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Glycine betaine uptake and metabolism in marine microbial communities

Glycine betaine (GBT) is a compatible solute in high concentrations in marine microorganisms. As a component of labile organic matter, GBT has complex biochemical potential as a substrate for microbial use that is unconstrained in the environment. Here we determine the uptake kinetics and metabolic...

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Autores principales: Boysen, Angela K., Durham, Bryndan P., Kumler, William, Key, Rebecca S., Heal, Katherine R., Carlson, Laura T., Groussman, Ryan D., Armbrust, E. Virginia, Ingalls, Anitra E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321204/
https://www.ncbi.nlm.nih.gov/pubmed/35466501
http://dx.doi.org/10.1111/1462-2920.16020
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author Boysen, Angela K.
Durham, Bryndan P.
Kumler, William
Key, Rebecca S.
Heal, Katherine R.
Carlson, Laura T.
Groussman, Ryan D.
Armbrust, E. Virginia
Ingalls, Anitra E.
author_facet Boysen, Angela K.
Durham, Bryndan P.
Kumler, William
Key, Rebecca S.
Heal, Katherine R.
Carlson, Laura T.
Groussman, Ryan D.
Armbrust, E. Virginia
Ingalls, Anitra E.
author_sort Boysen, Angela K.
collection PubMed
description Glycine betaine (GBT) is a compatible solute in high concentrations in marine microorganisms. As a component of labile organic matter, GBT has complex biochemical potential as a substrate for microbial use that is unconstrained in the environment. Here we determine the uptake kinetics and metabolic fate of GBT in two natural microbial communities in the North Pacific characterized by different nitrate concentrations. Dissolved GBT had maximum uptake rates of 0.36 and 0.56 nM h(−1) with half‐saturation constants of 79 and 11 nM in the high nitrate and low nitrate stations respectively. During multiday incubations, most GBT taken into cells was retained as a compatible solute. Stable isotopes derived from the added GBT were also observed in other metabolites, including choline, carnitine and sarcosine, suggesting that GBT was used for biosynthesis and for catabolism to pyruvate and ammonium. Where nitrate was scarce, GBT was primarily metabolized via demethylation to glycine. Gene transcript data were consistent with SAR11 using GBT as a source of methyl groups to fuel the methionine cycle. Where nitrate concentrations were higher, more GBT was partitioned for lipid biosynthesis by both bacteria and eukaryotic phytoplankton. Our data highlight unexpected metabolic pathways and potential routes of microbial metabolite exchange.
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spelling pubmed-93212042022-07-30 Glycine betaine uptake and metabolism in marine microbial communities Boysen, Angela K. Durham, Bryndan P. Kumler, William Key, Rebecca S. Heal, Katherine R. Carlson, Laura T. Groussman, Ryan D. Armbrust, E. Virginia Ingalls, Anitra E. Environ Microbiol Research Articles Glycine betaine (GBT) is a compatible solute in high concentrations in marine microorganisms. As a component of labile organic matter, GBT has complex biochemical potential as a substrate for microbial use that is unconstrained in the environment. Here we determine the uptake kinetics and metabolic fate of GBT in two natural microbial communities in the North Pacific characterized by different nitrate concentrations. Dissolved GBT had maximum uptake rates of 0.36 and 0.56 nM h(−1) with half‐saturation constants of 79 and 11 nM in the high nitrate and low nitrate stations respectively. During multiday incubations, most GBT taken into cells was retained as a compatible solute. Stable isotopes derived from the added GBT were also observed in other metabolites, including choline, carnitine and sarcosine, suggesting that GBT was used for biosynthesis and for catabolism to pyruvate and ammonium. Where nitrate was scarce, GBT was primarily metabolized via demethylation to glycine. Gene transcript data were consistent with SAR11 using GBT as a source of methyl groups to fuel the methionine cycle. Where nitrate concentrations were higher, more GBT was partitioned for lipid biosynthesis by both bacteria and eukaryotic phytoplankton. Our data highlight unexpected metabolic pathways and potential routes of microbial metabolite exchange. John Wiley & Sons, Inc. 2022-05-06 2022-05 /pmc/articles/PMC9321204/ /pubmed/35466501 http://dx.doi.org/10.1111/1462-2920.16020 Text en © 2022 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. 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 Research Articles
Boysen, Angela K.
Durham, Bryndan P.
Kumler, William
Key, Rebecca S.
Heal, Katherine R.
Carlson, Laura T.
Groussman, Ryan D.
Armbrust, E. Virginia
Ingalls, Anitra E.
Glycine betaine uptake and metabolism in marine microbial communities
title Glycine betaine uptake and metabolism in marine microbial communities
title_full Glycine betaine uptake and metabolism in marine microbial communities
title_fullStr Glycine betaine uptake and metabolism in marine microbial communities
title_full_unstemmed Glycine betaine uptake and metabolism in marine microbial communities
title_short Glycine betaine uptake and metabolism in marine microbial communities
title_sort glycine betaine uptake and metabolism in marine microbial communities
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321204/
https://www.ncbi.nlm.nih.gov/pubmed/35466501
http://dx.doi.org/10.1111/1462-2920.16020
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