Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals

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 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 meters identified 6 microbial groups: Prochlorococcus, three groups of Synechococcus, photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates for Prochlorococcus, all Synechococcus, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ d−1, respectively and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-hr 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 hr−1 to 387 ng hr−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 post-sunset 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 during environmentally-stressful conditions when symbioses with dinoflagellate algae - break down.

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

“…Corals invest up to 50% of fixed carbon on mucus production [12,13] for physical protection and to trap organic matter that can be consumed via heterotrophy [14,15]. The coral mucus and associated microbial community influences nutrient fluxes into the benthos, water column, and sediment [15][16][17][18][19][20] thus shaping the ecosystem functions. The coral microbiome benefits from the high nitrogen content and organic matter in the SML [7,17] and provides protection against coral pathogens via production of antimicrobials [21,22].…”

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

“…However, the microbial community structure in Bermuda's reef system is simultaneously selected by the coral host versus water and the local environment (i.e., inner reefs versus outer reefs), both at taxonomic and functional levels. The coral SML microbiome of P. strigosa was dominated by taxa commonly present in seawater that are found in other coral species [75,76] and are selectively trapped and consumed by the coral host [19,20]. In this study, P. strigosa from each reef zone had different microbial genera filling similar niches.…”

“…The coral SML efficiently traps Synechococcus from the pelagic picoplankton, which contributes to the flux of particulate organic matter (POM) from the water column to benthos [18]. Corals selectively remove Synechococcus and other pelagic microbes via feeding, and promote the growth of diverse picoplankton, shaping the microbial community in the surrounding reef water [19,20]. Heat-stressed corals preferentially fed on Synechococcus to access the high nitrogen content in their cells and to compensate for the loss of nitrogen from algal endosymbiont Symbiodiniaceae during recovery from bleaching [79].…”

Heat-stressed coral microbiomes are stable and potentially beneficial at the level of taxa and functional genes

“…1). Corals can preferentially feed onSynechococcus , especially to recover from heat stress and bleaching (McNally et al 2017;Meunier et al 2019;Hoadley et al 2021).…”