Corals and Their Microbiomes Are Differentially Affected by Exposure to Elevated Nutrients and a Natural Thermal Anomaly

Abstract

Nutrient pollution can increase the prevalence and severity of coral disease and bleaching in ambient temperature conditions or during experimental thermal challenge. However, there have been few opportunities to study the effects of nutrient pollution during natural thermal anomalies. Here we present results from an experiment conducted during the 2014 bleaching event in the Florida Keys, USA, that exposed Agaricia sp. (Undaria) and Siderastrea siderea corals to 3 types of elevated nutrients: nitrogen alone, phosphorous alone, and the combination of nitrogen and phosphorus. Overall, bleaching prevalence and severity was high regardless of treatment, but nitrogen enrichment alone both prolonged bleaching and increased coral mortality in Agaricia corals. At the same time, the elevated temperatures increased the prevalence of Dark Spot Syndrome (DSS), a disease typically associated with cold temperatures in Siderastrea siderea corals. However, nutrient exposure alone did not increase the prevalence or severity of disease, suggesting that thermal stress overwhelms the effects of nutrient pollution on this disease during such an extreme thermal event. Analysis of 78 Siderastrea siderea microbial metagenomes also showed that the thermal event was correlated with significant shifts in the composition and function of the associated microbiomes, and corals with DSS had microbiomes distinct from apparently healthy corals. In particular, we identified shifts in viral, archaeal, and fungal families. These shifts were likely driven by the extreme temperatures or other environmental co-variates occurring during the 2014 bleaching event. However, no microbial taxa were correlated with signs of DSS. Furthermore, although nutrient exposure did not affect microbial alpha diversity, it did significantly affect microbiome beta-diversity, an effect that was independent of time. These results suggest that strong thermal anomalies and local nutrient pollution both interact and act independently to alter coral health in a variety of ways, that ultimately contribute to disease, bleaching, and mortality of reefs in the Florida Keys.

Effects of ultraviolet radiation and nutrient level on the physiological response and organic matter release of the scleractinian coral Pocillopora damicornis following thermal stress

“…In other words, nutrient levels, or UVR exposure, did not increase the severity of bleaching above back ground levels, because temperature had a large impact alone. Two other studies, which have analysed the bleaching severity at different distances from nutrient sources, found no significant impact of nutrient levels on bleaching, in agreement with our observations [ 3 , 52 ]. It was however observed that high nutrient levels did, to some degree, prolonged bleaching in some coral species, and had a distinct effect on coral microbiomes that was independent of temperature [ 52 ].…”

“…Two other studies, which have analysed the bleaching severity at different distances from nutrient sources, found no significant impact of nutrient levels on bleaching, in agreement with our observations [ 3 , 52 ]. It was however observed that high nutrient levels did, to some degree, prolonged bleaching in some coral species, and had a distinct effect on coral microbiomes that was independent of temperature [ 52 ]. Many other studies have linked seawater eutrophication with a higher bleaching susceptibility of different coral species [ 11 , 53 , 54 , 55 ].…”

Microbial Diversity Exploration of Marine Hosts at Serrana Bank, a Coral Atoll of the Seaflower Biosphere Reserve

“…A total of 10 fungi orders, 25 genera, and 23 species were found to be specific for S. siderea (Supplementary Figure S2). The eukaryotic communities identified in this study were limited to Ascomycota (97.41%) and Basidiomycota (2.26%) groups, in contrast to previous studies in which Microsporidia, Chytridiomycota, and Entomophthoromycota were detected as the most abundant phyla within the coral microbiome (Wang et al, 2018). Among the observed classes, Dothideomycetes (55.44%) and Sordariomycetes (18.13%) were the predominant classes but unlike other samples, Orbiliomycetes (0.47%) and Lecanoromycetes (0.08%) were also identified in association with this host.…”

Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities

“…1). Coral bacterial communities are altered by changing environmental conditions such as pollution [17,74], nutrient availability [17,75], environmental anomalies such as temperature [16,21,76], salinity [28], pH [77,78], and eutrophication [79]. Such compositional flexibility indicates a potential capacity for local acclimatization (or adaptation), and thus may be critical for promoting holobiont fitness a.…”