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Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study

Marine phytoplankton vary widely in size across taxa, and in cell suspension densities across habitats and growth states. Cell suspension density and total biovolume determine the bulk influence of a phytoplankton community upon its environment. Cell suspension density also determines the intercellu...

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Autores principales: Omar, Naaman M., Prášil, Ondřej, McCain, J. Scott P., Campbell, Douglas A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9030875/
https://www.ncbi.nlm.nih.gov/pubmed/35456871
http://dx.doi.org/10.3390/microorganisms10040821
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author Omar, Naaman M.
Prášil, Ondřej
McCain, J. Scott P.
Campbell, Douglas A.
author_facet Omar, Naaman M.
Prášil, Ondřej
McCain, J. Scott P.
Campbell, Douglas A.
author_sort Omar, Naaman M.
collection PubMed
description Marine phytoplankton vary widely in size across taxa, and in cell suspension densities across habitats and growth states. Cell suspension density and total biovolume determine the bulk influence of a phytoplankton community upon its environment. Cell suspension density also determines the intercellular spacings separating phytoplankton cells from each other, or from co-occurring bacterioplankton. Intercellular spacing then determines the mean diffusion paths for exchanges of solutes among co-occurring cells. Marine phytoplankton and bacterioplankton both produce and scavenge reactive oxygen species (ROS), to maintain intracellular ROS homeostasis to support their cellular processes, while limiting damaging reactions. Among ROS, hydrogen peroxide (H(2)O(2)) has relatively low reactivity, long intracellular and extracellular lifetimes, and readily crosses cell membranes. Our objective was to quantify how cells can influence other cells via diffusional interactions, using H(2)O(2) as a case study. To visualize and constrain potentials for cell-to-cell exchanges of H(2)O(2), we simulated the decrease of [H(2)O(2)] outwards from representative phytoplankton taxa maintaining internal [H(2)O(2)] above representative seawater [H(2)O(2)]. [H(2)O(2)] gradients outwards from static cell surfaces were dominated by volumetric dilution, with only a negligible influence from decay. The simulated [H(2)O(2)] fell to background [H(2)O(2)] within ~3.1 µm from a Prochlorococcus cell surface, but extended outwards 90 µm from a diatom cell surface. More rapid decays of other, less stable ROS, would lower these threshold distances. Bacterioplankton lowered simulated local [H(2)O(2)] below background only out to 1.(2) µm from the surface of a static cell, even though bacterioplankton collectively act to influence seawater ROS. These small diffusional spheres around cells mean that direct cell-to-cell exchange of H(2)O(2) is unlikely in oligotrophic habits with widely spaced, small cells; moderate in eutrophic habits with shorter cell-to-cell spacing; but extensive within phytoplankton colonies.
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spelling pubmed-90308752022-04-23 Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study Omar, Naaman M. Prášil, Ondřej McCain, J. Scott P. Campbell, Douglas A. Microorganisms Article Marine phytoplankton vary widely in size across taxa, and in cell suspension densities across habitats and growth states. Cell suspension density and total biovolume determine the bulk influence of a phytoplankton community upon its environment. Cell suspension density also determines the intercellular spacings separating phytoplankton cells from each other, or from co-occurring bacterioplankton. Intercellular spacing then determines the mean diffusion paths for exchanges of solutes among co-occurring cells. Marine phytoplankton and bacterioplankton both produce and scavenge reactive oxygen species (ROS), to maintain intracellular ROS homeostasis to support their cellular processes, while limiting damaging reactions. Among ROS, hydrogen peroxide (H(2)O(2)) has relatively low reactivity, long intracellular and extracellular lifetimes, and readily crosses cell membranes. Our objective was to quantify how cells can influence other cells via diffusional interactions, using H(2)O(2) as a case study. To visualize and constrain potentials for cell-to-cell exchanges of H(2)O(2), we simulated the decrease of [H(2)O(2)] outwards from representative phytoplankton taxa maintaining internal [H(2)O(2)] above representative seawater [H(2)O(2)]. [H(2)O(2)] gradients outwards from static cell surfaces were dominated by volumetric dilution, with only a negligible influence from decay. The simulated [H(2)O(2)] fell to background [H(2)O(2)] within ~3.1 µm from a Prochlorococcus cell surface, but extended outwards 90 µm from a diatom cell surface. More rapid decays of other, less stable ROS, would lower these threshold distances. Bacterioplankton lowered simulated local [H(2)O(2)] below background only out to 1.(2) µm from the surface of a static cell, even though bacterioplankton collectively act to influence seawater ROS. These small diffusional spheres around cells mean that direct cell-to-cell exchange of H(2)O(2) is unlikely in oligotrophic habits with widely spaced, small cells; moderate in eutrophic habits with shorter cell-to-cell spacing; but extensive within phytoplankton colonies. MDPI 2022-04-15 /pmc/articles/PMC9030875/ /pubmed/35456871 http://dx.doi.org/10.3390/microorganisms10040821 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Omar, Naaman M.
Prášil, Ondřej
McCain, J. Scott P.
Campbell, Douglas A.
Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title_full Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title_fullStr Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title_full_unstemmed Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title_short Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H(2)O(2) as a Case Study
title_sort diffusional interactions among marine phytoplankton and bacterioplankton: modelling h(2)o(2) as a case study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9030875/
https://www.ncbi.nlm.nih.gov/pubmed/35456871
http://dx.doi.org/10.3390/microorganisms10040821
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