1887

Abstract

Coral diseases contribute to the decline of coral reefs globally and threaten the health and future of coral reef communities. Acute Montipora white syndrome (aMWS) is a tissue loss disease that has led to the mortality of hundreds of Montipora capitata colonies in Kāne‘ohe Bay, Hawai‘i in recent years. This study describes the analysis of coral-associated bacterial communities using high-throughput sequencing generated by the PacBio RSII platform. Samples from three health states of M. capitata (healthy, healthy-diseased and diseased) were collected during an ongoing aMWS outbreak and a non-outbreak period and the bacterial communities were identified to determine whether a shift in community structure had occurred between the two periods. The bacterial communities associated with outbreak and non-outbreak samples were significantly different, and one major driver was a high abundance of operational taxonomic units (OTUs) identified as Escherichia spp. in the outbreak sequences. In silico bacterial source tracking suggested this OTU was likely from sewage contamination of livestock, rather than human, origin. The most abundant coliform OTU was a culturable E. fergusonii isolate, strain OCN300, however, it did not induce disease signs on healthy M. capitata colonies when used in laboratory infection trials. In addition, screening of the sequencing output found that the most abundant OTUs corresponded to previously described M. capitata pathogens. The synergistic combination of known coral pathogens, sewage contaminants and other stressors, such as fluctuating seawater temperatures and bacterial pathogens, have the potential to escalate the deterioration of coral reef ecosystems.

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2018-07-27
2019-09-24
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References

  1. Bourne DG, Munn CB. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 2005;7:1162–1174 [CrossRef][PubMed]
    [Google Scholar]
  2. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N. Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 2001;20:85–91
    [Google Scholar]
  3. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 2002;243:1–10 [CrossRef]
    [Google Scholar]
  4. Siboni N, Ben-Dov E, Sivan A, Kushmaro A. Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 2008;10:2979–2990 [CrossRef][PubMed]
    [Google Scholar]
  5. Kellogg CA. Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 2004;273:81–88 [CrossRef]
    [Google Scholar]
  6. Wegley L, Yu Y, Breitbart M, Casas V, Kline DI et al. Coral-associated Archaea. Mar Ecol Prog Ser 2004;273:89–96 [CrossRef]
    [Google Scholar]
  7. Patten NL, Harrison PL, Mitchell JG. Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef. Coral Reefs 2008;27:569–580 [CrossRef]
    [Google Scholar]
  8. Thurber RLV, Correa AMS. Viruses of reef-building scleractinian corals. J Exp Mar Bio Ecol 2011;408:102–113 [CrossRef]
    [Google Scholar]
  9. Wilson WH, Dale AL, Davy JE, Davy SK. An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 2005;24:145–148 [CrossRef]
    [Google Scholar]
  10. Amend AS, Barshis DJ, Oliver TA. Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 2012;6:1291–1301 [CrossRef][PubMed]
    [Google Scholar]
  11. Bentis CJ, Kaufman L, Golubic S. Endolithic fungi in reef-building corals (Order : Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 2000;198:254–260 [CrossRef][PubMed]
    [Google Scholar]
  12. Campion-Alsumard TL, Golubic S, Priess K. Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Oceanogr Lit Rev 1995;9:776–777
    [Google Scholar]
  13. Antonius AA, Lipscomb D. First protozoan coral-killer identified in the Indo-Pacific. Atoll Res Bull 2000;481: [CrossRef]
    [Google Scholar]
  14. Kramarsky-Winter E, Harel M, Siboni N, Ben Dov E, Brickner I et al. Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 2006;317:67–73 [CrossRef]
    [Google Scholar]
  15. Sharp KH, Ritchie KB. Multi-partner interactions in corals in the face of climate change. Biol Bull 2012;223:66–77 [CrossRef][PubMed]
    [Google Scholar]
  16. Bourne DG, Webster NS. Coral reef bacterial communities. The Prokaryotes Springer; 2013; pp.163–187
    [Google Scholar]
  17. Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA et al. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc Natl Acad Sci USA 2014;111:10227–10232 [CrossRef][PubMed]
    [Google Scholar]
  18. Morrow KM, Moss AG, Chadwick NE, Liles MR. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 2012;78:6438–6449 [CrossRef][PubMed]
    [Google Scholar]
  19. Ainsworth TD, Thurber RV, Gates RD. The future of coral reefs: a microbial perspective. Trends Ecol Evol 2010;25:233–240 [CrossRef][PubMed]
    [Google Scholar]
  20. Bourne D, Iida Y, Uthicke S, Smith-Keune C. Changes in coral-associated microbial communities during a bleaching event. ISME J 2008;2:350–363 [CrossRef][PubMed]
    [Google Scholar]
  21. Hernandez-Agreda A, Leggat W, Bongaerts P, Ainsworth TD. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio 2016;7:e00560-16 [CrossRef][PubMed]
    [Google Scholar]
  22. 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;5:355–362 [CrossRef][PubMed]
    [Google Scholar]
  23. Sweet MJ, Croquer A, Bythell JC. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 2011;30:39–52 [CrossRef]
    [Google Scholar]
  24. Williams AD, Brown BE, Putchim L, Sweet MJ. Age-related shifts in bacterial diversity in a reef coral. PLoS One 2015;10:e0144902 [CrossRef][PubMed]
    [Google Scholar]
  25. Sunagawa S, Woodley CM, Medina M. Threatened corals provide underexplored microbial habitats. PLoS One 2010;5:e9554 [CrossRef][PubMed]
    [Google Scholar]
  26. Krediet CJ, Ritchie KB, Alagely A, Teplitski M. Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J 2013;7:980–990 [CrossRef][PubMed]
    [Google Scholar]
  27. Kvennefors EC, Sampayo E, Kerr C, Vieira G, Roff G et al. Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol 2012;63:605–618 [CrossRef][PubMed]
    [Google Scholar]
  28. Mills E, Shechtman K, Loya Y, Rosenberg E. Bacteria appear to play important roles in both causing and preventing the bleaching of the coral Oculina patagonica. Mar Ecol Prog Ser 2013;489:155–162 [CrossRef]
    [Google Scholar]
  29. Nissimov J, Rosenberg E, Munn CB. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 2009;292:210–215 [CrossRef][PubMed]
    [Google Scholar]
  30. Ritchie KB. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 2006;322:1–14 [CrossRef]
    [Google Scholar]
  31. Rypien KL, Ward JR, Azam F. Antagonistic interactions among coral-associated bacteria. Environ Microbiol 2010;12:28–39 [CrossRef][PubMed]
    [Google Scholar]
  32. Barneah O, Ben-Dov E, Kramarsky-Winter E, Kushmaro A. Characterization of black band disease in Red Sea stony corals. Environ Microbiol 2007;9:1995–2006 [CrossRef][PubMed]
    [Google Scholar]
  33. Shore-Maggio A, Runyon CM, Ushijima B, Aeby GS, Callahan SM. Differences in bacterial community structure in two color morphs of the Hawaiian reef coral Montipora capitata. Appl Environ Microbiol 2015;81:7312–7318 [CrossRef][PubMed]
    [Google Scholar]
  34. Pantos O, Cooney RP, Le Tissier MD, Barer MR, O'Donnell AG et al. The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ Microbiol 2003;5:370–382 [CrossRef][PubMed]
    [Google Scholar]
  35. Wilson B, Aeby GS, Work TM, Bourne DG. Bacterial communities associated with healthy and Acropora white syndrome-affected corals from American Samoa. FEMS Microbiol Ecol 2012;80:509–520 [CrossRef][PubMed]
    [Google Scholar]
  36. Aeby GS, Ross M, Williams GJ, Lewis TD, Works TM. Disease dynamics of Montipora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility. Dis Aquat Organ 2010;91:1–8 [CrossRef][PubMed]
    [Google Scholar]
  37. Ushijima B, Smith A, Aeby GS, Callahan SM. Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS One 2012;7:e46717 [CrossRef][PubMed]
    [Google Scholar]
  38. Aeby GS, Callahan S, Cox EF, Runyon C, Smith A et al. Emerging coral diseases in Kāne'ohe Bay, O'ahu, Hawai'i (USA): two major disease outbreaks of acute Montipora white syndrome. Dis Aquat Organ 2016;119:189–198 [CrossRef][PubMed]
    [Google Scholar]
  39. Beurmann S, Ushijima B, Svoboda CM, Videau P, Smith AM et al. Pseudoalteromonas piratica sp. nov., a budding, prosthecate bacterium from diseased Montipora capitata, and emended description of the genus Pseudoalteromonas. Int J Syst Evol Microbiol 2017;67:2683–2688 [CrossRef][PubMed]
    [Google Scholar]
  40. Cooney RP, Pantos O, Le Tissier MD, Barer MR, O'Donnell AG et al. Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 2002;4:401–413 [CrossRef][PubMed]
    [Google Scholar]
  41. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW. Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 2002;68:2214–2228 [CrossRef][PubMed]
    [Google Scholar]
  42. Haley BJ, Grim CJ, Hasan NA, Choi SY, Chun J et al. Comparative genomic analysis reveals evidence of two novel Vibrio species closely related to V. cholerae. BMC Microbiol 2010;10:154 [CrossRef][PubMed]
    [Google Scholar]
  43. Sawabe T, Kita-Tsukamoto K, Thompson FL. Inferring the evolutionary history of vibrios by means of multilocus sequence analysis. J Bacteriol 2007;189:7932–7936 [CrossRef][PubMed]
    [Google Scholar]
  44. Suzuki MT, Giovannoni SJ. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 1996;62:625–630[PubMed]
    [Google Scholar]
  45. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537–7541 [CrossRef][PubMed]
    [Google Scholar]
  46. Team RC. R: A Language and Environment for Statistical Computing. Version 3.1. 3 Vienna, Austria: R Foundation for Statistical Computing; 2015
    [Google Scholar]
  47. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 2013;79:5112–5120 [CrossRef][PubMed]
    [Google Scholar]
  48. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007;35:7188–7196 [CrossRef][PubMed]
    [Google Scholar]
  49. Schloss PD. Secondary structure improves OTU assignments of 16S rRNA gene sequences. ISME J 2013;7:457–460 [CrossRef][PubMed]
    [Google Scholar]
  50. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194–2200 [CrossRef][PubMed]
    [Google Scholar]
  51. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007;73:5261–5267 [CrossRef][PubMed]
    [Google Scholar]
  52. Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ. Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr Biol 2012;22:R518–R519 [CrossRef][PubMed]
    [Google Scholar]
  53. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  54. Mosher JJ, Bowman B, Bernberg EL, Shevchenko O, Kan J et al. Improved performance of the PacBio SMRT technology for 16S rDNA sequencing. J Microbiol Methods 2014;104:59–60 [CrossRef][PubMed]
    [Google Scholar]
  55. Shannon CE. A mathematical theory of communication. Bell System Technical Journal 1948;27:379–423 [CrossRef]
    [Google Scholar]
  56. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003;100:9440–9445 [CrossRef][PubMed]
    [Google Scholar]
  57. Bray JR, Curtis JT. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 1957;27:325–349 [CrossRef]
    [Google Scholar]
  58. Okabe S, Shimazu Y. Persistence of host-specific Bacteroides-Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity. Appl Microbiol Biotechnol 2007;76:935–944 [CrossRef][PubMed]
    [Google Scholar]
  59. Thomopson J, Higgins DG, Gibson TJ. ClustalW. Nucleic Acids Res 1994;22:4673–4680
    [Google Scholar]
  60. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406–425 [CrossRef][PubMed]
    [Google Scholar]
  61. Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res 1999;9:868–877 [CrossRef][PubMed]
    [Google Scholar]
  62. Ushijima B, Videau P, Burger AH, Shore-Maggio A, Runyon CM et al. Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol 2014;80:2102–2109 [CrossRef][PubMed]
    [Google Scholar]
  63. Beurmann S, Ushijima B, Videau P, Svoboda CM, Smith AM et al. Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata. PLoS One 2017;12:e0188319 [CrossRef][PubMed]
    [Google Scholar]
  64. Ushijima B, Videau P, Poscablo D, Stengel JW, Beurmann S et al. Mutation of the toxR or mshA genes from Vibrio coralliilyticus strain OCN014 reduces infection of the coral Acropora cytherea. Environ Microbiol 2016;18:4055–4067 [CrossRef][PubMed]
    [Google Scholar]
  65. Schloss PD, Jenior ML, Koumpouras CC, Westcott SL, Highlander SK. Sequencing 16S rRNA gene fragments using the PacBio SMRT DNA sequencing system. PeerJ 2016;4:e1869 [CrossRef][PubMed]
    [Google Scholar]
  66. Ishii S, Sadowsky MJ. Escherichia coli in the environment: implications for water quality and human health. Microbes Environ 2008;23:101–108 [CrossRef][PubMed]
    [Google Scholar]
  67. Patterson KL, Porter JW, Ritchie KB, Polson SW, Mueller E et al. The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 2002;99:8725–8730 [CrossRef][PubMed]
    [Google Scholar]
  68. Sutherland KP, Shaban S, Joyner JL, Porter JW, Lipp EK. Human pathogen shown to cause disease in the threatened eklhorn coral Acropora palmata. PLoS One 2011;6:e23468 [CrossRef][PubMed]
    [Google Scholar]
  69. Pootakham W, Mhuantong W, Yoocha T, Putchim L, Sonthirod C et al. High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci Rep 2017;7:2774 [CrossRef][PubMed]
    [Google Scholar]
  70. Hernandez-Agreda A, Gates RD, Ainsworth TD. Defining the core microbiome in corals' microbial soup. Trends Microbiol 2017;25:125–140 [CrossRef][PubMed]
    [Google Scholar]
  71. Wagner J, Coupland P, Browne HP, Lawley TD, Francis SC et al. Evaluation of PacBio sequencing for full-length bacterial 16S rRNA gene classification. BMC Microbiol 2016;16:274 [CrossRef][PubMed]
    [Google Scholar]
  72. Lipp EK, Jarrell JL, Griffin DW, Lukasik J, Jacukiewicz J et al. Preliminary evidence for human fecal contamination in corals of the Florida Keys, USA. Mar Pollut Bull 2002;44:666–670 [CrossRef][PubMed]
    [Google Scholar]
  73. Gerba CP, McLeod JS. Effect of sediments on the survival of Escherichia coli in marine waters. Appl Environ Microbiol 1976;32:114–120[PubMed]
    [Google Scholar]
  74. Dufour AP. 1977; Escherichia coli: the fecal coliform. www.astm.org/DIGITAL_LIBRARY/STP/PAGES/STP34817S.htm [cited 24 Jan 2017]
  75. Wear SL, Thurber RV. Sewage pollution: mitigation is key for coral reef stewardship. Ann N Y Acad Sci 2015;1355:15–30 [CrossRef][PubMed]
    [Google Scholar]
  76. Edwards DD, McFeters GA, Venkatesan MI. Distribution of Clostridium perfringens and fecal sterols in a benthic coastal marine environment influenced by the sewage outfall from McMurdo Station, Antarctica. Appl Environ Microbiol 1998;64:2596–2600[PubMed]
    [Google Scholar]
  77. Bahr KD, Jokiel PL, Toonen RJ. The unnatural history of Kāne'ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 2015;3:e950 [CrossRef][PubMed]
    [Google Scholar]
  78. Tanaka K, Guidry MW, Gruber N. Ecosystem responses of the subtropical Kaneohe Bay, Hawaii, to climate change: a nitrogen cycle modeling approach. Aquat Geochem 2013;19:569–590 [CrossRef]
    [Google Scholar]
  79. Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A. Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev 2014;38:1–40 [CrossRef][PubMed]
    [Google Scholar]
  80. Betancourt WQ, Fujioka RS. Bacteroides spp. as reliable marker of sewage contamination in Hawaii's environmental waters using molecular techniques. Water Sci Technol 2006;54:101–107 [CrossRef][PubMed]
    [Google Scholar]
  81. Mayer JJ, Brisbin IL. Wild Pigs in the United States: Their History, Comparative Morphology, and Current Status University of Georgia Press; 2008
    [Google Scholar]
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