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. We measured the metabolic fluxe...
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ftcdlib:oai:escholarship.org/ark:/13030/qt8ms5490n 2023-05-15T18:18:42+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 EK Deming, Jody W Tang, Yinjie J 12507 - 12512 2018-12-01 https://escholarship.org/uc/item/8ms5490n unknown eScholarship, University of California qt8ms5490n https://escholarship.org/uc/item/8ms5490n public Proceedings of the National Academy of Sciences of the United States of America, vol 115, iss 49 Alteromonadaceae Energy Metabolism Models Biological Oceans and Seas Heterotrophic Processes Cold Temperature ED pathway gluconeogensis marine psychrophile metabolic flux short-chain fatty acids MD Multidisciplinary article 2018 ftcdlib 2021-01-24T17:38:27Z 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. 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 CO2 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. We suggest that marine heterotrophic bacteria in general may rely upon simplified metabolic strategies to overcome thermodynamic constraints and thrive in the cold ocean. Article in Journal/Newspaper Sea ice University of California: eScholarship |
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Open Polar |
collection |
University of California: eScholarship |
op_collection_id |
ftcdlib |
language |
unknown |
topic |
Alteromonadaceae Energy Metabolism Models Biological Oceans and Seas Heterotrophic Processes Cold Temperature ED pathway gluconeogensis marine psychrophile metabolic flux short-chain fatty acids MD Multidisciplinary |
spellingShingle |
Alteromonadaceae Energy Metabolism Models Biological Oceans and Seas Heterotrophic Processes Cold Temperature ED pathway gluconeogensis marine psychrophile metabolic flux short-chain fatty acids MD Multidisciplinary Czajka, Jeffrey J Abernathy, Mary H Benites, Veronica T Baidoo, Edward EK Deming, Jody W Tang, Yinjie J Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H. |
topic_facet |
Alteromonadaceae Energy Metabolism Models Biological Oceans and Seas Heterotrophic Processes Cold Temperature ED pathway gluconeogensis marine psychrophile metabolic flux short-chain fatty acids MD Multidisciplinary |
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. 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 CO2 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. We suggest that marine heterotrophic bacteria in general may rely upon simplified metabolic strategies to overcome thermodynamic constraints and thrive in the cold ocean. |
format |
Article in Journal/Newspaper |
author |
Czajka, Jeffrey J Abernathy, Mary H Benites, Veronica T Baidoo, Edward EK Deming, Jody W Tang, Yinjie J |
author_facet |
Czajka, Jeffrey J Abernathy, Mary H Benites, Veronica T Baidoo, Edward EK 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. |
publisher |
eScholarship, University of California |
publishDate |
2018 |
url |
https://escholarship.org/uc/item/8ms5490n |
op_coverage |
12507 - 12512 |
genre |
Sea ice |
genre_facet |
Sea ice |
op_source |
Proceedings of the National Academy of Sciences of the United States of America, vol 115, iss 49 |
op_relation |
qt8ms5490n https://escholarship.org/uc/item/8ms5490n |
op_rights |
public |
_version_ |
1766195365657182208 |