Coral reefs worldwide are exhibiting increasing densities of fleshy algae potentially caused by global climate stressors and proximal effects such as nutrient enrichment and the removal of herbivorous fishes. Even after local disturbances are mitigated these shifts to algal-dominated states may be maintained through a positive feedback whereby algae remain dominant and suppress coral recovery through a combination of effects on nutrient availability, microbial activity and allelopathy. We investigated the hypothesis that differences in the amount and composition of dissolved organic carbon (DOC) exuded by corals and algae as a portion of their daily production may play a central role in coral-algal interactions and reef biogeochemical processes by influencing the growth rate and community composition of bacterioplankton in the surrounding water. We measured the production rate and sugar composition (as acid-hydrolyzed dissolved combined neutral sugars; DCNS) of exudates from four dominant benthic producers (one hermatypic coral holobiont and three macroalgae; one each phaeophyta, rhodophyta and chrysophyta) in the coral reef system of Moorea, French Polynesia. We measured the growth response of heterotrophic bacterioplankton to these exudates using dark seawater culture experiments, tracking changes in community composition (via 16S rRNA pyrosequencing), growth rates, DOC utilization and oxygen consumption.
Results/Conclusions
Algae exuded more DOC than corals and the exudates differed markedly in initial DCNS composition. Rates of bacterioplankton growth and DOC utilization were significantly higher in algal exudate treatments than in coral exudate and control incubations. Each substrate engendered a phylogenetically distinct bacterial community, with significant differences among treatments in the relative abundances of 9 of the 25 dominant family-level clades. These communities exhibited differential removal of DCNS components over the course of incubations. We further identified 18 operational taxonomic units (OTUs; sequences clustered at an average 95% sequence identity level) significantly enriched in individual treatments relative to controls. Coral exudates engendered the smallest shift in bacterioplankton community structure and differentially enriched OTUs from proteobacterial lineages with few cultured representatives (Hyphomonadaceae, Sneathiellaceae, and deeply branching clades of the Alteromonadaceae). In contrast, macroalgal exudates selected for Flavobacteria, Rhodobacteraceae, and multiple OTUs closely related to cultured copiotrophic Gammaproteobacteria from families containing known coral pathogens (Vibrionaceae, Alteromonadaceae, Pseudoalteromonadaceae and Oceanospirillaceae). These results suggest that algal exudates foster more rapid growth of bacterioplankton and select for more copiotrophic taxa than coral exudates, with implications for coral-algal interactions and the role of bacterioplankton in tropical reef ecosystems.