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Early Life Stages of a Common Broadcast Spawning Coral Associate with Specific Bacterial Communities Despite Lack of Internalized Bacteria

  • Invertebrate Microbiology
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Abstract

Coral-associated bacteria are critical for the well-being of their host and may play essential roles during ontogeny, as suggested by the vertical transmission of some bacteria in brooding corals. Bacterial acquisition patterns in broadcast spawners remain uncertain, as 16S rRNA gene metabarcoding of coral early life stages suggests the presence of bacterial communities, which have not been detected by microscopic examinations. Here, we combined 16S rRNA gene metabarcoding with fluorescence in situ hybridization (FISH) microscopy to analyze bacterial assemblages in Acropora tenuis egg–sperm bundles, embryos, and larvae following a spawning event. Metabarcoding results indicated that A. tenuis offspring ≤ 4-day-old were associated with diverse and dynamic bacterial microbiomes, dominated by Rhodobacteraceae, Alteromonadaceae, and Oceanospirillaceae. While FISH analyses confirmed the lack of internalized bacteria in A. tenuis offspring, metabarcoding showed that even the earliest life stages examined (egg–sperm bundles and two-cell stages) were associated with a diverse bacterial community, suggesting the bacteria were confined to the mucus layer. These results can be explained by vertical transmission of certain taxa (mainly Endozoicomonas) in the mucus surrounding the gametes within bundles, or by horizontal bacterial transmission through the release of bacteria by spawning adults into the water column.

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Availability of Data and Material

The sequence data generated and analyzed in this study are available at NCBI under http://www.ncbi.nlm.nih.gov/bioproject/517286, BioProject accession PRJNA517286.

References

  1. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919–1925

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46

    Google Scholar 

  3. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253

    Article  PubMed  Google Scholar 

  4. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9:683–693

    PubMed  Google Scholar 

  5. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 3:e2836

    PubMed  PubMed Central  Google Scholar 

  6. Apprill A, Marlow HQ, Martindale MQ, Rappe MS (2009) The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3:685–699

    PubMed  Google Scholar 

  7. Apprill A, Marlow HQ, Martindale MQ, Rappe MS (2012) Specificity of associations between bacteria and the coral Pocillopora meandrina during early development. Appl. Environ. Microbiol. 78:7467–7475

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of Scleractinian corals. Annu. Rev. Ecol. Evol. Syst. 40:551–571

    Google Scholar 

  9. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change: shifting to new algal symbionts may safeguard devastated reefs from extinction. Nature 430:741

    CAS  PubMed  Google Scholar 

  10. Bayer T, Neave MJ, Alsheikh-Hussain A, Adanda M, Yum LK, Mincer T, Hughen K, Apprill A, Voolstra CR (2013) The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79:4759–4762

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57:289–300

    Google Scholar 

  12. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc Biol Sci / R Soc 273:2305–2312

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  14. Blackall LL, Wilson B, van Oppen MJ (2015) Coral—the world’s most diverse symbiotic ecosystem. Mol. Ecol. 24:5330–5347

    PubMed  Google Scholar 

  15. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10:57–59

    CAS  PubMed  Google Scholar 

  16. Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM, van Oppen MJ (2016) Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J 10:2693–2701

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70:317–340

    CAS  PubMed  Google Scholar 

  18. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:1–8

    Google Scholar 

  19. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13:581–583

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME journal 11:2639–2643

    PubMed  PubMed Central  Google Scholar 

  21. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley S, Knights D, Koening JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Ceh J, Raina JB, Soo RM, van Keulen M, Bourne DG (2012) Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef. PLoS One 7:e36920

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Ceh J, van Keulen M, Bourne DG (2013a) Intergenerational transfer of specific bacteria in corals and possible implications for offspring fitness. Microb. Ecol. 65:227–231

    CAS  PubMed  Google Scholar 

  24. Ceh J, Kilburn MR, Cliff JB, Raina J-B, van Keulen M, Bourne DG (2013b) Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol 3:2393–2400

    Google Scholar 

  25. Chiu H-H, Mette A, Shiua J-H, Tang SL (2012) Bacterial distribution in the epidermis and mucus of the coral Euphyllia glabrescens by CARD-FISH. Zool Stud. 51:1332–1342

    CAS  Google Scholar 

  26. Courtesy of Integration and Application Network , IAN Symbol Libraries, ian.umces.edu/symbols/ Accessed 2018

  27. Damjanovic K, van Oppen MJH, Menéndez P, Blackall LL, (2019) Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea. Front Microbiol 10:1702

  28. 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

    Google Scholar 

  29. De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    PubMed  Google Scholar 

  30. Durante MK, Baums IB, Williams DE, Vohsen S, Kemp DW (2019) What drives phenotypic divergence among coral clonemates of Acropora palmata? Mol. Ecol. 28(13):3208–3322

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Epstein H, Torda G, Munday PL, van Oppen MJH (2019) Parental and early life stage environments drive establishment of bacterial and dinoflagellate communities in a common coral. ISME J 13:1635–1638

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Frade PR, Roll K, Bergauer K, Herndl GJ (2016) Archaeal and bacterial communities associated with the surface mucus of Caribbean corals differ in their degree of host specificity and community turnover over reefs. PLoS One 11:e0144702

    PubMed  PubMed Central  Google Scholar 

  33. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, pp 59–85

  34. Harrison PL, Booth DJ (2007) Coral reefs: naturally dynamic and increasingly disturbed ecosystems. In: Connell SD, Gillanders BM (eds) Marine ecology. Oxford University Press, Melbourne, pp 316–377

    Google Scholar 

  35. Herve M (2018) RVAideMemoire: testing and plotting procedures for biostatistics. R package version 0.9–69

  36. Hoegh-Guldberg O (2011) The impact of climate change on coral reef ecosystems. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, pp 391–403

  37. Hoegh-Guldberg O, Kennedy EV, Beyer HL, McClennen C, Possingham HP (2018) Securing a long-term future for coral reefs. Trends Ecol Evol 33(12):936–944

    PubMed  Google Scholar 

  38. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom. J. 50:346–363

    PubMed  Google Scholar 

  39. Hugenholtz P, Tyson GW, Blackall LL (2002) Design and evaluation of 16S rRNA-targeted oligonucleotide probes for fluorescence in situ hybridization. Methods Mol. Biol. 179:29–42

    CAS  PubMed  Google Scholar 

  40. Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Methods Enzymol. 397:292–308

    CAS  PubMed  Google Scholar 

  41. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Hobbs J-PA, Hoey AS, Hoogenboom MO, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    CAS  PubMed  Google Scholar 

  42. Johansson ME, Hansson GC (2012) Preservation of mucus in histological sections, immunostaining of mucins in fixed tissue, and localization of bacteria with FISH. Methods Mol Biol 842:229–235

    CAS  PubMed  Google Scholar 

  43. Lande R (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76:5–13

    Google Scholar 

  44. Lee MD, Walworth NG, Sylvan JB, Edwards KJ, Orcutt BN (2015) Microbial communities on seafloor basalts at Dorado Outcrop reflect level of alteration and highlight global lithic clades. Front Microbiol 6:1470

    PubMed  PubMed Central  Google Scholar 

  45. Legendre P, Legendre L (1998) Numerical ecology (developments in environmental modelling). Elsevier Science

  46. Leite DCA, Leao P, Garrido AG, Lins U, dos Santos HF, Pires DO, Castro CB, van Elsas JD, Zilberberg C, Rosado AS, Peixoto RS (2017) Broadcast spawning coral Mussismilia hispida can vertically transfer its associated bacterial core. Front Microbiol 8:1–12

    Google Scholar 

  47. Lema KA, Bourne DG, Willis BL (2014) Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora. Mol. Ecol. 23:4682–4695

    CAS  PubMed  Google Scholar 

  48. Lema KA, Clode PL, Kilburn MR, Thornton R, Willis BL, Bourne DG (2016) Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora. ISME J 10:1804–1808

    CAS  PubMed  Google Scholar 

  49. Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152

    CAS  Google Scholar 

  50. Littman RA, Willis BL, Bourne DG (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389:45–59

    Google Scholar 

  51. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550

    PubMed  PubMed Central  Google Scholar 

  52. McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, Wilke A, Huse S, Hufnagle J, Meyer F, Knight R, Caporaso JG (2012) The biological observation matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. GigaScience 1:1–6

    Google Scholar 

  53. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Muscatine L, Porter JW (1977) Reef corals—mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Google Scholar 

  55. Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215

    CAS  PubMed  Google Scholar 

  56. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson CL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2016) Vegan: community ecology package. R package version 2.4–1

  57. Padilla-Gamiño JL, Weatherby TM, Waller RG, Gates RD (2010) Formation and structural organization of the egg–sperm bundle of the scleractinian coral Montipora capitata. Coral Reefs 30:371–380

    Google Scholar 

  58. Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, Vega Thurber R, Zaneveld JR (2018) Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9:1–13

    CAS  Google Scholar 

  59. Porter TM, Hajibabaei M (2018) Scaling up: a guide to high-throughput genomic approaches for biodiversity analysis. Mol. Ecol. 27:313–338

    PubMed  Google Scholar 

  60. QIIME 2 Development Team, QIIME 2, https://docs.qiime2.org Accessed 2017a

  61. QIIME 2 Development Team, q2-demux, https://github.com/qiime2/q2-demux Accessed 2017b

  62. QIIME 2 Development Team, q2-feature-classifier, https://github.com/qiime2/q2-feature-classifier Accessed 2017c

  63. QIIME 2 Development Team, q2-taxa, https://github.com/qiime2/q2-taxa Accessed 2017d

  64. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596

    CAS  PubMed  Google Scholar 

  65. R Core Team, R: a language and environment for statistical computing. http://www.R-project.org. Accessed 2018

  66. Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Raina JB, Clode PL, Cheong S, Bougoure J, Kilburn MR, Reeder A, Foret S, Stat M, Beltran V, Thomas-Hall P, Tapiolas D, Motti CM, Gong B, Pernice M, Marjo CE, Seymour JR, Willis BL, Bourne DG (2017) Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. eLIFE 6:e23008

    PubMed  PubMed Central  Google Scholar 

  68. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ. Microbiol. 8:2068–2073

    CAS  PubMed  Google Scholar 

  69. Ricardo GF, Jones RJ, Negri AP, Stocker R (2016a) That sinking feeling: suspended sediments can prevent the ascent of coral egg bundles. Sci. Rep. 6:21567

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Ricardo GF, Jones RJ, Clode PL, Negri AP (2016b) Mucous secretion and cilia beating defend developing coral larvae from suspended sediments. PLoS One 11:e0162743

    PubMed  PubMed Central  Google Scholar 

  71. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    CAS  Google Scholar 

  72. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Google Scholar 

  73. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    CAS  PubMed  Google Scholar 

  74. Röthig T, Ochsenkuhn MA, Roik A, van der Merwe R, Voolstra CR (2016) Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25:1308–1323

    PubMed  PubMed Central  Google Scholar 

  75. Salter SS, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12:1–12

    Google Scholar 

  76. Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ (2010) Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS One 5:e10898

    PubMed  PubMed Central  Google Scholar 

  77. Sharp KH, Distel D, Paul VJ (2012) Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J 6:790–801

    CAS  PubMed  Google Scholar 

  78. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380

    CAS  PubMed  Google Scholar 

  79. Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5:1–7

    Google Scholar 

  80. Sweet MJ, Croquer A, Bythell JC (2010) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52

    Google Scholar 

  81. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci 112:2307–2313

    PubMed  PubMed Central  Google Scholar 

  82. Wada N, Pollock FJ, Willis BL, Ainsworth T, Mano N, Bourne DG (2016) In situ visualization of bacterial populations in coral tissues: pitfalls and solutions. PeerJ 4:e2424

    PubMed  PubMed Central  Google Scholar 

  83. Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143

    CAS  PubMed  Google Scholar 

  84. Webster NS, Reusch T (2017) Microbial contributions to the persistence of coral reefs. ISME J:1–8

  85. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vazquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27

    PubMed  PubMed Central  Google Scholar 

  86. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Google Scholar 

  87. Wickham H (2017) tidyverse: easily install and load the ‘Tidyverse’. R package version 1.2.1

  88. Zhang Y, Ling J, Yang Q, Wen C, Yan Q, Sun H, Van Nostrand JD, Shi Z, Zhou J, Dong J (2015) The functional gene composition and metabolic potential of coral-associated microbial communities. Sci. Rep. 5:16191

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Zhou G, Cai L, Yuan T, Tian R, Tong H, Zhang W, Jiang L, Guo M, Liu S, Qian PY, Huang H (2017) Microbiome dynamics in early life stages of the scleractinian coral Acropora gemmifera in response to elevated pCO2. Environ Microbiol 19:3342–3352

    CAS  PubMed  Google Scholar 

  90. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:14213

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors thank the team of the National Sea Simulator at AIMS for technical support in conducting the experiment. KD is very grateful to Dr. Naohisa Wada and Dr. Nicole Webster for extensive discussions and insights about FISH on coral samples, and also thanks Dr. David Bourne, Dr. Koty Sharp, and Dr. Kim Lema for their advice on the topic. We are grateful to Dr. Gabriela Segal for her instructions regarding the use of the confocal microscope and Zeiss software. Many thanks to Dr. Andrew Negri, Leela Chakravarti, and Lesa Peplow for their assistance during spawning, to Ashley Dungan for logistical help, and to Marie Roman for the images of adult coral and egg–sperm bundles used in Fig. 5.

Funding

This work was funded by an Australian Research Council grant (DP160101468) to van Oppen and Blackall, the Australian Institute of Marine Science (AIMS) and a Holsworth Wildlife Research Endowment (Equity Trustees Charitable Foundation & the Ecological Society of Australia). KD is the recipient of an International Postgraduate Research Scholarship and Australian Post-graduate Award (University of Melbourne). MvO acknowledges Australian Research Council Laureate Fellowship FL180100036.

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Damjanovic, K., Menéndez, P., Blackall, L.L. et al. Early Life Stages of a Common Broadcast Spawning Coral Associate with Specific Bacterial Communities Despite Lack of Internalized Bacteria. Microb Ecol 79, 706–719 (2020). https://doi.org/10.1007/s00248-019-01428-1

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