Evidence points to a link between environmental stressors, coral-associated bacteria, and coral disease; however, few studies have examined the details of this relationship under tightly controlled experimental conditions. To address this gap, an array of closed-system, precision-controlled experimental aquaria were used to investigate the effects of an abrupt 1°C above summer ambient temperature increase on the bacterial community structure and photophysiology of Porites compressa corals. While the temperature treatment rapidly impacted the photophysiology of the coral host, it did not elicit a statistically significant shift in bacterial community structure from control, untreated corals as determined by terminal restriction fragment length polymorphism analysis of 16S rRNA genes. Two of three coral colonies harbored more closely related bacterial communities at the time of collection and, despite statistically significant shifts in bacterial community structure for both control and treatment corals during the 10-day acclimation period, maintained this relationship over the course of the experiment. The experimental design used in this study proved to be a robust, reproducible system for investigating coral microbiology in an aquarium setting. 1. Introduction The worldwide degradation of coral reef ecosystems is due, in part, to the emergence of novel pathogenic diseases affecting scleractinian corals [1, 2], and it has been speculated that the widespread proliferation of coral diseases is linked to increasing sea surface temperatures (SSTs) [3, 4]. Many disease outbreaks correlate with temperature anomalies and seasonal warming [3, 5, 6], and increased SSTs have also been shown to affect the virulence of coral disease pathogens [7]. For example, infection of Pocillopora damicornis by the bacterial pathogen Vibrio coralyticus increases rapidly with increased temperatures [8], and disease outbreaks often follow or co-occur with temperature-induced coral bleaching [2, 6, 9]. Discriminating between bacteria acting as causative agents of coral bleaching [10, 11] versus postbleaching opportunists has been ambiguous [12, 13]. However, it remains undisputed that bacteria play important roles in both maintaining and destabilizing the health of the coral holobiont, which is composed of coral host polyps, symbiotic dinoflagellates known as zooxanthellae, and a diverse assemblage of associated algae, fungi, Bacteria, Archaea, and viruses associated with the skeleton, tissues, and mucus layer of adult coral colonies [14, 15]. Our limited understanding of the
References
[1]
K. D. Lafferty, J. W. Porter, and S. E. Ford, “Are diseases increasing in the ocean?” Annual Review of Ecology, Evolution, and Systematics, vol. 35, pp. 31–54, 2004.
[2]
C. Harvell, E. Jordán-Dalhgren, S. Merkel, et al., “Coral disease, environmental drivers and the balance between coral and microbial associates,” Oceanography, vol. 20, pp. 172–195, 2007.
[3]
C. D. Harvell, C. E. Mitchell, J. R. Ward et al., “Climate warming and disease risks for terrestrial and marine biota,” Science, vol. 296, no. 5576, pp. 2158–2162, 2002.
[4]
J. R. Ward and K. D. Lafferty, “The elusive baseline of marine disease: are diseases in ocean ecosystems increasing?” PLoS Biology, vol. 2, no. 4, pp. 542–547, 2004.
[5]
K. G. Kuta and L. L. Richardson, “Ecological aspects of black band disease of corals: relationships between disease incidence and environmental factors,” Coral Reefs, vol. 21, no. 4, pp. 393–398, 2002.
[6]
R. J. Jones, J. Bowyer, O. Hoegh-Guldberg, and L. L. Blackall, “Dynamics of a temperature-related coral disease outbreak,” Marine Ecology Progress Series, vol. 281, pp. 63–77, 2004.
[7]
J. M. Cervino, R. L. Hayes, S. W. Polson et al., “Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals,” Applied and Environmental Microbiology, vol. 70, no. 11, pp. 6855–6864, 2004.
[8]
Y. Ben-Haim and E. Rosenberg, “A novel Vibrio sp. pathogen of the coral Pocillopora damicornis,” Marine Biology, vol. 141, no. 1, pp. 47–55, 2002.
[9]
M. E. Brandt and J. W. Mcmanus, “Disease incidence is related to bleaching extent in reef-building corals,” Ecology, vol. 90, no. 10, pp. 2859–2867, 2009.
[10]
Y. Ben-Haim, E. Banim, A. Kushmaro, Y. Loya, and E. Rosenberg, “Inhibition of photosynthesis and bleaching of zooxanthellae by the coral pathogen Vibrio shiloi,” Environmental Microbiology, vol. 1, no. 3, pp. 223–229, 1999.
[11]
E. Banin, T. Israely, M. Fine, Y. Loya, and E. Rosenberg, “Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host,” FEMS Microbiology Letters, vol. 199, no. 1, pp. 33–37, 2001.
[12]
M. P. Lesser, J. C. Bythell, R. D. Gates, R. W. Johnstone, and O. Hoegh-Guldberg, “Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data,” Journal of Experimental Marine Biology and Ecology, vol. 346, no. 1-2, pp. 36–44, 2007.
[13]
T. D. Ainsworth, M. Fine, G. Roff, and O. Hoegh-Guldberg, “Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica,” ISME Journal, vol. 2, no. 1, pp. 67–73, 2008.
[14]
N. Knowlton and F. Rohwer, “Multispecies microbial mutualisms on coral reefs: the host as a habitat,” American Naturalist, vol. 162, no. 4, pp. S51–S62, 2003.
[15]
F. Rohwer, V. Seguritan, F. Azam, and N. Knowlton, “Diversity and distribution of coral-associated bacteria,” Marine Ecology Progress Series, vol. 243, pp. 1–10, 2002.
[16]
H. Ducklow and R. Mitchell, “Bacterial populations and adaptations in the mucus layers on living corals,” Limnology and Oceanography, vol. 24, no. 4, pp. 715–725, 1979.
[17]
M. Wafar, S. Wafar, and J. J. David, “Nitrification in reef corals,” Limnology & Oceanography, vol. 35, no. 3, pp. 725–730, 1990.
[18]
F. Rohwer, M. Breitbart, J. Jara, F. Azam, and N. Knowlton, “Diversity of bacteria associated with the Caribbean coral Montastraea franksi,” Coral Reefs, vol. 20, no. 1, pp. 85–91, 2001.
[19]
M. P. Lesser, C. H. Mazel, M. Y. Gorbunov, and P. G. Falkowski, “Discovery of symbiotic nitrogen-fixing cyanobacteria in corals,” Science, vol. 305, no. 5686, pp. 997–1000, 2004.
[20]
K. B. Ritchie, “Regulation of microbial populations by coral surface mucus and mucus-associated bacteria,” Marine Ecology Progress Series, vol. 322, pp. 1–14, 2006.
[21]
D. I. Kline, N. M. Kuntz, M. Breitbart, N. Knowlton, and F. Rohwer, “Role of elevated organic carbon levels and microbial activity in coral mortality,” Marine Ecology Progress Series, vol. 314, pp. 119–125, 2006.
[22]
J. S. Klaus, I. Janse, J. M. Heikoop, R. A. Sanford, and B. W. Fouke, “Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution,” Environmental Microbiology, vol. 9, no. 5, pp. 1291–1305, 2007.
[23]
R. V. Thurber, D. Willner-Hall, B. Rodriguez-Mueller et al., “Metagenomic analysis of stressed coral holobionts,” Environmental Microbiology, vol. 11, no. 8, pp. 2148–2163, 2009.
[24]
O. Pantos, R. P. Cooney, M. D. A. Le Tissier, M. R. Barer, A. G. O'Donnell, and J. C. Bythell, “The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis,” Environmental Microbiology, vol. 5, no. 5, pp. 370–382, 2003.
[25]
R. J. Jones and O. Hoegh-Guldberg, “Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing,” Marine Ecology Progress Series, vol. 177, pp. 83–91, 1999.
[26]
K. Maxwell and G. N. Johnson, “Chlorophyll fluorescence—a practical guide,” Journal of Experimental Botany, vol. 51, no. 345, pp. 659–668, 2000.
[27]
M. E. Warner, W. K. Fitt, and G. W. Schmidt, “Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 14, pp. 8007–8012, 1999.
[28]
M. T. Suzuki, O. Béjà, L. T. Taylor, and E. F. DeLong, “Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton,” Environmental Microbiology, vol. 3, no. 5, pp. 323–331, 2001.
[29]
W.-T. Liu, T. L. Marsh, H. Cheng, and L. J. Forney, “Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA,” Applied and Environmental Microbiology, vol. 63, no. 11, pp. 4516–4522, 1997.
[30]
C. A. Osborne, G. N. Rees, Y. Bernstein, and P. H. Janssen, “New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities,” Applied and Environmental Microbiology, vol. 72, no. 2, pp. 1270–1278, 2006.
[31]
K. R. Clarke and R. N. Gorley, PRIMER v6: User Manual/Tutorial, PRIMER-E, Plymouth, UK, 2006.
[32]
M. J. Anderson, R. N. Gorely, and K. R. Clarke, PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods, PRIMER-E, Plymouth, UK, 2008.
[33]
K. R. Clarke and R. M. Warwick, Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, PRIMER-E, Plymouth, UK, 2nd edition, 2001.
[34]
R. N. Shepard, “The analysis of proximities: multidimensional scaling with an unknown distance function. I.,” Psychometrika, vol. 27, no. 2, pp. 125–140, 1962.
[35]
J. B. Kruskal, “Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis,” Psychometrika, vol. 29, no. 1, pp. 1–27, 1964.
[36]
J. Frias-Lopez, J. S. Klaus, G. T. Bonheyo, and B. W. Fouke, “Bacterial community associated with black band disease in corals,” Applied and Environmental Microbiology, vol. 70, no. 10, pp. 5955–5962, 2004.
[37]
O. Pantos and J. C. Bythell, “Bacterial community structure associated with white band disease in the elkhorn coral Acropora palmata determined using culture-independent 16S rRNA techniques,” Diseases of Aquatic Organisms, vol. 69, no. 1, pp. 79–88, 2006.
[38]
S. L. Coles and Y. H. Fadlallah, “Reef coral survival and mortality at low temperatures in the Arabian Gulf: new species-specific lower temperature limits,” Coral Reefs, vol. 9, no. 4, pp. 231–237, 1991.
[39]
P. L. Jokiel and S. L. Coles, “Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature,” Coral Reefs, vol. 8, no. 4, pp. 155–162, 1990.
[40]
B. E. Brown, “Coral bleaching: causes and consequences,” Coral Reefs, vol. 16, no. 1, pp. S129–S138, 1997.
