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Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals

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 Stephanocoe...

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Autores principales: Hoadley, Kenneth D., Hamilton, Maria, Poirier, Camille L., Choi, Chang Jae, Yung, Cheuk-Man, Worden, Alexandra Z.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091028/
https://www.ncbi.nlm.nih.gov/pubmed/33674432
http://dx.doi.org/10.1128/AEM.03175-20
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author Hoadley, Kenneth D.
Hamilton, Maria
Poirier, Camille L.
Choi, Chang Jae
Yung, Cheuk-Man
Worden, Alexandra Z.
author_facet Hoadley, Kenneth D.
Hamilton, Maria
Poirier, Camille L.
Choi, Chang Jae
Yung, Cheuk-Man
Worden, Alexandra Z.
author_sort Hoadley, Kenneth D.
collection PubMed
description 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.
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spelling pubmed-80910282021-10-13 Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals Hoadley, Kenneth D. Hamilton, Maria Poirier, Camille L. Choi, Chang Jae Yung, Cheuk-Man Worden, Alexandra Z. Appl Environ Microbiol Microbial Ecology 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. American Society for Microbiology 2021-04-13 /pmc/articles/PMC8091028/ /pubmed/33674432 http://dx.doi.org/10.1128/AEM.03175-20 Text en Copyright © 2021 Hoadley et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Microbial Ecology
Hoadley, Kenneth D.
Hamilton, Maria
Poirier, Camille L.
Choi, Chang Jae
Yung, Cheuk-Man
Worden, Alexandra Z.
Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title_full Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title_fullStr Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title_full_unstemmed Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title_short Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals
title_sort selective uptake of pelagic microbial community members by caribbean reef corals
topic Microbial Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091028/
https://www.ncbi.nlm.nih.gov/pubmed/33674432
http://dx.doi.org/10.1128/AEM.03175-20
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