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Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs

1. The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate...

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Autores principales: Mueller, Benjamin, Brocke, Hannah J., Rohwer, Forest L., Dittmar, Thorsten, Huisman, Jef, Vermeij, Mark J. A., de Goeij, Jasper M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9543674/
https://www.ncbi.nlm.nih.gov/pubmed/36247100
http://dx.doi.org/10.1111/1365-2435.14101
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author Mueller, Benjamin
Brocke, Hannah J.
Rohwer, Forest L.
Dittmar, Thorsten
Huisman, Jef
Vermeij, Mark J. A.
de Goeij, Jasper M.
author_facet Mueller, Benjamin
Brocke, Hannah J.
Rohwer, Forest L.
Dittmar, Thorsten
Huisman, Jef
Vermeij, Mark J. A.
de Goeij, Jasper M.
author_sort Mueller, Benjamin
collection PubMed
description 1. The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night‐DOM release and its potential contribution to the microbialization of reefs remains to be investigated. 2. We first tested the occurrence of hypoxic conditions at the turf algae–water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night‐time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night‐DOC to the reef‐wide DOC production. 3. A rapid shift from supersaturated to hypoxic conditions at the turf algae–water interface occurred immediately after the onset of darkness, resulting in night‐DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night‐DOC was utilized by bacterioplankton two times faster than day‐DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night‐DOC release by BCMs and turf algae accounting for >50% of the total release over a diurnal cycle. 4. Night‐DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog.
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spelling pubmed-95436742022-10-14 Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs Mueller, Benjamin Brocke, Hannah J. Rohwer, Forest L. Dittmar, Thorsten Huisman, Jef Vermeij, Mark J. A. de Goeij, Jasper M. Funct Ecol Plant Physiological Ecology 1. The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night‐DOM release and its potential contribution to the microbialization of reefs remains to be investigated. 2. We first tested the occurrence of hypoxic conditions at the turf algae–water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night‐time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night‐DOC to the reef‐wide DOC production. 3. A rapid shift from supersaturated to hypoxic conditions at the turf algae–water interface occurred immediately after the onset of darkness, resulting in night‐DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night‐DOC was utilized by bacterioplankton two times faster than day‐DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night‐DOC release by BCMs and turf algae accounting for >50% of the total release over a diurnal cycle. 4. Night‐DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog. John Wiley and Sons Inc. 2022-07-04 2022-08 /pmc/articles/PMC9543674/ /pubmed/36247100 http://dx.doi.org/10.1111/1365-2435.14101 Text en © 2022 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Plant Physiological Ecology
Mueller, Benjamin
Brocke, Hannah J.
Rohwer, Forest L.
Dittmar, Thorsten
Huisman, Jef
Vermeij, Mark J. A.
de Goeij, Jasper M.
Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title_full Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title_fullStr Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title_full_unstemmed Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title_short Nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
title_sort nocturnal dissolved organic matter release by turf algae and its role in the microbialization of reefs
topic Plant Physiological Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9543674/
https://www.ncbi.nlm.nih.gov/pubmed/36247100
http://dx.doi.org/10.1111/1365-2435.14101
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