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Population differentiation of Rhodobacteraceae along with coral compartments


Coral mucus, tissue, and skeleton harbor compositionally different microbiota, but how these coral compartments shape the microbial evolution remains unexplored. Here, we sampled bacteria inhabiting a prevalent coral species Platygyra acuta and sequenced genomes of 234 isolates comprising two populations in Rhodobacteraceae, an alphaproteobacterial lineage representing a significant but variable proportion (5–50%) of the coral microbiota. The Ruegeria population (20 genomes) contains three clades represented by eight, six, and six isolates predominantly sampled from the skeleton (outgroup), mucus (clade-M), and skeleton (clade-S), respectively. The clade-M possesses functions involved in the utilization of coral osmolytes abundant in the mucus (e.g., methylamines, DMSP, taurine, and L-proline), whereas the clade-S uniquely harbors traits that may promote adaptation to the low-energy and diurnally anoxic skeleton (e.g., sulfur oxidation and swimming motility). These between-clade genetic differences were largely supported by physiological assays. Expanded analyses by including genomes of 24 related isolates (including seven new genomes) from other marine environments suggest that clade-M and clade-S may have diversified in non-coral habitats, but they also consolidated a key role of distinct coral compartments in diversifying many of the above-mentioned traits. The unassigned Rhodobacteraceae population (214 genomes) varies only at a few dozen nucleotide sites across the whole genomes, but the number of between-compartment migration events predicted by the Slatkin–Maddison test supported that dispersal limitation between coral compartments is another key mechanism diversifying microbial populations. Collectively, our results suggest that different coral compartments represent ecologically distinct and microgeographically separate habitats that drive the evolution of the coral microbiota.

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Fig. 1: The phylogeny and population differentiation of the Ruegeria population.
Fig. 2: The genomic differentiation of the Ruegeria population.
Fig. 3: The catabolic pathways of methylamine-related coral osmolytes in the Ruegeria population.
Fig. 4: Growth experiments of three clade-M strains and three clade-S strains.
Fig. 5: The phylogenetic distribution and pseudogene characterization of the flagellar gene cluster fla1 across the expanded Ruegeria population composed of isolates from both coral and non-coral marine habitats, along with the motility assays of select isolates.
Fig. 6: Compartmentalization of two subpopulations of the Rhodobacteraceae population each from a distinct coral individual.

Data availability

The assembled genomic sequences and raw reads of the coral-associated Ruegeria population, the seven Ruegeria isolates from non-coral marine habitats, and the coral-associated unassigned Rhodobacteraceae population are made publicly available at NCBI under GenBank assembly accession number PRJNA596594, PRJNA682389, and PRJNA596592, respectively.


  1. 1.

    Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40.

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Ainsworth TD, Thurber RV, Gates RD. The future of coral reefs: a microbial perspective. Trends Ecol Evol. 2010;25:233–40.

    PubMed  Article  Google Scholar 

  3. 3.

    Huettel M, Wild C, Gonelli S. Mucus trap in coral reefs: formation and temporal evolution of particle aggregates caused by coral mucus. Mar Ecol Prog Ser. 2006;307:69–84.

    Article  Google Scholar 

  4. 4.

    Coffroth M. Mucous sheet formation on poritid corals: an evaluation of coral mucus as a nutrient source on reefs. Mar Biol. 1990;105:39–49.

    CAS  Article  Google Scholar 

  5. 5.

    Brown BE, Bythell JC. Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser. 2005;296:291–309.

    CAS  Article  Google Scholar 

  6. 6.

    Sweet M, Croquer A, Bythell J. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs. 2011;30:39–52.

    Article  Google Scholar 

  7. 7.

    Yancey PH. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol. 2005;208:2819–30.

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Burg MB, Ferraris JD. Intracellular organic osmolytes: function and regulation. J Biol Chem. 2008;283:7309–13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Singh LR, Dar TA, editors. Cellular osmolytes: from chaperoning protein folding to clinical perspectives. 1st ed. Singapore: Springer Nature Singapore Pte Ltd.; 2017.

  10. 10.

    Yancey PH, Heppenstall M, Ly S, Andrell RM, Gates RD, Carter VL, et al. Betaines and dimethylsulfoniopropionate as major osmolytes in cnidaria with endosymbiotic dinoflagellates. Physiol Biochem Zool. 2010;83:167–73.

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Mayfield AB, Gates RD. Osmoregulation in anthozoan—dinoflagellate symbiosis. Compar Biochem Physiol A. 2007;147:1–10.

    Article  CAS  Google Scholar 

  12. 12.

    Rublee PA, Lasker HR, Gottfried M, Roman MR. Production and bacterial colonization of mucus from the soft coral Briarium asbestinum. Bull Mar Sci. 1980;30:888–93.

    Google Scholar 

  13. 13.

    Wild C, Woyt H, Huettel M. Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser. 2005;287:87–98.

    CAS  Article  Google Scholar 

  14. 14.

    Coles SL, Strathmann R. Observations on coral mucus “flocs” and their potential trophic significance. Limnol Oceanogr. 1973;18:673–8.

    Article  Google Scholar 

  15. 15.

    Pernice M, Raina J-B, Rädecker N, Cárdenas A, Pogoreutz C, Voolstra CR. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J. 2020;14:325–34.

    PubMed  Article  Google Scholar 

  16. 16.

    Falini G, Fermani S, Goffredo S. Coral biomineralization: a focus on intra-skeletal organic matrix and calcification. Semin Cell Dev Biol. 2015;46:17–26.

    Article  Google Scholar 

  17. 17.

    Constantz B, Weiner S. Acidic macromolecules associated with the mineral phase of scleractinian coral skeletons. J Exp Zool. 1988;248:253–8.

    CAS  Article  Google Scholar 

  18. 18.

    Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D. Stable isotopes (delta C-13 and delta N-15) of organic matrix from coral skeleton. Proc Natl Acad Sci USA. 2005;102:1525–30.

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Sorek M, Díaz-Almeyda EM, Medina M, Levy O. Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar Genom. 2014;14:47–57.

    Article  Google Scholar 

  20. 20.

    Agostini S, Suzuki Y, Higuchi T, Casareto B, Yoshinaga K, Nakano Y, et al. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs. 2012;31:147–56.

    Article  Google Scholar 

  21. 21.

    Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol. 2007;5:355–62.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Ritchie KB. Bacterial symbionts of corals and Symbiodinium. In: Rosenberg E, Gophna U editors. Beneficial microorganisms in multicellular life forms. 1st ed. Berlin Heidelberg: Springer-Verlag Berlin Heidelberg; 2012. pp 139–50.

  23. 23.

    Apprill A, Weber LG, Santoro AE. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems. 2016;1:e00143–00116.

    PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat Commun. 2018;9:1–13.

    CAS  Article  Google Scholar 

  25. 25.

    Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, et al. Population genomics of early events in the ecological differentiation of bacteria. Science. 2012;336:48–51.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Youngblut ND, Wirth JS, Henriksen JR, Smith M, Simon H, Metcalf WW, et al. Genomic and phenotypic differentiation among Methanosarcina mazei populations from Columbia River sediment. ISME J. 2015;9:2191–205.

    PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Wielgoss S, Didelot X, Chaudhuri RR, Liu X, Weedall GD, Velicer GJ, et al. A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. ISME J. 2016;10:2468–77.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Chase AB, Arevalo P, Brodie EL, Polz MF, Karaoz U, Martiny JB. Maintenance of sympatric and allopatric populations in free-living terrestrial bacteria. Mbio. 2019;10:e02361–02319.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Huggett MJ, Apprill A. Coral microbiome database: integration of sequences reveals high diversity and relatedness of coral-associated microbes. Environ Microbiol Rep. 2019;11:372–85.

    PubMed  Article  Google Scholar 

  30. 30.

    Apprill A, Marlow HQ, Martindale MQ, Rappe MS. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 2009;3:685–99.

    PubMed  Article  Google Scholar 

  31. 31.

    Epstein HE, Torda G, Munday PL, van Oppen MJH. Parental and early life stage environments drive establishment of bacterial and dinoflagellate communities in a common coral. ISME J. 2019;13:1635–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Freire I, Gutner-Hoch E, Muras A, Benayahu Y, Otero A. The effect of bacteria on planula-larvae settlement and metamorphosis in the octocoral Rhytisma fulvum fulvum. PLoS ONE. 2019;14:e0223214.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Miura N, Motone K, Takagi T, Aburaya S, Watanabe S, Aoki W, et al. Ruegeria sp. strains isolated from the reef-building coral Galaxea fascicularis inhibit growth of the temperature-dependent pathogen Vibrio coralliilyticus. Mar Biotechnol. 2019;21:1–8.

    CAS  Article  Google Scholar 

  34. 34.

    Apprill A, Hughen K, Mincer T. Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ Microbiol. 2013;15:2063–72.

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Sekar R, Kaczmarsky LT, Richardson LL. Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser. 2008;362:85–98.

    CAS  Article  Google Scholar 

  36. 36.

    Casey JM, Connolly SR, Ainsworth TD. Coral transplantation triggers shift in microbiome and promotion of coral disease associated potential pathogens. Sci Rep. 2015;5:11903–11903.

    PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Tsang RHL, Ang PO. Resistance to temperature stress and Drupella corallivory may promote the dominance of Platygyra acuta in the marginal coral communities in Hong Kong. Mar Environ Res. 2019;144:20–27.

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Tam TW, Ang PO Jr. Repeated physical disturbances and the stability of sub‐tropical coral communities in Hong Kong, China. Aquat Conserv. 2008;18:1005–24.

    Article  Google Scholar 

  39. 39.

    Ang Jr PO, Choi LS, Choi MM, Cornish A, Fung HL, Lee MW et al. Hong Kong. In: Centre JWR editors. Status of coral reefs of the East Asian Seas region: 2004. Tokyo: Ministry of the Environment; 2005. pp 121–52.

  40. 40.

    Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev. 2014;78:573–87.

    PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macián MC. The family Rhodobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F editors. The Prokaryotes: alphaproteobacteria and Betaproteobacteria. 4th ed. Berlin Heidelberg: Springer-Verlag Berlin Heidelberg; 2014. pp 439–512.

  42. 42.

    Johannes RE, Wiebe WJ. Method for determination of coral tissue biomass and composition. Limnol Oceanogr. 1970;15:822–4.

    Article  Google Scholar 

  43. 43.

    Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:1–14.

    Article  Google Scholar 

  44. 44.

    Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Achtman M, Wagner M. Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol. 2008;6:431–40.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Feil EJ, Spratt BG. Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol. 2001;55:561–90.

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Wang X, Zhang Y, Ren M, Xia T, Chu X, Liu C, et al. Cryptic speciation of a pelagic Roseobacter population varying at a few thousand nucleotide sites. ISME J. 2020;14:3106–19.

  48. 48.

    Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet. 2012;8:e1002453.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol. 2015;11:e1004041.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  50. 50.

    Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.

    PubMed  Article  Google Scholar 

  51. 51.

    Sun Y, Luo H. Homologous recombination in core genomes facilitates marine bacterial adaptation. Appl Environ Microbiol. 2018;84:e02545–02517.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Librado P, Vieira FG, Rozas J. BadiRate: estimating family turnover rates by likelihood-based methods. Bioinformatics. 2011;28:279–81.

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    Slatkin M, Maddison WP. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 1989;123:603–13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:1–8.

    Article  CAS  Google Scholar 

  55. 55.

    Lohr KE, Khattri RB, Guingab-Cagmat J, Camp EF, Merritt ME, Garrett TJ, et al. Metabolomic profiles differ among unique genotypes of a threatened Caribbean coral. Sci Rep. 2019;9:1–11.

    CAS  Article  Google Scholar 

  56. 56.

    Hill R, Li C, Jones A, Gunn J, Frade P. Abundant betaines in reef-building corals and ecological indicators of a photoprotective role. Coral Reefs. 2010;29:869–80.

    Article  Google Scholar 

  57. 57.

    Gowrishankar J. Nucleotide sequence of the osmoregulatory proU operon of Escherichia coli. J Bacteriol. 1989;171:1923–31.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. 58.

    Chandravanshi M, Gogoi P, Kanaujia SP. Computational characterization of TTHA0379: A potential glycerophosphocholine binding protein of Ugp ATP-binding cassette transporter. Gene. 2016;592:260–8.

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Ziegler C, Bremer E, Krämer R. The BCCT family of carriers: from physiology to crystal structure. Mol Microbiol. 2010;78:13–34.

    CAS  PubMed  Google Scholar 

  60. 60.

    Geiger O, López-Lara IM, Sohlenkamp C. Phosphatidylcholine biosynthesis and function in bacteria. Biochim Biophys Acta Mol Cell Biol Lipids. 2013;1831:503–13.

    CAS  Article  Google Scholar 

  61. 61.

    Lidbury I, Kimberley G, Scanlan DJ, Murrell JC, Chen Y. Comparative genomics and mutagenesis analyses of choline metabolism in the marine Roseobacter clade. Environ Microbiol. 2015;17:5048–62.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 62.

    Thole S, Kalhoefer D, Voget S, Berger M, Engelhardt T, Liesegang H, et al. Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J. 2012;6:2229–44.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, DuGar B, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57–63.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Jones M, Talfournier F, Bobrov A, Grossmann JG, Vekshin N, Sutcliffe MJ, et al. Electron transfer and conformational change in complexes of trimethylamine dehydrogenase and electron transferring flavoprotein. J Biol Chem. 2002;277:8457–65.

    CAS  PubMed  Article  Google Scholar 

  65. 65.

    Chen Y. Comparative genomics of methylated amine utilization by marine Roseobacter clade bacteria and development of functional gene markers (tmm, gmaS). Environ Microbiol. 2012;14:2308–22.

    CAS  PubMed  Article  Google Scholar 

  66. 66.

    Schäfer H, McDonald IR, Nightingale PD, Murrell JC. Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halide‐oxidizing bacteria. Environ Microbiol. 2005;7:839–52.

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    McNicholas PM, Chiang RC, Gunsalus RP. Anaerobic regulation of the Escherichia coli dmsABC operon requires the molybdate‐responsive regulator ModE. Mol Microbiol. 1998;27:197–208.

    CAS  PubMed  Article  Google Scholar 

  68. 68.

    Loschi L, Brokx SJ, Hills TL, Zhang G, Bertero MG, Lovering AL, et al. Structural and biochemical identification of a novel bacterial oxidoreductase. J Biol Chem. 2004;279:50391–50400.

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Hillyer KE, Dias DA, Lutz A, Wilkinson SP, Roessner U, Davy SK. Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs. 2017;36:105–18.

    Article  Google Scholar 

  70. 70.

    Rösgen J. Molecular basis of osmolyte effects on protein and metabolites. Methods Enzymol. 2007;428:459–86.

    PubMed  Article  CAS  Google Scholar 

  71. 71.

    Cunliffe M. Correlating carbon monoxide oxidation with cox genes in the abundant marine Roseobacter clade. ISME J. 2011;5:685–91.

    CAS  PubMed  Article  Google Scholar 

  72. 72.

    Bartling P, Vollmers J, Petersen J. The first world swimming championships of Roseobacters—phylogenomic insights into an exceptional motility phenotype. Syst Appl Microbiol. 2018;41:544–54.

    PubMed  Article  Google Scholar 

  73. 73.

    Michael V, Frank O, Bartling P, Scheuner C, Goker M, Brinkmann H, et al. Biofilm plasmids with a rhamnose operon are widely distributed determinants of the ‘swim-or-stick’ lifestyle in roseobacters. ISME J. 2016;10:2498–513.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. 74.

    Armitage JP. Behavioural responses of bacteria to light and oxygen. Arch Microbiol. 1997;168:249–61.

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Jorgensen NOG. Uptake of urea by estuarine bacteria. Aquat Micro Ecol. 2006;42:227–42.

    Article  Google Scholar 

  76. 76.

    Pernice M, Raina J-B, Rädecker N, Cárdenas A, Pogoreutz C, Voolstra CR. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J. 2019: 1–10.

  77. 77.

    Krajewska B, Ureases I. Functional, catalytic and kinetic properties: a review. J Mol Catal B Enzym. 2009;59:9–21.

    CAS  Article  Google Scholar 

  78. 78.

    Cheng L, Cord-Ruwisch R. In situ soil cementation with ureolytic bacteria by surface percolation. Ecol Eng. 2012;42:64–72.

    Article  Google Scholar 

  79. 79.

    Cho BC, Park MG, Shim JH, Azam F. Significance of bacteria in urea dynamics in coastal surface waters. Mar Ecol Prog Ser. 1996;142:19–26.

    Article  Google Scholar 

  80. 80.

    Jin D, Zhao SG, Zheng N, Beckers Y, Wang JQ. Urea metabolism and regulation by rumen bacterial urease in ruminants—a review. Ann Anim Sci. 2018;18:303–18.

    Article  Google Scholar 

  81. 81.

    Collier JL, Baker KM, Bell SL. Diversity of urea-degrading microorganisms in open-ocean and estuarine planktonic communities. Environ Microbiol. 2009;11:3118–31.

    CAS  PubMed  Article  Google Scholar 

  82. 82.

    Biscéré T, Ferrier-Pagès C, Grover R, Gilbert A, Rottier C, Wright A, et al. Enhancement of coral calcification via the interplay of nickel and urease. Aquat Toxicol. 2018;200:247–56.

    PubMed  Article  CAS  Google Scholar 

  83. 83.

    Crossland C, Barnes D. The role of metabolic nitrogen in coral calcification. Mar Biol. 1974;28:325–32.

    CAS  Article  Google Scholar 

  84. 84.

    Goodkin NF, Switzer AD, Mccorry D, Devantier L, True J, Hughen KA, et al. Coral communities of Hong Kong: long-lived corals in a marginal reef environment. Mar Ecol Prog Ser. 2011;426:185–96.

    Article  Google Scholar 

  85. 85.

    Bernasconi R, Stat M, Koenders A, Paparini A, Bunce M, Huggett MJ. Establishment of coral-bacteria symbioses reveal changes in the core bacterial community with host ontogeny. Front Mirobiol. 2019;10:1529.

    Article  Google Scholar 

  86. 86.

    Chu X, Li S, Wang S, Luo D, Luo H. Gene loss through pseudogenization contributes to the ecological diversification of a generalist Roseobacter lineage. ISME J. 2020;15:489–502.

    PubMed  Article  CAS  Google Scholar 

  87. 87.

    Gardner SN, Slezak T, Hall BG. kSNP3. 0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics. 2015;31:2877–8.

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Krzywinski M, Schein JE, Birol I, Connors JM, Gascoyne RD, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19:1639–45.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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We thank Ryan Ho-Leung Tsang for the coral sample collection, Tsz-Yan Ng for guiding coral sample processing, Xiao Chu and Shuangfei Zhang for their help on bacteria cultivation, Hao Zhang and Minglei Ren for their help in data analysis, and Xinqin Lin for her advice in experimental design. We thank Xiao Chu, Minglei Ren, and Zhichao Zhou for providing isolates from the brown algae ecosystem, sediments, and mangrove ecosystem. This work was supported by the Shenzhen Science and Technology Committee (JCYJ20180508161811899), the National Natural Science Foundation of China (41776129), the Hong Kong Environment and Conservation Fund (15/2016), the Hong Kong Research Grants Council General Research Fund (14163917), and the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16).

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Luo, D., Wang, X., Feng, X. et al. Population differentiation of Rhodobacteraceae along with coral compartments. ISME J (2021).

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