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A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides

The mixoplankton green Noctiluca scintillans (gNoctiluca) is known to form extensive green tides in tropical coastal ecosystems prone to eutrophication. In the Arabian Sea, their recent appearance and annual recurrence have upended an ecosystem that was once exclusively dominated by diatoms. Despite...

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Autores principales: Luo, Hao, Wang, Jingtian, Goes, Joaquim I., Gomes, Helga do R., Al-Hashmi, Khalid, Tobias, Craig, Koerting, Claudia, Lin, Senjie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723592/
https://www.ncbi.nlm.nih.gov/pubmed/37938758
http://dx.doi.org/10.1038/s43705-022-00187-4
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author Luo, Hao
Wang, Jingtian
Goes, Joaquim I.
Gomes, Helga do R.
Al-Hashmi, Khalid
Tobias, Craig
Koerting, Claudia
Lin, Senjie
author_facet Luo, Hao
Wang, Jingtian
Goes, Joaquim I.
Gomes, Helga do R.
Al-Hashmi, Khalid
Tobias, Craig
Koerting, Claudia
Lin, Senjie
author_sort Luo, Hao
collection PubMed
description The mixoplankton green Noctiluca scintillans (gNoctiluca) is known to form extensive green tides in tropical coastal ecosystems prone to eutrophication. In the Arabian Sea, their recent appearance and annual recurrence have upended an ecosystem that was once exclusively dominated by diatoms. Despite evidence of strong links to eutrophication, hypoxia and warming, the mechanisms underlying outbreaks of this mixoplanktonic dinoflagellate remain uncertain. Here we have used eco-physiological measurements and transcriptomic profiling to ascribe gNoctiluca’s explosive growth during bloom formation to the form of sexual reproduction that produces numerous gametes. Rapid growth of gNoctiluca coincided with active ammonium and phosphate release from gNoctiluca cells, which exhibited high transcriptional activity of phagocytosis and metabolism generating ammonium. This grazing-driven nutrient flow ostensibly promotes the growth of phytoplankton as prey and offers positive support successively for bloom formation and maintenance. We also provide the first evidence that the host gNoctiluca cell could be manipulating growth of its endosymbiont population in order to exploit their photosynthetic products and meet critical energy needs. These findings illuminate gNoctiluca’s little known nutritional and reproductive strategies that facilitate its ability to form intense and expansive gNoctiluca blooms to the detriment of regional water, food and the socio-economic security in several tropical countries.
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spelling pubmed-97235922023-01-04 A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides Luo, Hao Wang, Jingtian Goes, Joaquim I. Gomes, Helga do R. Al-Hashmi, Khalid Tobias, Craig Koerting, Claudia Lin, Senjie ISME Commun Article The mixoplankton green Noctiluca scintillans (gNoctiluca) is known to form extensive green tides in tropical coastal ecosystems prone to eutrophication. In the Arabian Sea, their recent appearance and annual recurrence have upended an ecosystem that was once exclusively dominated by diatoms. Despite evidence of strong links to eutrophication, hypoxia and warming, the mechanisms underlying outbreaks of this mixoplanktonic dinoflagellate remain uncertain. Here we have used eco-physiological measurements and transcriptomic profiling to ascribe gNoctiluca’s explosive growth during bloom formation to the form of sexual reproduction that produces numerous gametes. Rapid growth of gNoctiluca coincided with active ammonium and phosphate release from gNoctiluca cells, which exhibited high transcriptional activity of phagocytosis and metabolism generating ammonium. This grazing-driven nutrient flow ostensibly promotes the growth of phytoplankton as prey and offers positive support successively for bloom formation and maintenance. We also provide the first evidence that the host gNoctiluca cell could be manipulating growth of its endosymbiont population in order to exploit their photosynthetic products and meet critical energy needs. These findings illuminate gNoctiluca’s little known nutritional and reproductive strategies that facilitate its ability to form intense and expansive gNoctiluca blooms to the detriment of regional water, food and the socio-economic security in several tropical countries. Nature Publishing Group UK 2022-10-20 /pmc/articles/PMC9723592/ /pubmed/37938758 http://dx.doi.org/10.1038/s43705-022-00187-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Luo, Hao
Wang, Jingtian
Goes, Joaquim I.
Gomes, Helga do R.
Al-Hashmi, Khalid
Tobias, Craig
Koerting, Claudia
Lin, Senjie
A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title_full A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title_fullStr A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title_full_unstemmed A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title_short A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides
title_sort grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread noctiluca green tides
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723592/
https://www.ncbi.nlm.nih.gov/pubmed/37938758
http://dx.doi.org/10.1038/s43705-022-00187-4
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