Ecology and microbiology of black band disease: new insights into the etiology of an old coral disease

Sato, Yui (2012) Ecology and microbiology of black band disease: new insights into the etiology of an old coral disease. PhD thesis, James Cook University.

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Abstract

The prevalence of black band disease (BBD), a virulent coral disease characterized by a thick microbial mat that migrates across coral colonies causing rapid tissue loss, is generally low on Indo-Pacific reefs, but the destructive impact that the disease has had on Caribbean reefs highlights the urgent need to understand the role that the disease could play in the dynamics of coral populations on the Great Barrier Reef (GBR). In 2006, the first recorded epizootic of BBD on the GBR infected an inshore assemblage of corals in the genus Montipora at Pelorus Island, located in the central GBR region. Over the next 2.7 years, recurring summer outbreaks of BBD were monitored, with BBD abundance peaking in the warmest month in each of three summers. Mean maximum abundance of BBD reached 16±6 colonies per 100 m² in summer, affecting up to 10% of coral colonies (n=485 colonies monitored), and decreased to 0-1 colony per 100 m² in winter. Reappearance of BBD on previously infected colonies and continuous tissue loss after BBD signs had disappeared suggest that disease impacts are of longer duration than indicated by the presence of macroscopic disease signs. On average, BBD lesions caused the loss of 40% of tissue surface area per colony, and 5% of infections led to whole colony mortality. Overall, the BBD epizootic had a substantial impact on Montipora assemblages on this inshore reef in the central GBR, clearly establishing the virulent nature of the disease for GBR corals.

Rates of new infections and linear progression of lesions recorded during the field monitoring program were both positively correlated with seasonal fluctuations in seawater temperature and light, suggesting that seasonal increases in these environmental parameters enhance the virulence of the disease. To isolate the potential contributions of temperature and light, which both vary seasonally, I examined the relative impacts of these two environmental variables on the virulence of BBD under controlled aquarium conditions. Progression rates of BBD lesions on Montipora hispida colonies were compared among three controlled temperature (28.0, 29.0, 30.5ºC) and two controlled light treatments (170, 440 μmol m⁻² s⁻¹). BBD progression rates were greatest (5.2 mm d⁻¹) in the 30.5ºC/high-light treatment and least (3.2 mm d⁻¹) in the 28ºC/lowvi light treatment. High light significantly enhanced BBD progression, whereas rates of disease progression did not vary significantly among temperature treatments, identifying the greater role of light in driving BBD dynamics within the temperature range examined. Greater BBD progression during the day compared to the night (by 2.2 - 3.6-fold across temperature and light treatments) corroborates my conclusion that light is the preeminent factor driving BBD progression at typical summer temperatures. Decreased photochemical efficiency of algal endosymbionts in the high-temperature/high-light treatments suggests that compromised health of the coral holobiont contributes to enhanced disease progression, highlighting the complexity of disease dynamics in host-pathogen systems responding to environmental variation.

The complex microbial consortium comprising BBD lesions, including cyanobacteria, sulfate-reducing bacteria, sulfide-oxidizing bacteria, marine fungi and other heterotrophic microorganisms, act together to produce highly concentrated sulfide and anoxic conditions beneath the BBD mat; conditions that are lethal to coral tissue. However, little is known about how this microbial community develops to form the complex microbial consortia of BBD in situ. While monitoring the BBD outbreak at Pelorus Island, I observed a less-virulent precursor stage, which I named 'cyanobacterial patch' (CP), and followed successional changes in microbial communities leading to the development of BBD from CP. CP lesions found on M. hispida colonies were macroscopically distinct from BBD lesions and preceded the onset of BBD in 19% of cases (n=262 CP lesions). Dominant cyanobacteria within CP lesions were morphologically and phylogenetically distinct from those dominating BBD lesions. Molecular analysis of cyanobacterial 16S ribosomal RNA (rRNA) coding genes confirmed shifts within cyanobacterial assemblages from Blennothrix/Trichodesmium spp.-related sequences dominating CP lesions to Oscillatoria sp.-related sequences, which were similar to those retrieved from other BBD samples worldwide, dominating BBD lesions. 16S rRNA gene clone libraries targeting Bacteria also demonstrated shifts in bacterial ribotypes during transitions from CP to BBD, with Alphaproteobacteria-affiliated sequences dominating in CP libraries, whereas gammaproteobacterial and cyanobacterial ribotypes were more abundant in BBD clone libraries. Sequences affiliated with sulfur-cycling organisms were commonly retrieved from lesions exhibiting characteristic field signs of BBD. Since high sulfide concentrations have been implicated in BBD-mediated coral tissue degradation, proliferation of a microbial community actively involved in sulfur-cycling potentially contributes to the higher progression rates found for BBD compared to CP lesions.

To further characterize microbial community interactions contributing to BBD pathogenicity, I investigated the diversity of Bacteria, as well as previously-unexplored Archaea, associated with both BBD and CP microbial consortia, using high-throughput pyrosequencing. Profiles of bacterial 16S rRNA genes of BBD and CP illustrated patterns of community changes during BBD development that were consistent with those observed in the clone library-based study, confirming that bacterial ribotypes often observed in oxygen-depleted, sulfide-rich environments become relatively abundant during disease onset. Archaeal sequences retrieved from BBD were dominated (up to 94%) by a novel ribotype distantly affiliated to Euryarchaeotes, whereas CP-derived profiles indicated the presence of diverse archaeal assemblages affiliated to species across the Thaumarchaeota and Euryarchaeota, and were similar to communities reported from oxic marine environments. Although function(s) of BBD-associated Archaea are unknown due to the novelty of the 16S rRNA sequences, given organic- and sulfide-rich anoxic microenvironments within BBD lesions, BBD-associated Archaea may carry out methanogenesis and/or anaerobic methane-oxidation, syntrophically coupled with bacterial sulfate-reduction, thereby potentially enhancing the virulence of BBD.

Lastly, I developed a model of BBD pathogenesis based on my studies of the in situ development of BBD from CP. The model demonstrates that successional changes in key cyanobacterial and bacterial members of the initial CP microbial community lead to the development of a complex polymicrobial consortium that provides ideal conditions for sulfide production and the development of anoxic conditions as CP lesions transition into BBD. The changing nature of this microenvironment facilitates the growth of anaerobic Bacteria and Archaea, further developing the virulence of the microbial community. Knowledge derived from this study provides new insights into the microbial ecology of BBD, contributing to a better mechanistic understanding of BBD pathogenesis that is vital for any future development of management strategies to mitigate the impacts of BBD on coral reef ecosystems.

Item ID: 32613
Item Type: Thesis (PhD)
Keywords: coral disease; black band disease; Great Barrier Reef; GBR; Pelorus Island; microbiology; ecology
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Sato, Yui, Bourne, David G., and Willis, Bette L. (2009) Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia). Proceedings of the Royal Society of London Series B, 276. pp. 2795-2803.

Chapter 3: Sato, Y., Bourne, D.G., and Willis, B.L. (2011) Effects of temperature and light on the progression of black band disease on the reef coral, Montipora hispida. Coral Reefs, 30 (3). pp. 753-761.

Chapter 4: Sato, Yui, Willis, Bette L., and Bourne, David G. (2010) Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME Journal, 4 (2). pp. 203-214.

Appendix A: Bourne, David G, Muirhead, Andrew, and Sato, Yui (2011) Changes in sulfate-reducing bacterial populations during the onset of black band disease. ISME Journal: multidisciplinary journal of microbial ecology, 5 (3). 559- 564.

Appendix B: Glas, Martin S., Sato, Yui, Ulstrup, Karin E., and Bourne, David G. (2012) Biogeochemical conditions determine virulence of black band disease in corals. ISME Journal: multidisciplinary journal of microbial ecology, 6 (8). pp. 1526-1534.

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Date Deposited: 30 Apr 2014 06:37
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 34%
06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060504 Microbial Ecology @ 33%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060405 Gene Expression (incl Microarray and other genome-wide approaches) @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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