Bacterial community dynamics are linked to patterns of coral heat tolerance

Nature Communications

Volumn 8, Issue , 2017, Pages

  Ziegler, Maren ^a   Seneca, Francois O ^b   Yum, Lauren K ^a   Palumbi, Stephen R ^b   Voolstra, Christian R ^a  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BLEACHING; COMMUNITY DYNAMICS; CORAL REEF; ENVIRONMENTAL STRESS; MICROBIAL COMMUNITY; TEMPERATURE TOLERANCE; WARMING;

BLEACHING; CORAL; HABITAT; HEAT STRESS; HEAT TOLERANCE; IMMUNE RESPONSE; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; ADAPTATION; ANIMAL; ANTHOZOA; BACTERIUM; CLASSIFICATION; CORAL REEF; DNA SEQUENCE; ECOSYSTEM; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; MICROFLORA; PHYLOGENY; PHYSIOLOGY; POPULATION DYNAMICS;

ANTHOZOA; BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; RNA 16S;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; BACTERIA; BACTERIAL PROTEINS; CORAL REEFS; ECOSYSTEM; GENOTYPE; HOT TEMPERATURE; MICROBIOTA; PHYLOGENY; POPULATION DYNAMICS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; THERMOTOLERANCE;

EID: 85012050443     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14213     Document Type: Article

References (49)

1. Fraune, S. et al. Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J. 9, 1543-1556 (2015).
2. Moran, N. A. & Yun, Y. Experimental replacement of an obligate insect symbiont. Proc. Natl Acad. Sci. USA 112, 2093-2096 (2015).
3. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
4. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229-3236 (2013).
5. Muscatine, L. & Porter, J. W. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27, 454-460 (1977).
6. Ainsworth, T. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261-2274 (2015).
7. 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).
8. Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1-14 (2006).
9. Rohwer, F., Seguritan, V., Azam, F. & Knowlton, N. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243, 1-10 (2002).
10. Bay, R. A. & Palumbi, S. R. Multilocus adaptation associated with heat resistance in reef-building corals. Curr. Biol. 24, 2952-2956 (2014).
11. Hume, B. C. C. et al. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc. Natl Acad. Sci. USA 113, 4416-4421 (2016).
12. Buddemeier, R. W. & Fautin, D. G. Coral bleaching as an adaptive mechanism. BioScience 43, 320-326 (1993).
13. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068-2073 (2006).
14. Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. bioRxiv. 1, e00028-16 (2016).
15. Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560-563 (2008).
16. Oliver, T. A. & Palumbi, S. R. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30, 429-440 (2011).
17. Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. USA 110, 1387-1392 (2013).
18. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895-898 (2014).
19. Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 11, 186-200 (2016).
20. Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315-8324 (2016).
21. 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).
22. Seneca, F. O. & Palumbi, S. R. The role of transcriptome resilience in resistance of corals to bleaching. Mol. Ecol. 24, 1467-1484 (2015).
23. Cáceres, M. D. & Legendre, P. Associations between species and groups of sites: indices and statistical inference. Ecology 90, 3566-3574 (2009).
24. Oliver, T. A. & Palumbi, S. R. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30, 241-250 (2010).
25. Lee, S. T. M., Davy, S. K., Tang, S.-L. & Kench, P. S. Mucus sugar content shapes the bacterial community structure in thermally stressed Acropora muricata. Front. Microbiol. 7, 371 (2016).
26. Liu, C. et al. Streptococcus mutans copes with heat stress by multiple transcriptional regulons modulating virulence and energy metabolism. Sci. Rep. 5, 12929 (2015).
27. Santos, H. F. et al. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. 8, 2272-2279 (2014).
28. Lin, Y.-H. et al. Overexpression of ferredoxin, PETF, enhances tolerance to heat stress in Chlamydomonas reinhardtii. Int. J. Mol. Sci. 14, 20913-20929 (2013).
29. Voolstra, C. R. et al. Effects of temperature on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10, 627 (2009).
30. Polato, N. R. et al. Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS ONE 5, e11221 (2010).
31. Martin, J., Horwich, A. & Hartl, F. Prevention of protein denaturation under heat stress by the chaperonin Hsp60. Science 258, 995-998 (1992).
32. Littman, R., Willis, B. L. & Bourne, D. G. Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ. Microbiol. Rep. 3, 651-660 (2011).
33. Coenye, T., Goris, J., Spilker, T., Vandamme, P. & LiPuma, J. J. Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J. Clin. Microbiol. 40, 2062-2069 (2002).
34. Chiron, R. et al. Clinical and microbiological features of Inquilinus sp. isolates from five patients with cystic fibrosis. J. Clin. Microbiol. 43, 3938-3943 (2005).
35. Bayer, T. et al. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79, 4759-4762 (2013).
36. Qin, Q.-L. et al. Comparative genomics of the marine bacterial genus Glaciecola reveals the high degree of genomic diversity and genomic characteristic for cold adaptation. Environ. Microbiol. 16, 1642-1653 (2014).
37. Kushmaro, A., Loya, Y., Fine, M. & Rosenberg, E. Bacterial infection and coral bleaching. Nature 380, 396-396 (1996).
38. Ainsworth, T. D., Fine, M., Roff, G. & Hoegh-Guldberg, O. Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. ISME J. 2, 67-73 (2008).
39. Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929-933 (2003).
40. Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460-1462 (2015).
41. Hoegh-Guldberg, O. et al. Assisted colonization and rapid climate change. Science 321, 345-346 (2008).
42. Andersson, A. F. et al. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE. 3, e2836 (2008).
43. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).
44. Edgar, R. C. et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200 (2011).
45. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).
46. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, USA, 2009).
47. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2015).
48. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300 (1995).
49. Langille, M. G. I. et al. Predictive functional profiling of microbial communities using 16S RNA marker gene sequences. Nat. Biotechnol. 31, 814-821 (2013).