Energy depletion and opportunistic microbial colonisation in white syndrome lesions from corals across the Indo-Pacific
1.
Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).
ADS CAS PubMed Google Scholar
2.
Spalding, M. D. & Brown, B. E. Warm-water coral reefs and climate change. Science 350, 769–771 (2015).
ADS CAS PubMed Google Scholar
3.
Randall, C. J. & van Woesik, R. Contemporary white-band disease in Caribbean corals driven by climate change. Nat. Clim. Change 5, 375–379 (2015).
ADS Google Scholar
4.
Randall, C. J. & van Woesik, R. Some coral diseases track climate oscillations in the Caribbean. Sci. Rep. 7, 5719 (2017).
ADS CAS PubMed PubMed Central Google Scholar
5.
Maynard, J. et al. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat. Clim. Change 5, 688–694 (2015).
ADS Google Scholar
6.
Harvell, D. et al. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20, 172–195 (2007).
Google Scholar
7.
Ruiz-Moreno, D. et al. Global coral disease prevalence associated with sea temperature anomalies and local factors. Diseases Aquatic Org. 100, 249–261 (2012).
Google Scholar
8.
Willis, B. L., Page, C. A. & Dinsdale, E. A (2004) Coral disease on the great barrier reef. in Coral Health and Disease (eds. Rosenberg, E. & Loya, Y.) 69–104 (Springer, Berlin, Heidelberg, 2004). https://doi.org/10.1007/978-3-662-06414-6_3.
9.
Haapkylä, J., Seymour, A. S., Trebilco, J. & Smith, D. Coral disease prevalence and coral health in the Wakatobi Marine Park, south-east Sulawesi, Indonesia. J. Marine Biol. Assoc. UK 87, 403–414 (2007).
Google Scholar
10.
Rosenberg, E. & Loya, Y. Coral Health and Disease. (Springer-Verlag, Berlin, 2004).
11.
Aeby, G. S. Baseline levels of coral disease in the Northwestern Hawaiian Islands. Atoll Res. Bull. 543, 471–488 (2006).
Google Scholar
12.
Roff, G., Hoegh-Guldberg, O. & Fine, M. Intra-colonial response to Acroporid ‘white syndrome’ lesions in tabular Acropora spp. (Scleractinia). Coral Reefs 25, 255–264 (2006).
13.
Ainsworth, T. D., Kramasky-Winter, E., Loya, Y., Hoegh-Guldberg, O. & Fine, M. Coral disease diagnostics: what’s between a plague and a band?. Appl. Environ. Microbiol. 73, 981–992 (2007).
CAS PubMed Google Scholar
14.
Bourne, D. G., Ainsworth, T. D., Pollock, F. J. & Willis, B. L. Towards a better understanding of white syndromes and their causes on Indo-Pacific coral reefs. Coral Reefs 34, 233–242 (2015).
ADS Google Scholar
15.
Williams, G. J., Aeby, G. S., Cowie, R. O. M. & Davy, S. K. Predictive modeling of coral disease distribution within a reef system. PLoS ONE 5, e9264 (2010).
ADS PubMed PubMed Central Google Scholar
16.
Bruno, J. F. et al. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5, e124 (2007).
PubMed PubMed Central Google Scholar
17.
Selig, E. R. et al. Analyzing the Relationship Between Ocean Temperature Anomalies and Coral Disease Outbreaks at Broad Spatial Scales. in Coral Reefs and Climate Change: Science and Management (eds. Phinney, J., Hoegh-Guldberg, O., Kleypas, J., Skirving, W. & Strong, A.) (American Geophysical Union, 2006).
18.
Brodnicke, O. B. et al. Unravelling the links between heat stress, bleaching and disease: fate of tabular corals following a combined disease and bleaching event. Coral Reefs 38, 591–603 (2019).
ADS Google Scholar
19.
Sussman, M., Willis, B. L., Victor, S. & Bourne, D. G. Coral pathogens identified for White Syndrome (WS) epizootics in the Indo-Pacific. PLoS ONE 3, e2393 (2008).
ADS PubMed PubMed Central Google Scholar
20.
Sweet, M. & Bythell, J. Ciliate and bacterial communities associated with White Syndrome and Brown Band Disease in reef-building corals. Environ. Microbiol. 14, 2184–2199 (2012).
PubMed PubMed Central Google Scholar
21.
Sweet, M. & Bythell, J. White Syndrome in Acropora muricata: Nonspecific bacterial infection and ciliate histophagy. Mol. Ecol. 24, 1150–1159 (2015).
PubMed PubMed Central Google Scholar
22.
Pollock, F. J. et al. Abundance and morphology of virus-like particles associated with the coral Acropora hyacinthus differ between healthy and white syndrome-infected states. Mar. Ecol. Prog. Ser. 510, 39–43 (2014).
ADS Google Scholar
23.
Work, T. M. & Aeby, G. S. Pathology of tissue loss (white syndrome) in Acropora sp. corals from the Central Pacific. J. Invertebrate Pathol. 107, 127–131 (2011).
24.
Ainsworth, T. D., Kvennefors, E. C., Blackall, L. L., Fine, M. & Hoegh-Guldberg, O. Disease and cell death in white syndrome of Acroporid corals on the Great Barrier Reef. Mar. Biol. 151, 19–29 (2007).
Google Scholar
25.
Petes, L. E., Harvell, C. D., Peters, E., Webb, M. & Mullen, K. Pathogens compromise reproduction and induce melanization in Caribbean sea fans. Mar. Ecol. Prog. Ser. 264, 167–171 (2003).
ADS Google Scholar
26.
Brown, B. & Bythell, J. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 296, 291–309 (2005).
ADS CAS Google Scholar
27.
Toledo-Hernández, C. & Ruiz-Diaz, C. P. The immune responses of the coral. Invertebrate Surv. J. 11, 319–328 (2014).
Google Scholar
28.
Mydlarz, L. D., Fuess, L. E., Mann, W. T., Pinzón, J. H. & Gochfeld, D. J. The Cnidaria, Past, Present and Future (Springer, Berlin, 2016).
Google Scholar
29.
Miller, D. J. et al. The innate immune repertoire in cnidaria–ancestral complexity and stochastic gene loss. Genome Biol. 8, R59 (2007).
PubMed PubMed Central Google Scholar
30.
Vidal-Dupiol, J. et al. Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus. J. Exp. Biol. 214, 1533–1545 (2011).
CAS PubMed Google Scholar
31.
Wright, R. M., Aglyamova, G. V., Meyer, E. & Matz, M. V. Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus. BMC Genom. 16, 371 (2015).
Google Scholar
32.
Mydlarz, L. D. & Harvell, C. D. Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 146, 54–62 (2007).
PubMed Google Scholar
33.
Mydlarz, L. D., Jones, L. E. & Harvell, C. D. Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annu. Rev. Ecol. Evol. Syst. 37, 251–288 (2006).
Google Scholar
34.
Anderson, D. & Gilchrist, S. Development of a novel method for coral RNA isolation and the expression of a programmed cell death gene in White Plague-diseased Diploria strigosa (Dana, 1846). in Proceedings of the 11th International Coral Reef Symposium (2008).
35.
Anderson, D. A., Walz, M. E., Weil, E., Tonellato, P. & Smith, M. C. RNA-Seq of the Caribbean reef-building coral Orbicella faveolata (Scleractinia-Merulinidae) under bleaching and disease stress expands models of coral innate immunity. PeerJ 4, e1616 (2016).
PubMed PubMed Central Google Scholar
36.
Loya, Y. Skeletal regeneration in a Red Sea scleractinian coral population. Nature 261, 490–491 (1976).
ADS CAS PubMed Google Scholar
37.
Wahle, C. M. Regeneration of injuries among Jamaican gorgonians: the roles of colony physiology and environment. Biol. Bull. 165, 778–790 (1983).
PubMed Google Scholar
38.
Ward, S. The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 187, 193–206 (1995).
CAS Google Scholar
39.
Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073 (2006).
CAS PubMed Google Scholar
40.
Sheridan, C. et al. Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33, 1067–1076 (2014).
ADS Google Scholar
41.
Palmer, C. V. Immunity and the coral crisis. Commun. Biol. 1, 91 (2018).
PubMed PubMed Central Google Scholar
42.
Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. A., Grottoli, A. G. & Middlebrook, R (2011) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. J. Ecol. (2011). https://doi.org/10.1111/j.1365-2435.2008.01531.x@10.1111/(ISSN)1365-2745.VI_OA_2011.
43.
Lesser, M. P. Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things?. Coral Reefs 32, 25–33 (2013).
ADS Google Scholar
44.
Parrish, C. C. Lipids in marine ecosystems. ISRN Oceanography 604045 (2013) https://doi.org/10.5402/2013/604045.
45.
Bergé, J.-P. & Barnathan, G. Fatty acids from lipids of marine organisms: molecular biodiversity, rolesas biomarkers, biologically active compounds, and economical aspects. in Marine Biotechnology I (eds. Ulber, R. & Le Gal, Y.) 49–125 (Springer, Berlin, Heidelberg, 2005). https://doi.org/10.1007/b135782.
46.
Farre, B., Cuif, J.-P. & Dauphin, Y. Occurrence and diversity of lipids in modern coral skeletons. Zoology 113, 250–257 (2010).
PubMed Google Scholar
47.
Azeez, O. I., Meintjes, R. & Chamunorwa, J. P. Fat body, fat pad and adipose tissues in invertebrates and vertebrates: the nexus. Lipids Health Disease 13, 71 (2014).
Google Scholar
48.
Baumann, J., Grottoli, A. G., Hughes, A. D. & Matsui, Y. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J. Exp. Mar. Biol. Ecol. 461, 469–478 (2014).
CAS Google Scholar
49.
Towle, E. K., Enochs, I. C. & Langdon, C. Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE 10, e0123394 (2015).
PubMed PubMed Central Google Scholar
50.
Meesters, E. H. & Bak, R. P. M. Effects of coral bleaching on tissue regeneration potential and colony survival. Mar. Ecol. Prog. Ser. 96, 189–198 (1993).
ADS Google Scholar
51.
Mascarelli, P. E. & Bunkley-William, L. An experimental field evaluation of healing in damaged, unbleached and artificially bleached star coral, Montastraea annularis. Bull. Mar. Sci. 65, 577–586 (1999).
Google Scholar
52.
Oren, U., Rinkevich, B. & Loya, Y. Oriented intra-colonial transport of 14C labeled materials during coral regeneration. Mar. Ecol. Prog. Ser. 161, 117–122 (1997).
ADS Google Scholar
53.
Oren, U., Brickner, I. & Loya, Y. Prudent sessile feeding by the corallivore snail, Coralliophila violacea on coral energy sinks. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 2043–2050 (1998).
Google Scholar
54.
Roff, G., Hoegh-Guldberg, O. & Fine, M. Intra-colonial response to Acroporid “white syndrome” lesions in tabular Acropora spp. (Scleractinia). Coral Reefs 25, 255 (2006).
55.
Kramarsky-Winter, E. What Can Regeneration Processes Tell Us About Coral Disease? in Coral Health and Disease (eds. Rosenberg, E. & Loya, Y.) 217–230 (Springer, Berlin, Heidelberg, 2004). https://doi.org/10.1007/978-3-662-06414-6_10.
56.
Mullen, K. M., Peters, E. C. & Harvell, C. D. Coral Resistance to Disease. in Coral Health and Disease (eds. Rosenberg, E. & Loya, Y.) 377–399 (Springer, Berlin, Heidelberg, 2004). https://doi.org/10.1007/978-3-662-06414-6_22.
57.
Andersen, S. B., Vestergaard, M. L., Ainsworth, T. D., Hoegh-Guldberg, O. & Kühl, M. Acute tissue death (white syndrome) affects the microenvironment of tabular Acropora corals. Aquatic Biol. 10, 99–104 (2010).
Google Scholar
58.
Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).
CAS PubMed Google Scholar
59.
Bourne, D. G. et al. Microbial disease and the coral holobiont. Trends Microbiol. 17, 554–562 (2009).
CAS PubMed Google Scholar
60.
Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1–14 (2006).
ADS CAS Google Scholar
61.
Shnit-Orland, M. & Kushmaro, A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol. Ecol. 67, 371–380 (2009).
CAS PubMed Google Scholar
62.
Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).
CAS PubMed Google Scholar
63.
Sweet, M. J. & Bulling, M. T. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4, 9 (2017).
Google Scholar
64.
Egan, S. & Gardiner, M. Microbial dysbiosis: rethinking disease in marine ecosystems. Front. Microbiol. 7, 991 (2016).
PubMed PubMed Central Google Scholar
65.
Sweet, M. et al. Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease. Microbiome 7, 139 (2019).
PubMed PubMed Central Google Scholar
66.
Kvennefors, E. C. E. et al. Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev. Comp. Immunol. 34, 1219–1229 (2010).
CAS PubMed Google Scholar
67.
Connelly, M. T., McRae, C. J., Liu, P.-J. & Traylor-Knowles, N. Lipopolysaccharide treatment stimulates Pocillopora coral genotype-specific immune responses but does not alter coral-associated bacteria communities. Dev. Comp. Immunol. 109, 103717 (2020).
CAS PubMed Google Scholar
68.
Pollock, F. J., Wada, N., Torda, G., Willis, B. L. & Bourne, D. G. White syndrome-affected corals have a distinct microbiome at disease lesion fronts. Appl. Environ. Microbiol. 83, e02799-e2816 (2017).
PubMed Google Scholar
69.
Wada, N. et al. In situ visualization of bacterial populations in coral tissues: pitfalls and solutions. PeerJ 4, e2424 (2016).
PubMed PubMed Central Google Scholar
70.
Daims, H., Brühl, A., Amann, R., Schleifer, K. H. & Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434–444 (1999).
CAS PubMed Google Scholar
71.
Wallner, G., Amann, R. & Beisker, W. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136–143 (1993).
CAS PubMed Google Scholar
72.
Zack, G. W., Rogers, W. E. & Latt, S. A. Automatic measurement of sister chromatid exchange frequency. J. Histochem. Cytochem. 25, 741–753 (1977).
CAS PubMed Google Scholar
73.
Conlan, J. A., Jones, P. L., Turchini, G. M., Hall, M. R. & Francis, D. S. Changes in the nutritional composition of captive early-mid stage Panulirus ornatus phyllosoma over ecdysis and larval development. Aquaculture 434, 159–170 (2014).
CAS Google Scholar
74.
Parrish, C. C., Bodennec, G. & Gentien, P. Determination of glycoglycerolipids by Chromarod thin-layer chromatography with Iatroscan flame ionization detection. J. Chromatogr. A 741, 91–97 (1996).
CAS Google Scholar
75.
Christie, W. W. & Han, X. Lipid Analysis: Isolation, separation, identification and lipidomic analysis (Woodhead Publishing Limited, Cambridge, 2010).
Google Scholar
76.
Ackman, R. G. The gas chromatograph in practical analyses of common and uncommon fatty acids for the 21st century. Anal. Chim. Acta 465, 175–192 (2002).
CAS Google Scholar
77.
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2016).
78.
RStudio: Integrated development environment for R 0.99.903. (2015).
79.
de Mendiburu, F. Statistical Procedures for Agricultural Research. (2019).
80.
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, New York, 2016).
Google Scholar
81.
Handl, S., Dowd, S. E., Garcia-Mazcorro, J. F., Steiner, J. M. & Suchodolski, J. S. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol. Ecol. 76, 301–310 (2011).
CAS PubMed Google Scholar
82.
Suchodolski, J. S. et al. The effect of the macrolide antibiotic tylosin on microbial diversity in the canine small intestine as demonstrated by massive parallel 16S rRNA gene sequencing. BMC Microbiol. 9, 210 (2009).
PubMed PubMed Central Google Scholar
83.
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).
CAS PubMed PubMed Central Google Scholar
84.
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
CAS PubMed PubMed Central Google Scholar
85.
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acids Res. 41, D590–D596 (2013).
CAS PubMed Google Scholar
86.
Anderson, M., Gorley, R. N. & Clarke, R. K. Permanova+ for Primer: Guide to Software and Statistical Methods. (Primer-E Limited, 2008).
87.
Clarke, K. R. & Gorley, R. N. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research) (Primer-E Ltd, Plymouth, 2006).
Google Scholar
88.
Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46 (2001).
Google Scholar
89.
Morton, J. T. et al. Balance Trees Reveal Microbial Niche Differentiation. mSystems 2, e00162-16 (2017).
90.
Dixon, P. & Palmer, M. W. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
Google Scholar
91.
Kolde, R. Pretty Heatmaps. (2018).
92.
Martinez Arbizu, P. pairwiseAdonis: Pairwise multilevel comparison using adonis. (2019).
93.
Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. emmeans: Estimated Marginal Means, aka Least-Square Means. (2019).
94.
Graves, S., Piepho, H.-P. & Selzer, L. multcompView: Visualizations of Paired Comparisons. (2015).
95.
Wada, N. et al. Characterization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. Sci. Rep. 9, 14662 (2019).
ADS PubMed PubMed Central Google Scholar
96.
Sunagawa, S. et al. Bacterial diversity and White Plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512–521 (2010).
Google Scholar
97.
Cárdenas, A., Rodriguez-R, L. M., Pizarro, V., Cadavid, L. F. & Arévalo-Ferro, C. Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease. ISME J. 6, 502–512 (2012).
PubMed Google Scholar
98.
Mydlarz, L. D., Holthouse, S. F., Peters, E. C. & Harvell, C. D. Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS ONE 3, e1811 (2008).
ADS PubMed PubMed Central Google Scholar
99.
Palmer, C. V. & Traylor-Knowles, N. Towards an integrated network of coral immune mechanisms. Proc. R. Soc. B: Biol. Sci. 279, 4106–4114 (2012).
CAS Google Scholar
100.
Fang, L., Chen, Y. J. & Chen, C. Why does the white tip of stony coral grow so fast without zooxanthellae?. Mar. Biol. 103, 359–363 (1989).
Google Scholar
101.
Conlan, J. A., Humphrey, C. A., Severati, A. & Francis, D. S. Intra-colonial diversity in the scleractinian coral, Acropora millepora: identifying the nutritional gradients underlying physiological integration and compartmentalised functioning. PeerJ 6, e4239 (2018).
PubMed PubMed Central Google Scholar
102.
Dodds, L. A., Black, K. D., Orr, H. & Roberts, J. M. Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar. Ecol. Prog. Ser. 397, 113–124 (2009).
ADS CAS Google Scholar
103.
Harriott, V. J. Coral lipids and environmental stress. Environ. Monit. Assess. 25, 131–139 (1993).
CAS PubMed Google Scholar
104.
Grottoli, A. G. & Rodrigues, L. J. Bleached Porites compressa and Montipora capitata corals catabolize δ13C-enriched lipids. Coral Reefs 30, 687 (2011).
ADS Google Scholar
105.
Rodrigues, L. J., Grottoli, A. G. & Pease, T. K. Lipid class composition of bleached and recoveringPorites compressaDana 1846 andMontipora capitataDana, 1846 corals from Hawaii. J. Exp. Mar. Biol. Ecol. 358, 136–143 (2008).
CAS Google Scholar
106.
Figueiredo, J. et al. Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31, 613–619 (2012).
ADS Google Scholar
107.
Pollock, F. J. et al. Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals. R. Soc. Open Sci. 6, 190355 (2019).
ADS CAS PubMed PubMed Central Google Scholar
108.
Stanley, D. W. Eicosanoids in Invertebrate Signal Transduction Systems (Princeton University Press, Princeton, 2014).
Google Scholar
109.
Dennis, E. A. & Norris, P. C. Eicosanoid storm in infection and inflammation. Nat. Rev. Immunol. 15, 511–523 (2015).
CAS PubMed PubMed Central Google Scholar
110.
Kaur, G., Cameron-Smith, D., Garg, M. & Sinclair, A. J. Docosapentaenoic acid (22:5n–3): a review of its biological effects. Prog. Lipid Res. 50, 28–34 (2011).
CAS PubMed Google Scholar
111.
Ushijima, B. et al. Mutation of the toxR or mshA genes from Vibrio coralliilyticus strain OCN014 reduces infection of the coral Acropora cytherea. Environ. Microbiol. 18, 4055–4067 (2016).
CAS PubMed Google Scholar
112.
Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 17121 (2017).
CAS PubMed Google Scholar
113.
Flanagan, J. L. et al. Loss of bacterial diversity during antibiotic treatment of intubated patients colonized with Pseudomonas aeruginosa. J. Clin. Microbiol. 45, 1954–1962 (2007).
CAS PubMed PubMed Central Google Scholar
114.
Roder, C. et al. Bacterial profiling of White Plague disease in a comparative coral species framework. ISME J.l 8, 31–39 (2014).
CAS Google Scholar
115.
Sekar, R., Mills, D. K., Remily, E. R., Voss, J. D. & Richardson, L. L. Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl. Environ. Microbiol. 72, 5963–5973 (2006).
CAS PubMed PubMed Central Google Scholar
116.
Meyer, J. L., Paul, V. J. & Teplitski, M. Community shifts in the surface microbiomes of the coral Porites astreoides with Unusual Lesions. PLoS ONE 9, e100316 (2014).
ADS PubMed PubMed Central Google Scholar
117.
Apprill, A., Hughen, K. & Mincer, T. Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ. Microbiol. 15, 2063–2072 (2013).
CAS PubMed Google Scholar
118.
Mouchka, M. E., Hewson, I. & Harvell, C. D. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 50, 662–674 (2010).
PubMed Google Scholar
119.
Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The Microbial Signature Provides Insight into the Mechanistic Basis of Coral Success across Reef Habitats. mBio 7, e00560–16 (2016).
120.
Reis, A. M. M. et al. Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis. J. Appl. Microbiol. 106, 1378–1387 (2009).
CAS PubMed Google Scholar
121.
Morrow, K. M., Moss, A. G., Chadwick, N. E. & Liles, M. R. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl. Environ. Microbiol. 78, 6438–6449 (2012).
CAS PubMed PubMed Central Google Scholar
122.
Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. 105, 629–640 (2016).
CAS PubMed Google Scholar
123.
Meron, D. et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51–60 (2011).
PubMed Google Scholar
124.
Meron, D. et al. Changes in coral microbial communities in response to a natural pH gradient. ISME J. 6, 1775–1785 (2012).
CAS PubMed PubMed Central Google Scholar
125.
Frias-Lopez, J., Zerkle, A. L., Bonheyo, G. T. & Fouke, B. W. Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl. Environ. Microbiol. 68, 2214–2228 (2002).
CAS PubMed PubMed Central Google Scholar
126.
Webster, N. S., Xavier, J. R., Freckelton, M., Motti, C. A. & Cobb, R. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ. Microbiol. 10, 3366–3376 (2008).
CAS PubMed Google Scholar
127.
Pantos, O. & Bythell, J. C. Bacterial community structure associated with white band disease in the Elkhorn coral Acropora palmata determined using culture-independent 16S rRNA techniques. Diseases Aquat. Org. 69, 79–88 (2006).
CAS Google Scholar
128.
de Castro, A. P. et al. Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from Eastern Brazil. Microb. Ecol. 59, 658–667 (2010).
PubMed Google Scholar
129.
Garcia, G. D. et al. Metagenomic analysis of healthy and white plague-affected Mussismilia braziliensis corals. Microb. Ecol. 65, 1076–1086 (2013).
PubMed Google Scholar
130.
Cottrell, M. T. & Kirchman, D. L. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66, 1692–1697 (2000).
CAS PubMed PubMed Central Google Scholar
131.
Peixoto, R. S., Rosado, P. M., Leite, D. C. de A., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 341 (2017).
132.
Raina, J.-B., Tapiolas, D., Willis, B. L. & Bourne, D. G. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 75, 3492–3501 (2009).
CAS PubMed PubMed Central Google Scholar
133.
Todd, J. D. et al. Molecular dissection of bacterial acrylate catabolism–unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Environ. Microbiol. 12, 327–343 (2010).
CAS PubMed Google Scholar
134.
Pisapia, C., Anderson, K. & Pratchett, M. S. Intraspecific Variation in Physiological Condition of Reef-Building Corals Associated with Differential Levels of Chronic Disturbance. PLoS One 9, (2014).
135.
Towle, E. K. Heterotrophy and lipids as indicators of resilience to climate change stress in scleractinian corals. (University of Miami, 2015). More