Coral Reefs

, Volume 38, Issue 6, pp 1097–1106 | Cite as

Characterisation of coral-associated bacterial communities in an urbanised marine environment shows strong divergence over small geographic scales

  • Benjamin J. WainwrightEmail author
  • Lutfi Afiq-Rosli
  • Geoffrey L. Zahn
  • Danwei Huang


The coral holobiont contains a diverse community of bacteria that have been widely acknowledged as a major contributor in the maintenance of host health and in promoting reef resilience under changing environments. However, little is known regarding the spatial distribution of these communities or the processes and mechanisms that are responsible for creating these patterns. Here we show that bacterial communities associated with the reef-building coral, Pocillopora acuta, from nine offshore islands in an urbanised coral reef ecosystem (Singapore) can diverge sharply and are significantly different among sampling locations. We suggest that small-scale environmental factors such as prevailing surface currents and wind direction, even over short distances (< 1 km), are responsible for generating bacterial community structure. Considering the sharp differentiation we observe among bacterial communities from different sites, we recommend that future coral reef restoration projects consider the microbial aspect of the coral holobiont as this may affect the success of coral transplants in recipient populations.


Coral reef Singapore 16S Holobiont Dispersal Southeast Asia 



This research is supported by the National Research Foundation, Prime Minister’s Office, Singapore under its Marine Science R&D Programme (MSRDP-P03).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

338_2019_1837_MOESM1_ESM.xlsx (4.7 mb)
Supplementary file1 (XLSX 4828 kb)


  1. Agogué H, Lamy D, Neal PR, Sogin ML, Herndl GJ (2011) Water mass specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Mol Ecol 20:258–274CrossRefGoogle Scholar
  2. Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M, Gates RD, Padilla-Gamiño JL, Spalding HL, Smith C, Woolsey ES, Bourne DG, Bongaerts P, Hoegh-Guldberg O, Leggat W (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274. CrossRefGoogle Scholar
  3. Albright MBN, Martiny JB (2018) Dispersal alters bacterial diversity and composition in a natural community. ISME 12:296–299. CrossRefGoogle Scholar
  4. Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174. CrossRefPubMedGoogle Scholar
  5. Bulan DE, Wilantho A, Krainara P, Viyakarn V, Chavanich S, Somboonna N (2018) Spatial and seasonal variability of reef bacterial communities in the upper Gulf of Thailand. Front Mar Sci 5:441. CrossRefGoogle Scholar
  6. Burke L, Selig E, Spalding M (2002) Reefs at Risk in Southeast Asia. World Resources Institute, Washington, DC, 72 pp.Google Scholar
  7. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High resolution sample inference from Illumina amplicon data. Nat Meth 13:581–583. CrossRefGoogle Scholar
  8. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Noah Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522. CrossRefPubMedGoogle Scholar
  9. Charpy L, Casareto BE, Langlade MJ, Suzuki J (2012) Cyanobacteria in coral reef ecosystems: a review. J Mar Biol 259571. Scholar
  10. Chou LM, Huang D, Tan KS, Toh TC, Goh BPL, Tun K (2019) Singapore. In: Sheppard CRC (Ed), World Seas: An Environmental Evaluation. Volume II: The Indian Ocean to the Pacific. Academic Press, London, pp. 539–558. CrossRefGoogle Scholar
  11. Chow WTL, Cheong BD, Ho BH (2016) A multimethod approach towards assessing urban flood patterns and its associated vulnerabilities in Singapore. Adv Meteorol 7159132. CrossRefGoogle Scholar
  12. Chow GSE, Samuel Chan YK, Jain SS, Huang D (2019) Light limitation selects for depth generalists in urbanised reef coral communities. Mar Environ Res 147:101–112. CrossRefPubMedGoogle Scholar
  13. Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:D169–D172. CrossRefPubMedGoogle Scholar
  14. Daniels CA, Zeifman A, Heym K, Ritchie KB, Watson CA, Berzins I, Breitbart M (2011) Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis. Mar Ecol Prog Ser 426:29–40. CrossRefGoogle Scholar
  15. Davis NM, Proctor D, Holmes SP, Relman DA, Callahan BJ (2017) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6:226. CrossRefGoogle Scholar
  16. de Castro AP, Araújo SD Jr, Reis AM, Moura RL, Francini-Filho RB, Pappas G Jr, Rodrigues TB, Thompson FL, Krüger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismiliahispida from eastern Brazil. Microb Ecol 59:658–657. CrossRefPubMedGoogle Scholar
  17. Frias-Lopez J, Bonheyo GT, Jin Q, Fouke BW (2016) Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific reefs. Appl Environ Micro 69:2409–2413. CrossRefGoogle Scholar
  18. Galand PE, Potvin M, Casamayor EO, Lovejoy C (2009) Hydrography shapes bacterial biogeography of the deep Arctic Ocean. Nature 4:564–576Google Scholar
  19. Garrison VH, Shinn EA, Foreman WT, Griffin DW, Holmes CW, Kellogg CA, Majewski MS, Richardson LL, Ritchie KB, Smith GW (2003) African and Asian dust: from desert soils to coral reefs. Bioscience 53:469–480. CrossRefGoogle Scholar
  20. Gin KYH, Lin X, Zhang S (2000) Dynamics and size structure of phytoplankton in the coastal waters of Singapore. J Plankton Res 22:1465–1485. CrossRefGoogle Scholar
  21. Griffin DW, Garrison VH, Herman JR, Shinn EA (2001) African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia 17:203–213CrossRefGoogle Scholar
  22. Guest JR, Tun K, Low J, Vergés A, Vergés A, Marzinelli EM, Campbell AH, Campbell AH, Bauman AG, Feary DA, Chou LM, Steinberg PD, Steinberg PD (2016) 27 years of benthic and coral community dynamics on turbid, highly urbanised reefs off Singapore. Sci Rep 6:36260. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hamonts K, Bissett A, Macdonald BCT, Barton PS, Manning AD, Young A (2017) Effects of ecological restoration on soil microbial diversity in a temperate grassy woodland. Appl Soil Ecol 117:117–128. CrossRefGoogle Scholar
  24. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol. 10:497–506. CrossRefPubMedGoogle Scholar
  25. Heery EC, Hoeksema BW, Browne NK, Reimer JD, Ang PO, Huang D, Friess DA, Chou LM, Loke LHL, Saksena-Taylor P, Alsagoff N, Yeemin T, Sutthacheep M, Vo ST, Bos AR, Gumanao GS, Syed Hussein MA, Waheed Z, Lane DJW, Johan O, Kunzmann A, Jompa J, Suharsono Taira D, Bauman AG, Todd PA (2018) Urban coral reefs: degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia. Mar Pollut Bull 135:654–681. CrossRefPubMedGoogle Scholar
  26. Hilton MJ, Manning SS (1995) Conversion of coastal habitats in Singapore: indications of unsustainable development. Environ Conserv 22:307–322. CrossRefGoogle Scholar
  27. (accessed 03 Aug 2018)
  28. Huang D, Tun KPP, Chou LM, Todd PA (2009) An inventory of zooxanthellate scleractinian corals in Singapore including 33 new records. Raffles Bull Zool S22:69–80Google Scholar
  29. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000CrossRefGoogle Scholar
  30. Low JKY, Chou LM (1994) Coral reef fish communities in a sediment stressed environment. Fourth LIPI-JSPS Joint Seminar on Marine Science, Jakarta 15–18 November 1994, pp. 91–99Google Scholar
  31. Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Meth 10:999–1002. CrossRefGoogle Scholar
  32. Marrs RH (2016) Soil microbes call the shots. Nat Plants 1:1–2. CrossRefGoogle Scholar
  33. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal 17:10–12. CrossRefGoogle Scholar
  34. McMurdie PJ, Holmes S (2013) Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  37. O’Malley MA (2008) ‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences. 39:314–325. CrossRefGoogle Scholar
  38. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: Community Ecology Package (Version 2.4-0). Retrieved from Accessed 20 June 2019
  39. Peixoto RS, Rosado PM, Leite DCA, Rosado AS, Bourne DG (2017) Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol 8:341. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, Vega Thurber RL, Zaneveld JR (2018) Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat Comm 9:4921. CrossRefGoogle Scholar
  41. Pootakham W, Mhuantong W, Yoocha T, Putchim L, Sonthirod C, Naktang C, Thongtham N, Tangphatsornruang S (2017) High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci Rep 7:2774. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Poquita-Du RC, Ng CSL, Loo JB, Afiq-Rosli L, Tay YC, Todd PA, Chou LM, Huang D (2017) New evidence shows that Pocilloporadamicornis-like” corals in Singapore are actually Pocillopora acuta (Scleractinia: Pocilloporidae). Biodivers Data J 5:e11407. CrossRefGoogle Scholar
  43. Poquita-Du RC, Quek ZBR, Jain SS, Schmidt-Roach S, Tun K, Heery EC, Chou LM, Todd PA, Huang D (2019) Last species standing: loss of Pocilloporidae corals associated with coastal urbanization in a tropical city state. Mar Biodivers. CrossRefGoogle Scholar
  44. Pratte ZA, Longo GO, Burns SA, Hay ME, Stewart FJ (2017) Contact with turf algae alters the coral microbiome: contact versus systemic impacts. Coral Reefs 37:1–13. CrossRefGoogle Scholar
  45. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596. CrossRefGoogle Scholar
  46. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 20 June 2019
  47. Rinkevich B (2014) Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Curr Opin Environ Sustain 7:28–36. CrossRefGoogle Scholar
  48. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of miroorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. CrossRefPubMedGoogle Scholar
  49. Schliep KP (2011) Phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593. CrossRefPubMedGoogle Scholar
  50. Shelyakin PV, Garushyants SK, Nikitin MA, Mudrova SV, Berumen M, Speksnijder AGCL, Hoeksema BW, Fontaneto D, Gelfand MS, Ivanenko VN (2018) Microbiomes of gall-inducing copepod crustaceans from the corals Stylophora pistillata (Scleractinia) and Gorgonia ventalina (Alcyonacea). Sci Rep 8:11563. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sherwood AR, Dittbern MN, Johnston ET, Conklin KY (2016) A metabarcoding comparison of windward and leeward airborne algal diversity across the Ko‘olau mountain range on the island of O'ahu, Hawai‘i. J Phycol 53:437–445. CrossRefGoogle Scholar
  52. Sin TM, Ang HW, Buurman J, Lee AC, Leong YL, Ooi SK, Steinberg P, Teo SL (2016) The urban marine environment of Singapore. Reg Stud Mar Sci 8:331–339. CrossRefGoogle Scholar
  53. Taira D, Poquita-Du RC, Toh TC, Toh KB, Ng CSL, Afiq-Rosli L, Chou LM, Song T (2018) Spatial variability of fish communities in a highly urbanised reef system. Urban Ecosyst 21:85–95. CrossRefGoogle Scholar
  54. Tanzil JTI, Goodkin NF, Sin TM, Chen MT, Fabbro GN, Boyle EA, Lee AC, Toh KB (2019) Multi-colony coral skeletal Ba/Ca from Singapore’s turbid urban reefs: Relationship with contemporaneous in-situ seawater parameters. Geochim Cosmochim Acta 250:191–208. CrossRefGoogle Scholar
  55. Timm J, Kochzius M, Madduppa HH, Neuhaus AI, Dohna T (2017) Small scale genetic population structure of coral reef organisms in Spermonde Archipelago. Indonesia. Front Mar Sci 4:294. CrossRefGoogle Scholar
  56. Tun KPP (2012) Optimisation of Reef Survey Methods and Application of Reef Metrics and Biocriteria for the Monitoring of Sediment-Impacted Reefs. PhD Thesis, Department of Biological Sciences, National University of SingaporeGoogle Scholar
  57. Vos M, Wolf BA, Jennings SJ, Kowalchuk GA (2013) Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol Rev 37:936–954. CrossRefPubMedGoogle Scholar
  58. Wainwright BJ, Zahn GL, Spalding HL, Sherwood AR, Smith CM, Amend AS (2017) Fungi associated with mesophotic macroalgae from the Au‘au Channel, west Maui are differentiated by host and overlap terrestrial communities. PeerJ 5:e3532. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wainwright BJ, Zahn GL, Arlyza IS, Amend AS (2018) Seagrass-associated fungal communities follow Wallace’s line, but host genotype does not structure fungal community. J Biogeogr 45:762–770. CrossRefGoogle Scholar
  60. Wainwright BJ, Arlyza IS, Karl SA (2019) Population genetics of the collector urchin, Tripneustes gratilla, in the Indonesian archipelago. Mar Ecol 39:e12530. CrossRefGoogle Scholar
  61. Wright ES (2016) Using DECIPHER v2.0 to analyze big biological sequence data in R. R J 8:352–359CrossRefGoogle Scholar
  62. Zahn G, Amend AS (2017) Foliar microbiome transplants confer disease resistance in a critically-endangered plant. PeerJ 5:e4020. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105:629–640. CrossRefPubMedGoogle Scholar
  64. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Comm 8:14213. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Benjamin J. Wainwright
    • 1
    Email author
  • Lutfi Afiq-Rosli
    • 1
    • 2
  • Geoffrey L. Zahn
    • 3
  • Danwei Huang
    • 1
    • 2
  1. 1.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  2. 2.Tropical Marine Science InstituteNational University of SingaporeSingaporeSingapore
  3. 3.Biology DepartmentUtah Valley UniversityOremUSA

Personalised recommendations