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Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

The concept of biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Microbial biomass is usually assumed to grow by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Resource investment in storage allow...

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Autores principales: Mason-Jones, Kyle, Breidenbach, Andreas, Dyckmans, Jens, Banfield, Callum C., Dippold, Michaela A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10115882/
https://www.ncbi.nlm.nih.gov/pubmed/37076457
http://dx.doi.org/10.1038/s41467-023-37713-4
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author Mason-Jones, Kyle
Breidenbach, Andreas
Dyckmans, Jens
Banfield, Callum C.
Dippold, Michaela A.
author_facet Mason-Jones, Kyle
Breidenbach, Andreas
Dyckmans, Jens
Banfield, Callum C.
Dippold, Michaela A.
author_sort Mason-Jones, Kyle
collection PubMed
description The concept of biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Microbial biomass is usually assumed to grow by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Resource investment in storage allows microbes to decouple their metabolic activity from immediate resource supply, supporting more diverse microbial responses to environmental changes. Here we show that microbial C storage in the form of triacylglycerides (TAGs) and polyhydroxybutyrate (PHB) contributes significantly to the formation of new biomass, i.e. growth, under contrasting conditions of C availability and complementary nutrient supply in soil. Together these compounds can comprise a C pool 0.19 ± 0.03 to 0.46 ± 0.08 times as large as extractable soil microbial biomass and reveal up to 279 ± 72% more biomass growth than observed by a DNA-based method alone. Even under C limitation, storage represented an additional 16–96% incorporation of added C into microbial biomass. These findings encourage greater recognition of storage synthesis as a key pathway of biomass growth and an underlying mechanism for resistance and resilience of microbial communities facing environmental change.
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spelling pubmed-101158822023-04-21 Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth Mason-Jones, Kyle Breidenbach, Andreas Dyckmans, Jens Banfield, Callum C. Dippold, Michaela A. Nat Commun Article The concept of biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Microbial biomass is usually assumed to grow by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Resource investment in storage allows microbes to decouple their metabolic activity from immediate resource supply, supporting more diverse microbial responses to environmental changes. Here we show that microbial C storage in the form of triacylglycerides (TAGs) and polyhydroxybutyrate (PHB) contributes significantly to the formation of new biomass, i.e. growth, under contrasting conditions of C availability and complementary nutrient supply in soil. Together these compounds can comprise a C pool 0.19 ± 0.03 to 0.46 ± 0.08 times as large as extractable soil microbial biomass and reveal up to 279 ± 72% more biomass growth than observed by a DNA-based method alone. Even under C limitation, storage represented an additional 16–96% incorporation of added C into microbial biomass. These findings encourage greater recognition of storage synthesis as a key pathway of biomass growth and an underlying mechanism for resistance and resilience of microbial communities facing environmental change. Nature Publishing Group UK 2023-04-19 /pmc/articles/PMC10115882/ /pubmed/37076457 http://dx.doi.org/10.1038/s41467-023-37713-4 Text en © The Author(s) 2023 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
Mason-Jones, Kyle
Breidenbach, Andreas
Dyckmans, Jens
Banfield, Callum C.
Dippold, Michaela A.
Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title_full Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title_fullStr Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title_full_unstemmed Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title_short Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
title_sort intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10115882/
https://www.ncbi.nlm.nih.gov/pubmed/37076457
http://dx.doi.org/10.1038/s41467-023-37713-4
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