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Bacterial and algal symbiont dynamics in early recruits exposed to two adult coral species

Abstract

Corals live in a symbiotic relationship with various microorganisms including bacteria, some of which are essential for host health and survival. Bacterial assemblages are typically highly diverse in juveniles and are speculated to exert roles critical to coral ontogenetic development. However, knowledge about bacterial dynamics in coral recruits is scarce, especially in brooders. In this study, we investigated the temporal dynamics of bacterial communities associated with Pocillopora acuta early recruits exposed to different microbial environments. One week after settlement, recruits were grown in a flow-through system with 0.4 µm filtered seawater either alone, or in the vicinity of adult Pocillopora acuta or Platygyra daedalea coral fragments, which associate with different microbiomes. After 5 weeks, all corals were transferred to a mesocosm containing various marine organisms, where they were reared for another 4 weeks. In addition to observing the development of coral-associated microbial communities, we assessed whether exposing Pocillopora acuta recruits to different adult coral species influenced their bacterial communities. Our motivation was to examine whether this approach can be used to modify bacteria and Symbiodiniaceae associated with these early life stages. While adult Pocillopora acuta fragments had bacterial assemblages dominated by Endozoicomonadaceae, bacterial communities of Platygyra daedalea fragments were dominated by Flammeovirgaceae and Rhodospirillaceae. Bacterial communities associated with recruits were more diverse than those found in adults and contained larger relative abundances of Flavobacteriaceae, Rhodobacteraceae and Erythrobacteraceae. All recruits harbored the same Symbiodiniaceae type throughout the experiment (dominated by Cladocopium C1d sequences), and their bacterial communities did not differ across treatments. Instead, there was a significant change over time characterized by a decline in the relative abundance of Flavobacteriaceae and an increase in the abundance of Endozoicomonadaceae. Our findings indicate that Pocillopora acuta recruits harbor dynamic and diverse bacterial assemblages, which were not influenced by nearby adult corals in our experimental design.

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Data availability

The sequence data generated and analyzed in this study are available at NCBI under http://www.ncbi.nlm.nih.gov/bioproject/527938, BioProject accession PRJNA527938.

References

  1. Anderson CR, Condron LM, Clough TJ, Fiers M, Stewart A, Hill RA, Sherlock RR (2011) Biochar induced soil microbial community change: Implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54:309–320

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

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

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

  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

  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

  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

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

  9. 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

  10. 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. Frontiers in Microbiology 10:1529

  11. 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

  12. Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174

  13. 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

  14. Bourne DG, Dennis PG, Uthicke S, Soo RM, Tyson GW, Webster N (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7:1452–1458

  15. Brener-Raffalli K, Clerissi C, Vidal-Dupiol J, Adjeroud M, Bonhomme F, Pratlong M, Aurelle D, Mitta G, Toulza E (2018) Thermal regime and host clade, rather than geography, drive Symbiodinium and bacterial assemblages in the scleractinian coral Pocillopora damicornis sensu lato. Microbiome 6:39

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

  17. 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

  18. 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

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

  20. 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

  21. Chan WY, Peplow LM, Menendez P, Hoffmann AA, van Oppen MJH (2019) The roles of age, parentage and environment on bacterial and algal endosymbiont communities in Acropora corals. Mol Ecol

  22. Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120

  23. Damjanovic K, Blackall LL, Webster NS, van Oppen MJH (2017) The contribution of microbial biotechnology to mitigating coral reef degradation. Microb Biotechnol 10:1236–1243

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

  25. Damjanovic K, Menendez P, Blackall LL, van Oppen MJH (2019b) Early life stages of a common broadcast spawning coral associate with specific bacterial communities despite lack of internalized bacteria. Microb Ecol

  26. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Cote IM, Bellwood D (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386

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

  28. 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

  29. Gignoux-Wolfsohn SA, Vollmer SV (2015) Identification of candidate coral pathogens on white band disease-infected staghorn coral. PLoS One 10:e0134416

  30. Herve M (2018) RVAideMemoire: Testing and plotting procedures for biostatistics. R package version 0.9-69

  31. Hoey AS, Howells E, Johansen JL, Hobbs J-PA, Messmer V, McCowan DM, Wilson SK, Pratchett MS (2016) Recent advances in understanding the effects of climate change on coral reefs. Diversity 8:1–22

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

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

  34. Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, Wiedenmann J, Voolstra CR, SymPortal Framework (2019) https://github.com/didillysquat/SymPortal_framework

  35. Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, Wiedenmann J, Voolstra CR (2019b) SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour 19:1063–1080

  36. Illumina (2017) Illumina 16S metagenomic sequencing library preparation (Illumina Technical Note 15044223), http://support.illumina.com/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf

  37. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PloS One 5:1–14

  38. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161

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

  40. Legendre P, Legendre L (1998) Numerical Ecology (Developments in environmental modelling). Elsevier Science, Amsterdam

  41. Lema KA, Willis BL, Bourne DG (2014a) Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16:3345–3359

  42. Lema KA, Bourne DG, Willis BL (2014b) 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

  43. Liang J, Yu K, Wang Y, Huang X, Huang W, Qin Z, Pan Z, Yao Q, Wang W, Wu Z (2017) Distinct bacterial communities associated with massive and branching scleractinian corals and potential linkages to coral susceptibility to thermal or cold stress. Front Microbiol 8:979

  44. 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

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

  46. Magalon H, Flot J-F, Baudry E (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551–558

  47. 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

  48. McFall-Ngai MJ (2002) Unseen forces: the influence of bacteria on animal development. Dev Biol 242:1–14

  49. McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PloS one 8:e61217

  50. McNally SP, Parsons RJ, Santoro AE, Apprill A (2016) Multifaceted impacts of the stony coral Porites astreoides on picoplankton abundance and community composition. Limnology and Oceanography 62:217–234

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

  52. Neave MJ, Michell CT, Apprill A, Voolstra CR (2017) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci Rep 7:40579

  53. Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG, Apprill A, Voolstra CR (2016) Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J 11:186–200

  54. Nitschke MR, Davy SK, Ward S (2015) Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs 35:335–344

  55. 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

  56. Pantos O, Bongaerts P, Dennis PG, Tyson GW, Hoegh-Guldberg O (2015) Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9:1916–1927

  57. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078

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

  59. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc Biol Sci 279:4352–4361

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

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

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

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

  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

  65. Quigley KM, Warner PA, Bay LK, Willis BL (2018) Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity (Edinb) 121:524–536

  66. Quigley KM, Roa CA, Torda G, Bourne DG, Willis BL (2019) Co-dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles. MicrobiologyOpen (accepted)

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

  68. 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

  69. Robbins SJ, Singleton CM, Chan CX, Messer LF, Geers AU, Ying H, Baker A, Bell SC, Morrow KM, Ragan MA, Miller DJ, Foret S, ReFuGe C, Voolstra CR, Tyson GW, Bourne DG (2019) A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat Microbiol

  70. Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22:939–946

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

  72. Rosado PM, Leite DCA, Duarte GAS, Chaloub RM, Jospin G, Nunes da Rocha U, Saraiva JP, Dini-Andreote F, Eisen JA, Bourne DG, Peixoto RS (2018) Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J:1751–7370

  73. 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

  74. Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96

  75. Thompson JR, Rivera HE, Closek CJ, Medina M (2015) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4:176

  76. van Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nat Rev Microbiol 17:557–567

  77. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences 112:2307–2313

  78. 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

  79. Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York

  80. Wickham H (2017) tidyverse: Easily Install and Load the ‘Tidyverse’. R package version 1(2):1

  81. Wilkinson SP, Fisher PL, van Oppen MJH, Davy SK (2015) Intra-genomic variation in symbiotic dinoflagellates: recent divergence or recombination between lineages? BMC Evol Biol 15:46

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Acknowledgements

The authors thank the National Sea Simulator team at AIMS for their assistance with experimental setup. We also thank Bettina Glasl and Dr. Pedro Frade for their help in collecting coral colonies, Sophie Stephenson for help with recruit rearing and Lesa Peplow for support in the molecular laboratory. We are also grateful to Dr. Nicole Webster and Dr. Andrew Negri for discussions and advice about experimental design. This work was funded by an Australian Research Council grant to MvO and LB (DP160101468) and AIMS. KD is the recipient of an International Postgraduate Research Scholarship and Australian Postgraduate Award (University of Melbourne) and funded by Ecological Society of Australia (TP825824). MvO acknowledges Australian Research Council Laureate Fellowship FL180100036.

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Correspondence to Katarina Damjanovic.

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Damjanovic, K., Blackall, L.L., Menéndez, P. et al. Bacterial and algal symbiont dynamics in early recruits exposed to two adult coral species. Coral Reefs 39, 189–202 (2020). https://doi.org/10.1007/s00338-019-01871-z

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Keywords

  • Coral recruits
  • Microbial dynamics
  • Pocillopora acuta
  • Platygyra daedalea
  • Bacterial transmission