Protein costs do not explain evolution of metabolic strategies and regulation of ribosomal content: does protein investment explain an anaerobic bacterial Crabtree effect?

A. Goel, T.H. Eckhardt, P. Puri, A. de Jong, F. Santos, M.A. Giera, F. Fusetti, W.M. Vos, J. Kok, B. Poolman, D. Molenaar, O.P. Kuipers, B. Teusink

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Protein investment costs are considered a major driver for the choice of alternative metabolic strategies. We tested this premise in Lactococcus lactis, a bacterium that exhibits a distinct, anaerobic version of the bacterial Crabtree/Warburg effect; with increasing growth rates it shifts from a high yield metabolic mode [mixed-acid fermentation; 3 adenosine triphosphate (ATP) per glucose] to a low yield metabolic mode (homolactic fermentation; 2 ATP per glucose). We studied growth rate-dependent relative transcription and protein ratios, enzyme activities, and fluxes of L.lactis in glucose-limited chemostats, providing a high-quality and comprehensive data set. A three- to fourfold higher growth rate rerouted metabolism from acetate to lactate as the main fermentation product. However, we observed hardly any changes in transcription, protein levels and enzyme activities. Even levels of ribosomal proteins, constituting a major investment in cellular machinery, changed only slightly. Thus, contrary to the original hypothesis, central metabolism in this organism appears to be hardly regulated at the level of gene expression, but rather at the metabolic level. We conclude that L.lactis is either poorly adapted to growth at low and constant glucose concentrations, or that protein costs play a less important role in fitness than hitherto assumed.
Original languageEnglish
Article number1
Pages (from-to)77-92
JournalMolecular Microbiology
Issue number97
DOIs
Publication statusPublished - 2015

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Fermentation
Costs and Cost Analysis
Glucose
Growth
Proteins
Adenosine Triphosphate
Lactococcus lactis
Ribosomal Proteins
Enzymes
Lactic Acid
Acetates
Bacteria
Gene Expression
Acids
Datasets

Cite this

Goel, A. ; Eckhardt, T.H. ; Puri, P. ; de Jong, A. ; Santos, F. ; Giera, M.A. ; Fusetti, F. ; Vos, W.M. ; Kok, J. ; Poolman, B. ; Molenaar, D. ; Kuipers, O.P. ; Teusink, B. / Protein costs do not explain evolution of metabolic strategies and regulation of ribosomal content: does protein investment explain an anaerobic bacterial Crabtree effect?. In: Molecular Microbiology. 2015 ; No. 97. pp. 77-92.
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title = "Protein costs do not explain evolution of metabolic strategies and regulation of ribosomal content: does protein investment explain an anaerobic bacterial Crabtree effect?",
abstract = "Protein investment costs are considered a major driver for the choice of alternative metabolic strategies. We tested this premise in Lactococcus lactis, a bacterium that exhibits a distinct, anaerobic version of the bacterial Crabtree/Warburg effect; with increasing growth rates it shifts from a high yield metabolic mode [mixed-acid fermentation; 3 adenosine triphosphate (ATP) per glucose] to a low yield metabolic mode (homolactic fermentation; 2 ATP per glucose). We studied growth rate-dependent relative transcription and protein ratios, enzyme activities, and fluxes of L.lactis in glucose-limited chemostats, providing a high-quality and comprehensive data set. A three- to fourfold higher growth rate rerouted metabolism from acetate to lactate as the main fermentation product. However, we observed hardly any changes in transcription, protein levels and enzyme activities. Even levels of ribosomal proteins, constituting a major investment in cellular machinery, changed only slightly. Thus, contrary to the original hypothesis, central metabolism in this organism appears to be hardly regulated at the level of gene expression, but rather at the metabolic level. We conclude that L.lactis is either poorly adapted to growth at low and constant glucose concentrations, or that protein costs play a less important role in fitness than hitherto assumed.",
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Protein costs do not explain evolution of metabolic strategies and regulation of ribosomal content: does protein investment explain an anaerobic bacterial Crabtree effect? / Goel, A.; Eckhardt, T.H.; Puri, P.; de Jong, A.; Santos, F.; Giera, M.A.; Fusetti, F.; Vos, W.M.; Kok, J.; Poolman, B.; Molenaar, D.; Kuipers, O.P.; Teusink, B.

In: Molecular Microbiology, No. 97, 1, 2015, p. 77-92.

Research output: Contribution to JournalArticleAcademicpeer-review

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T1 - Protein costs do not explain evolution of metabolic strategies and regulation of ribosomal content: does protein investment explain an anaerobic bacterial Crabtree effect?

AU - Goel, A.

AU - Eckhardt, T.H.

AU - Puri, P.

AU - de Jong, A.

AU - Santos, F.

AU - Giera, M.A.

AU - Fusetti, F.

AU - Vos, W.M.

AU - Kok, J.

AU - Poolman, B.

AU - Molenaar, D.

AU - Kuipers, O.P.

AU - Teusink, B.

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AB - Protein investment costs are considered a major driver for the choice of alternative metabolic strategies. We tested this premise in Lactococcus lactis, a bacterium that exhibits a distinct, anaerobic version of the bacterial Crabtree/Warburg effect; with increasing growth rates it shifts from a high yield metabolic mode [mixed-acid fermentation; 3 adenosine triphosphate (ATP) per glucose] to a low yield metabolic mode (homolactic fermentation; 2 ATP per glucose). We studied growth rate-dependent relative transcription and protein ratios, enzyme activities, and fluxes of L.lactis in glucose-limited chemostats, providing a high-quality and comprehensive data set. A three- to fourfold higher growth rate rerouted metabolism from acetate to lactate as the main fermentation product. However, we observed hardly any changes in transcription, protein levels and enzyme activities. Even levels of ribosomal proteins, constituting a major investment in cellular machinery, changed only slightly. Thus, contrary to the original hypothesis, central metabolism in this organism appears to be hardly regulated at the level of gene expression, but rather at the metabolic level. We conclude that L.lactis is either poorly adapted to growth at low and constant glucose concentrations, or that protein costs play a less important role in fitness than hitherto assumed.

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