The Hologenome Theory Disregards the Coral Holobiont

Online Correspondence

holobiont model15. We feel that the lack of The hologenome theory consideration of the wide and diverse scientific literature on coral bleaching, coupled with the absence of scientific evidence that disregards the coral holobiont supports a role for bacterial populations in driving global patterns of bleaching, combine ‡ § || § William Leggat* , Tracy Ainsworth* , John Bythell , Sophie Dove* , to raise serious questions as to the relevance of Ruth Gates¶, Ove Hoegh-Guldberg*§, Roberto Iglesias-Prieto# and the hologenome theory of evolution. David Yellowlees*‡ *ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, The ‘hologenome theory of evolution’, pro- between mass bleaching and the anomalous Australia. posed by Rosenberg and colleagues1, suggests temperatures that disrupt photosynthesis in ‡School of Pharmacy and Molecular Sciences, James that reef corals, and by extrapolation other the endosymbiotic dinoflagellates that are Cook University, Townsville, Queensland 4811, multicellular organisms, adapt to environ- harboured by corals5–8; this is analogous to Australia. mental stress by alterations in their resident the bleaching that occurs in higher plants9. §Centre for Marine Studies, University of Queensland, microbial communities. Although this is an However, this overwhelming evidence was Brisbane 4072, Australia. interesting idea, we strongly disagree with completely ignored by Rosenberg and col- ||School of Biology, Newcastle University, Newcastle aspects of this theory, specifically those that leagues. In addition, studies from both upon Tyne NE1 7RU, UK. arise from the omission and flawed interpreta- terrestrial and marine environments have ¶University of Hawaii, School of Ocean and Earth tion of the coral literature (for reviews of omit- demonstrated that there is increased disease Science and Technology, Hawaii Institute of Marine ted literature see Refs 2,3). prevalence and severity in stressed popula- Biology, Kaneohe HI96744, USA. The theory is based on the author’s obser- tions10, which suggests that a less-fit holobiont #Universidad Nacional Autónoma de México, Apartado vation that Oculina patagonica bleaches in has emerged. These observations completely Postal 1152, Cancún 77500, Mexico. response to Vibrio shiloi infection and it was contradict the expected outcomes of the hol- Correspondence to W.L. subsequently suggested that all coral bleaching ogenome theory. e-mail: [email protected] is the result of bacterial infection1,4. Our main Rosenberg and colleagues also over-sim- doi:10.1038/nrmicro1635C1 criticism of this hypothesis is that bleaching plify the highly complex relationship between 1. Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in is a broad stress response in corals, which has host and symbiont, and make broad assump- coral health, disease and evolution. Nature Rev. been observed even in the absence of the pro- tions about coral and invertebrate immunity. Microbiol. 5, 355–362 (2007). posed bacterial causal agents1. In fact, there For example, they fail to acknowledge the 2. Hoegh-Guldberg, O. Coral reefs in a century of rapid environmental change. Symbiosis 37, 1–31 (2004). is no experimental evidence to support a role molecular diversity of the endosymbiotic 3. Douglas, A. E. Coral bleaching — how and why? Mar. for bacteria in the mass coral-bleaching events dinoflagellates and the array of responses and Pollut. Bull. 46, 385–392 (2003). 4. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & that occur over large geographical scales. The adaptive mechanisms that this union provides Rosenberg, E. The coral probiotic hypothesis. Environ. bulk of the literature indicates a direct link the holobiont. They also ignore a range of Microbiol. 8, 2068–2073 (2006). 5. Iglesias-Prieto, R., Matta, J. L., Robins, W. A. & studies that clearly demonstrate the presence Trench, R. K. Photosynthetic response to elevated of highly conserved acclimatization mecha- temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl nisms, which are mobilized to accommodate Acad. Sci. USA 89, 10302–10305 (1992). changes in the environment in both coral 6. Warner, M. E., Fitt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: a and endosymbiotic dinoflagellates. These determinant of coral bleaching. Proc. Natl Acad. Sci. include the induction of heat-shock proteins USA 96, 8007–8012 (1999). 7. Jones, R. J., Hoegh-Guldberg, O., Larkum, A. W. D. & and antioxidant enzymes, restructuring of the Schreiber, U. Temperature-induced bleaching of corals

light-harvesting complexes and differential begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21, 1219–1230 expression of host pigmentation (reviewed (1998). in Ref. 11). In addition, the authors imply that 8. Tchernov, D. et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in invertebrates lack immune memory, which corals. Proc. Natl Acad. Sci. USA 101, 13531–13535 is a feature of acquired immunity in verte- (2004). 9. Sharkey, T. D. Effects of moderate heat stress on brates. A range of recent studies (reviewed in photosynthesis: importance of thylakoid reactions, Refs 12,13) have demonstrated the presence rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell of immune memory in invertebrates. Further, Environ. 28, 269–277 (2005). a recent survey of available cnidarian genome 10. Harvell, C. D. et al. Climate warming and disease risks information shows that Toll and Toll-like- for terrestrial and marine biota. Science 296, 2158–2162 (2002). 14 receptor homologues are present, which 11. Coles, S. L. & Brown, B. E. Coral bleaching-capacity for strongly suggests that a pathway for immune acclimatization and adaptation. Adv. Mar. Biol. 46, 183–223 (2003). memory exists in corals. 12. Kurtz, J. Specific memory within innate immune In conclusion, Rosenberg and colleagues systems. Trends Immunol. 26, 186–192 (2005). 13. Little, T. J., Hultmark, D. & Read, A. F. Invertebrate Figure 1 | A mass bleaching event on the present a hypothesis that is based on a small immunity and the limits of mechanistic immunology. subset of the available coral and bleaching lit- Nature Immunol. 6, 651–654 (2005). Great Barrier Reef in 2006. These events 14. Miller, D. et al. The innate immune repertoire in simultaneously affect multiple species over erature, and have dismissed without comment Cnidaria — ancestral complexity and stochastic gene large geographial ranges and are highly well-established facts about endosymbiosis loss. Genome Biol. 8, R59 (2007). 15. Rohwer, F., Seguritan, V., Azam, F. & Knowlton, N. correlated with elevated seawater and the host. Their microbial-centric view is Diversity and distribution of coral-associated bacteria. temperatures. at odds with the now widely embraced coral Mar. Ecol. Prog. Ser 243, 1–10 (2002).