Title: Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H

Abstract

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:

Czajka, Jeffrey J.; Abernathy, Mary H.; Benites, Veronica T.; Baidoo, Edward E. K.; Deming, Jody W.; Tang, Yinjie J.

Publication Date:

Fri Nov 16 00:00:00 EST 2018

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1482429

Alternate Identifier(s):

OSTI ID: 1559169

Grant/Contract Number:  

AC02-05CH11231

Resource 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 Volume: 115 Journal Issue: 49; Journal ID: ISSN 0027-8424

Publisher:

National Academy of Sciences, Washington, DC (United States)

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 54 ENVIRONMENTAL SCIENCES; marine psychrophile; metabolic flux; ED pathway; short-chain fatty acids; gluconeogensis