Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H
Colwellia psychrerythraea 34H is a model psychrophilic bacterium found in the cold ocean—polar sediments, sea ice, and the deep sea. Although the genomes of such psychrophiles have been sequenced, their metabolic strategies at low temperature have not been quantified. In this work, we measured the m...
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ftosti:oai:osti.gov:1559169 2023-07-30T04:06:47+02:00 Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H Czajka, Jeffrey J. Abernathy, Mary H. Benites, Veronica T. Baidoo, Edward E. K. Deming, Jody W. Tang, Yinjie J. 2021-10-27 application/pdf http://www.osti.gov/servlets/purl/1559169 https://www.osti.gov/biblio/1559169 https://doi.org/10.1073/pnas.1807804115 unknown http://www.osti.gov/servlets/purl/1559169 https://www.osti.gov/biblio/1559169 https://doi.org/10.1073/pnas.1807804115 doi:10.1073/pnas.1807804115 59 BASIC BIOLOGICAL SCIENCES 37 INORGANIC ORGANIC PHYSICAL AND ANALYTICAL CHEMISTRY 54 ENVIRONMENTAL SCIENCES 2021 ftosti https://doi.org/10.1073/pnas.1807804115 2023-07-11T09:36:28Z Colwellia psychrerythraea 34H is a model psychrophilic bacterium found in the cold ocean—polar sediments, sea ice, and the deep sea. Although the genomes of such psychrophiles have been sequenced, their metabolic strategies at low temperature have not been quantified. In this work, we measured the metabolic fluxes and gene expression of 34H at 4 °C (the mean global-ocean temperature and a normal-growth temperature for 34H), making comparative analyses at room temperature (above its upper-growth temperature of 18 °C) and with mesophilic Escherichia coli . When grown at 4 °C, 34H utilized multiple carbon substrates without catabolite repression or overflow byproducts; its anaplerotic pathways increased flux network flexibility and enabled CO 2 fixation. In glucose-only medium, the Entner–Doudoroff (ED) pathway was the primary glycolytic route; in lactate-only medium, gluconeogenesis and the glyoxylate shunt became active. In comparison, E. coli , cold stressed at 4 °C, had rapid glycolytic fluxes but no biomass synthesis. At their respective normal-growth temperatures, intracellular concentrations of TCA cycle metabolites (α-ketoglutarate, succinate, malate) were 4–17 times higher in 34H than in E. coli , while levels of energy molecules (ATP, NADH, NADPH) were 10- to 100-fold lower. Experiments with E. coli mutants supported the thermodynamic advantage of the ED pathway at cold temperature. Heat-stressed 34H at room temperature (2 hours) revealed significant down-regulation of genes associated with glycolytic enzymes and flagella, while 24 hours at room temperature caused irreversible cellular damage. Lastly, we suggest that marine heterotrophic bacteria in general may rely upon simplified metabolic strategies to overcome thermodynamic constraints and thrive in the cold ocean. Other/Unknown Material Sea ice SciTec Connect (Office of Scientific and Technical Information - OSTI, U.S. Department of Energy) Proceedings of the National Academy of Sciences 115 49 12507 12512 |
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SciTec Connect (Office of Scientific and Technical Information - OSTI, U.S. Department of Energy) |
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59 BASIC BIOLOGICAL SCIENCES 37 INORGANIC ORGANIC PHYSICAL AND ANALYTICAL CHEMISTRY 54 ENVIRONMENTAL SCIENCES |
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59 BASIC BIOLOGICAL SCIENCES 37 INORGANIC ORGANIC PHYSICAL AND ANALYTICAL CHEMISTRY 54 ENVIRONMENTAL SCIENCES Czajka, Jeffrey J. Abernathy, Mary H. Benites, Veronica T. Baidoo, Edward E. K. Deming, Jody W. Tang, Yinjie J. Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
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59 BASIC BIOLOGICAL SCIENCES 37 INORGANIC ORGANIC PHYSICAL AND ANALYTICAL CHEMISTRY 54 ENVIRONMENTAL SCIENCES |
description |
Colwellia psychrerythraea 34H is a model psychrophilic bacterium found in the cold ocean—polar sediments, sea ice, and the deep sea. Although the genomes of such psychrophiles have been sequenced, their metabolic strategies at low temperature have not been quantified. In this work, we measured the metabolic fluxes and gene expression of 34H at 4 °C (the mean global-ocean temperature and a normal-growth temperature for 34H), making comparative analyses at room temperature (above its upper-growth temperature of 18 °C) and with mesophilic Escherichia coli . When grown at 4 °C, 34H utilized multiple carbon substrates without catabolite repression or overflow byproducts; its anaplerotic pathways increased flux network flexibility and enabled CO 2 fixation. In glucose-only medium, the Entner–Doudoroff (ED) pathway was the primary glycolytic route; in lactate-only medium, gluconeogenesis and the glyoxylate shunt became active. In comparison, E. coli , cold stressed at 4 °C, had rapid glycolytic fluxes but no biomass synthesis. At their respective normal-growth temperatures, intracellular concentrations of TCA cycle metabolites (α-ketoglutarate, succinate, malate) were 4–17 times higher in 34H than in E. coli , while levels of energy molecules (ATP, NADH, NADPH) were 10- to 100-fold lower. Experiments with E. coli mutants supported the thermodynamic advantage of the ED pathway at cold temperature. Heat-stressed 34H at room temperature (2 hours) revealed significant down-regulation of genes associated with glycolytic enzymes and flagella, while 24 hours at room temperature caused irreversible cellular damage. Lastly, we suggest that marine heterotrophic bacteria in general may rely upon simplified metabolic strategies to overcome thermodynamic constraints and thrive in the cold ocean. |
author |
Czajka, Jeffrey J. Abernathy, Mary H. Benites, Veronica T. Baidoo, Edward E. K. Deming, Jody W. Tang, Yinjie J. |
author_facet |
Czajka, Jeffrey J. Abernathy, Mary H. Benites, Veronica T. Baidoo, Edward E. K. Deming, Jody W. Tang, Yinjie J. |
author_sort |
Czajka, Jeffrey J. |
title |
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
title_short |
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
title_full |
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
title_fullStr |
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
title_full_unstemmed |
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H |
title_sort |
model metabolic strategy for heterotrophic bacteria in the cold ocean based on colwellia psychrerythraea 34h |
publishDate |
2021 |
url |
http://www.osti.gov/servlets/purl/1559169 https://www.osti.gov/biblio/1559169 https://doi.org/10.1073/pnas.1807804115 |
genre |
Sea ice |
genre_facet |
Sea ice |
op_relation |
http://www.osti.gov/servlets/purl/1559169 https://www.osti.gov/biblio/1559169 https://doi.org/10.1073/pnas.1807804115 doi:10.1073/pnas.1807804115 |
op_doi |
https://doi.org/10.1073/pnas.1807804115 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
115 |
container_issue |
49 |
container_start_page |
12507 |
op_container_end_page |
12512 |
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1772819700382695424 |