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Title: 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 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 pathwaymore » 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.« less
Authors:
; ; ; ; ;
Publication Date:
Grant/Contract Number:
AC02-05CH11231
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
OSTI Identifier:
1482429

Czajka, Jeffrey J., Abernathy, Mary H., Benites, Veronica T., Baidoo, Edward E. K., Deming, Jody W., and Tang, Yinjie J.. Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H. United States: N. p., Web. doi:10.1073/pnas.1807804115.
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. United States. doi:10.1073/pnas.1807804115.
Czajka, Jeffrey J., Abernathy, Mary H., Benites, Veronica T., Baidoo, Edward E. K., Deming, Jody W., and Tang, Yinjie J.. 2018. "Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H". United States. doi:10.1073/pnas.1807804115.
@article{osti_1482429,
title = {Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H},
author = {Czajka, Jeffrey J. and Abernathy, Mary H. and Benites, Veronica T. and Baidoo, Edward E. K. and Deming, Jody W. and Tang, Yinjie J.},
abstractNote = {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 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. We suggest that marine heterotrophic bacteria in general may rely upon simplified metabolic strategies to overcome thermodynamic constraints and thrive in the cold ocean.},
doi = {10.1073/pnas.1807804115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = ,
volume = ,
place = {United States},
year = {2018},
month = {11}
}

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Propane Respiration Jump-Starts Microbial Response to a Deep Oil Spill
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