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Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis

Primary productivity occurs throughout the deep euphotic zone of the oligotrophic South Pacific Gyre (SPG), fueled largely by the regeneration of nutrients and thus recycling of organic matter. We investigated the heterotrophic capabilities of the SPG’s bacterial communities by examining their abili...

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Autores principales: Reintjes, Greta, Fuchs, Bernhard M., Amann, Rudolf, Arnosti, Carol
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775370/
https://www.ncbi.nlm.nih.gov/pubmed/33391202
http://dx.doi.org/10.3389/fmicb.2020.583158
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author Reintjes, Greta
Fuchs, Bernhard M.
Amann, Rudolf
Arnosti, Carol
author_facet Reintjes, Greta
Fuchs, Bernhard M.
Amann, Rudolf
Arnosti, Carol
author_sort Reintjes, Greta
collection PubMed
description Primary productivity occurs throughout the deep euphotic zone of the oligotrophic South Pacific Gyre (SPG), fueled largely by the regeneration of nutrients and thus recycling of organic matter. We investigated the heterotrophic capabilities of the SPG’s bacterial communities by examining their ability to process polysaccharides, an important component of marine organic matter. We focused on the initial step of organic matter degradation by measuring the activities of extracellular enzymes that hydrolyze six different polysaccharides to smaller sizes. This process can occur by two distinct mechanisms: “selfish uptake,” in which initial hydrolysis is coupled to transport of large polysaccharide fragments into the periplasmic space of bacteria, with little to no loss of hydrolysis products to the external environment, and “external hydrolysis,” in which low molecular weight (LMW) hydrolysis products are produced in the external environment. Given the oligotrophic nature of the SPG, we did not expect high enzymatic activity; however, we found that all six polysaccharides were hydrolyzed externally and taken up selfishly in the central SPG, observations that may be linked to a comparatively high abundance of diatoms at the depth and location sampled (75 m). At the edge of the gyre and close to the center of the gyre, four of six polysaccharides were externally hydrolyzed, and a lower fraction of the bacterial community showed selfish uptake. One polysaccharide (fucoidan) was selfishly taken up without measurable external hydrolysis at two stations. Additional incubations of central gyre water from depths of 1,250 and 2,800 m with laminarin (an abundant polysaccharide in the ocean) led to extreme growth of opportunistic bacteria (Alteromonas), as tracked by cell counts and next generation sequencing of the bacterial communities. These Alteromonas appear to concurrently selfishly take up laminarin and release LMW hydrolysis products. Overall, extracellular enzyme activities in the SPG were similar to activities in non-oligotrophic regions, and a considerable fraction of the community was capable of selfish uptake at all three stations. A diverse set of bacteria responded to and are potentially important for the recycling of organic matter in the SPG.
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spelling pubmed-77753702021-01-02 Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis Reintjes, Greta Fuchs, Bernhard M. Amann, Rudolf Arnosti, Carol Front Microbiol Microbiology Primary productivity occurs throughout the deep euphotic zone of the oligotrophic South Pacific Gyre (SPG), fueled largely by the regeneration of nutrients and thus recycling of organic matter. We investigated the heterotrophic capabilities of the SPG’s bacterial communities by examining their ability to process polysaccharides, an important component of marine organic matter. We focused on the initial step of organic matter degradation by measuring the activities of extracellular enzymes that hydrolyze six different polysaccharides to smaller sizes. This process can occur by two distinct mechanisms: “selfish uptake,” in which initial hydrolysis is coupled to transport of large polysaccharide fragments into the periplasmic space of bacteria, with little to no loss of hydrolysis products to the external environment, and “external hydrolysis,” in which low molecular weight (LMW) hydrolysis products are produced in the external environment. Given the oligotrophic nature of the SPG, we did not expect high enzymatic activity; however, we found that all six polysaccharides were hydrolyzed externally and taken up selfishly in the central SPG, observations that may be linked to a comparatively high abundance of diatoms at the depth and location sampled (75 m). At the edge of the gyre and close to the center of the gyre, four of six polysaccharides were externally hydrolyzed, and a lower fraction of the bacterial community showed selfish uptake. One polysaccharide (fucoidan) was selfishly taken up without measurable external hydrolysis at two stations. Additional incubations of central gyre water from depths of 1,250 and 2,800 m with laminarin (an abundant polysaccharide in the ocean) led to extreme growth of opportunistic bacteria (Alteromonas), as tracked by cell counts and next generation sequencing of the bacterial communities. These Alteromonas appear to concurrently selfishly take up laminarin and release LMW hydrolysis products. Overall, extracellular enzyme activities in the SPG were similar to activities in non-oligotrophic regions, and a considerable fraction of the community was capable of selfish uptake at all three stations. A diverse set of bacteria responded to and are potentially important for the recycling of organic matter in the SPG. Frontiers Media S.A. 2020-12-18 /pmc/articles/PMC7775370/ /pubmed/33391202 http://dx.doi.org/10.3389/fmicb.2020.583158 Text en Copyright © 2020 Reintjes, Fuchs, Amann and Arnosti. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Reintjes, Greta
Fuchs, Bernhard M.
Amann, Rudolf
Arnosti, Carol
Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title_full Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title_fullStr Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title_full_unstemmed Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title_short Extensive Microbial Processing of Polysaccharides in the South Pacific Gyre via Selfish Uptake and Extracellular Hydrolysis
title_sort extensive microbial processing of polysaccharides in the south pacific gyre via selfish uptake and extracellular hydrolysis
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775370/
https://www.ncbi.nlm.nih.gov/pubmed/33391202
http://dx.doi.org/10.3389/fmicb.2020.583158
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