Abstract

Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis, Porites astreoides, and Stephanocoenia intersepta Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus, three groups of Synechococcus, photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus, all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day-1, respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h-1 and 387 ng h-1, depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus, coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs.IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down.

Highlights

  • Coral reefs are possible sinks for microbes; the removal mechanisms at play are not well understood

  • The microbial communities found in the water column surrounding and overlying coral reef systems are largely comprised of small phytoplankton such as picoeukaryotes, Prochlorococcus, Synechococcus, and heterotrophic bacteria [6,7,8,9,10]

  • Flow cytometry-based quantification in an Australian fringing reef system with directional wave motion across the reef to the lagoon showed that concentrations of the cyanobacteria, Prochlorococcus and Synechococcus, small photosynthetic eukaryotes, and heterotrophic bacteria are higher over reef zones than in the sandy-bottomed lagoon behind the reef [12]

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Summary

Introduction

Coral reefs are possible sinks for microbes; the removal mechanisms at play are not well understood. Flow cytometry-based quantification in an Australian fringing reef system with directional wave motion across the reef to the lagoon showed that concentrations of the cyanobacteria, Prochlorococcus and Synechococcus, small photosynthetic eukaryotes, and heterotrophic bacteria are higher over reef zones than in the sandy-bottomed lagoon behind the reef (shoreside) [12] This raises questions about whether or not reef systems can remove pelagic microbial cells from the overlaying water column and, if so, by what mechanism and to what extent [11,12,13]. In the Florida Keys, the giant barrel sponge Xetospongia muta was shown to preferentially consume Prochlorococcus and Synechococcus over picoeukaryotes and bacteria, with preferential selection of the latter two occurring in a concentration-dependent manner (higher selectivity at higher concentrations) [7] These reef invertebrates can alter the relative abundance of different pelagic microbial groups in the outgoing water that is returned to the broader system. Selective feeding on microbial cells may be important for corals under environmentally stressful conditions when demand for heterotrophically derived carbon is high [26]

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