and impacts from human activities. Int Rev Hydrobiol 1999, 84:315-406.
• [12]Jensen A, Frederiksen R: The fauna associated with the bank-forming deepwater coral Lophelia pertusa (Scleractinia) on the Faroe shelf. Sarsia 1992, 77:53-69.
• [13]Costello M, McCrea M, Freiwald A, Lundälv T, Jonsson L, Bett BJ, van Weering TCE, de Haas H, Roberts JM, Allen D: Role of cold-water Lophelia pertusa coral reefs as fish habitat in the NE Atlantic. In Cold-Water Corals and Ecosystems. Edited by Freiwald A. Springer: Berlin Heidelberg; 2005:771-805.
• [14]Lessard-Pilon SA, Podowski EL, Cordes EE, Fisher CR: Megafauna community composition associated with Lophelia pertusa colonies in the Gulf of Mexico. Deep-Sea Res II Top Stud Oceanogr 2010, 57:1882-1890.
• [15]Fosså JH, Mortensen PB, Furevik DM: The deep-water coral Lophelia pertusa in Norwegian waters: distribution and fishery impacts. Hydrobiologia 2002, 471:1-12.
• [16]Hall-Spencer J, Allain V, Fosså JH: Trawling damage to Northeast Atlantic ancient coral reefs. Proc R Soc Lond B Biol Sci 2002, 269:507-511.
• [17]Guinotte JM, Orr J, Cairns S, Freiwald A, Morgan L, George R: Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals? Front Ecol Environ 2006, 4:141-146.
• [18]Turley C, Roberts J, Guinotte J: Corals in deep-water: will the unseen hand of ocean acidification destroy cold-water ecosystems? Coral Reefs 2007, 26:445-448.
• [19]Le Goff-Vitry MC, Rogers AD, Baglow D: A deep-sea slant on the molecular phylogeny of the Scleractinia. Mol Phylogenet Evol 2004, 30:167-177.
• [20]Le Goff-Vitry M-C: Molecular ecology of the deep-sea coral Lophelia pertusa in the North East Atlantic. University of Southampton, School of Ocean and Earth Science: PhD thesis; 2003.
• [21]Le Goff-Vitry MC, Pybus OG, Rogers AD: Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 2004, 13:537-549.
• [22]Morrison C, Ross S, Nizinski M, Brooke S, Järnegren J, Waller R, Johnson R, King T: Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 2011, 12:713-729.
• [23]Dahl MP, Pereyra RT, Lundälv T, André C: Fine-scale spatial genetic structure and clonal distribution of the cold-water coral Lophelia pertusa. Coral Reefs 2012, 31:1135-1148.
• [24]U.S. Department of Commerce NOaAA: 2-minute Gridded Global Relief Data (ETOPO2v2). : ; 2006. http://www.ngdc.noaa.gov/mgg/fliers/06mgg01.html webcite
• [25]Jakobsson M, Macnab R, Mayer L, Anderson R, Edwards M, Hatzky J, Schenke HW, Johnson P: An improved bathymetric portrayal of the Arctic Ocean: implications for ocean modeling and geological, geophysical and oceanographic analyses. Geophys Res Lett 2008., 35L07602
• [26]Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J: KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006, 4:259-263.
• [27]Nei M, Kumar S: Molecular Evolution and Phylogenetics. Oxford: Oxford University Press; 2000.
• [28]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
• [29]Li W-H, Wu C-I, Luo C-C: A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 1985, 2:150-174.
• [30]Tzeng Y-H, Pan R, Li W-H: Comparison of three methods for estimating rates of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 2004, 21:2290-2298.
• [31]Li W-H: Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 1993, 36:96-99.
• [32]Pamilo P, Bianchi NO: Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 1993, 10:271-281.
• [33]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
• [34]Zhang Z, Li J, Yu J: Computing Ka and Ks with a consideration of unequal transitional substitutions. BMC Evol Biol 2006, 6:44. BioMed Central Full Text
• [35]Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 1994, 11:725-736.
• [36]Muse SV, Gaut BS: A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol 1994, 11:715-724.
• [37]Flot J-F, Magalon H, Cruaud C, Couloux A, Tillier S: Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biologies 2008, 331:239-247.
• [38]Forsman Z, Barshis D, Hunter C, Toonen R: Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 2009, 9:45. BioMed Central Full Text
• [39]Flot J-F, Couloux A, Tillier S: Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evol Biol 2010, 10:372. BioMed Central Full Text
• [40]Flot J-F, Blanchot J, Charpy L, Cruaud C, Licuanan W, Nakano Y, Payri C, Tillier S: Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecol 2011, 11:22. BioMed Central Full Text
• [41]Stefani F, Benzoni F, Yang SY, Pichon M, Galli P, Chen C: Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 2011, 30:1033-1049.
• [42]Clark A: Inference of haplotypes from PCR-amplified samples of diploid populations. Mol Biol Evol 1990, 7:111-122.
• [43]Doyle JJ: The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Syst Bot 1995, 20:574-588.
• [44]Emblem Å, Karlsen BO, Evertsen J, Miller DJ, Moum T, Johansen SD: Mitogenome polymorphism in a single branch sample revealed by SOLiD deep sequencing of the Lophelia pertusa coral genome. Gene 2012, 506:344-349.
• [45]Hellberg M: No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 2006, 6:24. BioMed Central Full Text
• [46]Fukami H, Knowlton N: Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex (Cnidaria, Anthozoa, Scleractinia). Coral Reefs 2005, 24:410-417.
• [47]De Mol B, Van Rensbergen P, Pillen S, Van Herreweghe K, Van Rooij D, McDonnell A, Huvenne V, Ivanov M, Swennen R, Henriet JP: Large deep-water coral banks in the Porcupine Basin, southwest of Ireland. Mar Geol 2002, 188:193-231.
• [48]De Mol B, Henriet J-P, Canals M: Development of coral banks in Porcupine Seabight: do they have Mediterranean ancestors? In Cold-Water Corals and Ecosystems. Edited by Freiwald A, Roberts JM. Springer: Berlin Heidelberg; 2005:515-533.
• [49]McCulloch M, Taviani M, Montagna P, López Correa M, Remia A, Mortimer G: Proliferation and demise of deep-sea corals in the Mediterranean during the Younger Dryas. Earth Planet Sci Lett 2010, 298:143-152.
• [50]Schönfeld J, Zahn R: Late Glacial to Holocene history of the Mediterranean Outflow. Evidence from benthic foraminiferal assemblages and stable isotopes at the Portuguese margin. Palaeogeogr Palaeoclimatol Palaeoecol 2000, 159:85-111.
• [51]Frank N, Freiwald A, Correa ML, Wienberg C, Eisele M, Hebbeln D, Van Rooij D, Henriet J-P, Colin C, van Weering T: Northeastern Atlantic cold-water coral reefs and climate. Geology 2011, 39:743-746.
• [52]Tursi A, Mastrototaro F, Matarrese A, Maiorano P, D’Onghia G: Biodiversity of the white coral reefs in the Ionan Sea (Central Mediterranean). Chem Ecol 2004, 20:S107-S116.
• [53]Taviani M, Remia A, Corselli C, Freiwald A, Malinverno E, Mastrototaro F, Savini A, Tursi A: First geo-marine survey of living cold-water Lophelia reefs in the Ionian Sea (Mediterranean basin). Facies 2005, 50:409-417.
• [54]Mastrototaro F, D’Onghia G, Corriero G, Matarrese A, Maiorano P, Panetta P, Gherardi M, Longo C, Rosso A, Sciuto F: Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): An update. Deep-Sea Res II Top Stud Oceanogr 2010, 57:412-430.
• [55]Sargent TD, Jamrich M, Dawid IB: Cell interactions and the control of gene activity during early development of Xenopus laevis. Dev Biol 1986, 114:238-246.
• [56]Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N: Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 2004, 38:324-337.
• [57]Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols. Edited by Misener S, Krawetz SA. Totowa, NJ: Humana Press; 2000:365-386.
• [58]Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994, 3:294-299.
• [59]Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [60]Gray M, Lang B, Cedergren R, Golding G, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn T: Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 1998, 26:865-878.
• [61]Lowe T, Eddy S: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
• [62]Benson G: Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580.
• [63]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
• [64]Flot J-F, Tillier S: Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. Proceedings of the 10th International Coral Reef Symposium 2006, 1:24-29.