Range-wide population genetic structure of the Caribbean sea fan coral, Gorgonia ventalina.

The population structure of benthic marine organisms is of central relevance to the conservation and management of these often threatened species, as well as to the accurate understanding of their ecological and evolutionary dynamics. A growing body of evidence suggests that marine populations can be structured over short distances despite theoretically high dispersal potential. Yet the proposed mechanisms governing this structure vary, and existing empirical population genetic evidence is of insufficient taxonomic and geographic scope to allow for strong general inferences. Here, we describe the range-wide population genetic structure of an ecologically important Caribbean octocoral, Gorgonia ventalina. Genetic differentiation was positively correlated with geographic distance and negatively correlated with oceanographically modelled dispersal probability throughout the range. Although we observed admixture across hundreds of kilometres, estimated dispersal was low, and populations were differentiated across distances <2 km. These results suggest that populations of G. ventalina may be evolutionarily coupled via gene flow but are largely demographically independent. Observed patterns of differentiation corroborate biogeographic breaks found in other taxa (e.g. an east/west divide near Puerto Rico), and also identify population divides not discussed in previous studies (e.g. the Yucatan Channel). High genotypic diversity and absence of clonemates indicate that sex is the primary reproductive mode for G. ventalina. A comparative analysis of the population structure of G. ventalina and its dinoflagellate symbiont, Symbiodinium, indicates that the dispersal of these symbiotic partners is not coupled, and symbiont transmission occurs horizontally.

Antagonistic interactions among coral-associated bacteria.

Reef-building corals are comprised of close associations between the coral animal, symbiotic zooxanthellae, and a diversity of associated microbes (including Bacteria, Archaea and Fungi). Together, these comprise the coral holobiont - a paradigm that emphasizes the potential contributions of each component to the overall function and health of the coral. Little is known about the ecology of the coral-associated microbial community and its hypothesized role in coral health. We explored bacteria-bacteria antagonism among 67 bacterial isolates from the scleractinian coral Montastrea annularis at two temperatures using Burkholder agar diffusion assays. A majority of isolates exhibited inhibitory activity (69.6% of isolates at 25 degrees C, 52.2% at 31 degrees C), with members of the gamma-proteobacteria (Vibrionales and Alteromonadales) being especially antagonistic. Elevated temperatures generally reduced levels of antagonism, although the effects were complex. Several potential pathogens were observed in the microbial community of apparently healthy corals, and 11.6% of isolates were able to inhibit the growth of the coral pathogen Vibrio shiloi at 25 degrees C. Overall, this study demonstrates that antagonism could be a structuring force in coral-associated microbial communities and may contribute to pathogenesis as well as disease resistance.

Isotopic labeling and antifungal resistance as tracers of gut passage of the sea fan pathogen Aspergillus sydowii.

Vectors play a critical role in the ecology of infectious disease by facilitating between host transmission, emphasizing the multi-species nature of disease. Corals are suffering an onslaught of infectious diseases, yet we know little about the role of vector species in the ecology of these epizootics. The infection of octocorals by the fungus Aspergillus sydowii is a widespread Caribbean coral disease. The snail Cyphoma gibbosum is a likely vector species because it is a specialist predator of octocorals, moves regularly among coral colonies, and aggregates on diseased corals. We used a novel application of stable isotope techniques and antifungal-resistant strains of A. sydowii to identify the potential for this snail to vector disease. The use of both isotopically labeled and hygromycin-resistant fungus was successful in definitively tracing A. sydowii through the guts of C. gibbosum from ingestion to feces. Further, we demonstrated in laboratory experiments that snails fed antifungal-resistant A. sydowii excrete viable spores and hyphae in their feces. Overall, this study demonstrates the usefulness of isotopic labeling and antifungal-resistant fungi to trace the movement of pathogen propagules in microbially diverse environments, and suggests that C. gibbosum may be able to spread aspergillosis between octocoral hosts.

Influence of marine reserves on coral disease prevalence.

Predicted increases in disease with climate warming highlight the need for effective management strategies to mitigate disease effects in coral communities. We examined the role of marine protected areas (MPAs) in reducing disease in corals and the hypothesis that the composition of fish communities can influence coral health, by comparing disease prevalence between MPA and non-protected (control) reefs in Palau. Overall, the prevalence of diseases pooled, as well as the prevalence of skeletal eroding band (SEB), brown band disease (BrB) and growth anomalies (GAs) individually in major disease hosts (families Acroporidae and Poritidae), were not significantly reduced within MPAs. In fact, the prevalence of SEB was 2-fold higher within MPAs overall; however, the 4 studied MPAs were ineffective in enhancing coral assemblage or fish stock health. A negative association between the prevalence of SEB and richness of a fish species targeted by fishers in Palau highlights the potential role that well-managed MPAs could play in reducing SEB. The composition of coral communities and their susceptibility to bleaching also influenced the prevalence of disease on the studied reefs. The prevalence of diseases pooled and SEB were positively associated with the cover of major disease hosts (families Acroporidae and Poritidae), and the prevalence of BrB and bleaching were also positively associated. Although our study did not show positive effects of MPAs on coral heath, we did identify the potential for increased fish diversity within MPAs to reduce coral disease. Our study also highlights the complexity of relationships between fish assemblages, coral community composition and coral health on Indo-Pacific reefs.

The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate.

The ascomycete Aspergillus sydowii is associated with a serious epizootic of sea fan corals in the Caribbean. Corals are rich in the compatible solute, dimethylsulfoniopropionate (DMSP), produced by their symbionts, the dinoflagellate Symbiodinium. As other Aspergillus species can catabolize DMSP, liberating dimethyl sulfide (DMS) in the process, we tested A. sydowii strains, obtained from diseased corals and other environments, for this Ddd(+) phenotype. All the strains, irrespective of their geographical or environmental origins, made DMS from DMSP, and all of them contained homologs (>87% identical) of the dddP gene, which encodes an enzyme that releases DMS from DMSP and which occurs in other Ddd(+) fungi and in some marine bacteria. The dddP gene was likely acquired by the Aspergillus fungi by inter-domain horizontal gene transfer from alpha-proteobacteria.

Isolation and characterization of microsatellite loci in the Caribbean sea fan coral, Gorgonia ventalina.

Here we report primers for 10 microsatellite loci from the Caribbean sea fan coral, Gorgonia ventalina. Primers were tested on 237 genomic DNA extracts taken directly from tissue samples of G. ventalina. All loci were polymorphic with allelic richness ranging from 4 to 52. Expected heterozygosity ranged from 0.14 to 0.96. Preliminary data suggest that these microsatellites will be useful tools for studies of the population genetics of this important Caribbean coral species.

Isolation and characterization of microsatellite loci in Aspergillus sydowii, a pathogen of Caribbean sea fan corals.

Here we report on nine microsatellite loci designed for Aspergillus sydowii, a widely distributed soil saprobe that is also the pathogenic agent of aspergillosis in Caribbean sea fan corals. Primers were tested on 20 A. sydowii isolates from the Caribbean, 17 from diseased sea fans and three from environmental sources. All loci were polymorphic and exhibited varying degrees of allelic diversity (three to nine alleles). Gene diversity (expected heterozygosity) ranged from 0.353 to 0.821. These primers will enable future research into the epidemiology of A. sydowii as an emergent infectious disease.

Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii.

Recent outbreaks of new diseases in many ecosystems are caused by novel pathogens, impaired host immunity, or changing environmental conditions. Identifying the source of emergent pathogens is critical for mitigating the impacts of diseases, and understanding the cause of their recent appearances. One ecosystem suffering outbreaks of disease in the past decades is coral reefs, where pathogens such as the fungus Aspergillus sydowii have caused catastrophic population declines in their hosts. Aspergillosis is one of the best-characterized coral diseases, yet the origin of this typically terrestrial fungus in marine systems remains unknown. We examined the genetic structure of a global sample of A. sydowii, including isolates from diseased corals, diseased humans, and environmental sources. Twelve microsatellite markers reveal a pattern of global panmixia among the fungal isolates. A single origin of the pathogen into marine systems seems unlikely given the lack of isolation by distance and lack of evidence for a recent bottleneck. A neighbour-joining phylogeny shows that sea fan isolates are interspersed with environmental isolates, suggesting there have been multiple introductions from land into the ocean. Overall, our results underscore that A. sydowii is a true opportunist, with a diversity of nonrelated isolates able to cause disease in corals. This study highlights the challenge in distinguishing between the role of environment in allowing opportunistic pathogens to increase and actual introductions of new pathogenic microorganisms for coral diseases.