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Food Microbiology | Spotlight

Task Distribution between Acetate and Acetoin Pathways To Prolong Growth in Lactococcus lactis under Respiration Conditions

Bénédicte Cesselin, Christel Garrigues, Martin B. Pedersen, Célia Roussel, Alexandra Gruss, Philippe Gaudu
Edward G. Dudley, Editor
Bénédicte Cesselin
Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France
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Christel Garrigues
CED-Discovery, Chr. Hansen A/S, Hørsholm, Denmark
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Martin B. Pedersen
CED-Discovery, Chr. Hansen A/S, Hørsholm, Denmark
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Célia Roussel
Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France
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Alexandra Gruss
Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France
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Philippe Gaudu
Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France
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Edward G. Dudley
The Pennsylvania State University
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DOI: 10.1128/AEM.01005-18
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ABSTRACT

Lactococcus lactis is the main bacterium used for food fermentation and is a candidate for probiotic development. In addition to fermentation growth, supplementation with heme under aerobic conditions activates a cytochrome oxidase, which promotes respiration metabolism. In contrast to fermentation, in which cells consume energy to produce mainly lactic acid, respiration metabolism dramatically changes energy metabolism, such that massive amounts of acetic acid and acetoin are produced at the expense of lactic acid. Our goal was to investigate the metabolic changes that correlate with significantly improved growth and survival during respiration growth. Using transcriptional time course analyses, mutational analyses, and promoter-reporter fusions, we uncover two main pathways that can explain the robust growth and stability of respiration cultures. First, the acetate pathway contributes to biomass yield in respiration without affecting medium pH. Second, the acetoin pathway allows cells to cope with internal acidification, which directly affects cell density and survival in stationary phase. Our results suggest that manipulation of these pathways will lead to fine-tuning respiration growth, with improved yield and stability.

IMPORTANCE Lactococcus lactis is used in food and biotechnology industries for its capacity to produce lactic acid, aroma, and proteins. This species grows by fermentation or by an aerobic respiration metabolism when heme is added. Whereas fermentation leads mostly to lactic acid production, respiration produces acetate and acetoin. Respiration growth leads to greatly improved bacterial growth and survival. Our study aims at deciphering mechanisms of respiration metabolism that have a major impact on bacterial physiology. Our results showed that two metabolic pathways (acetate and acetoin) are key elements of respiration. The acetate pathway contributes to biomass yield. The acetoin pathway is needed for pH homeostasis, which affects metabolic activities and bacterial viability in stationary phase. This study clarifies key metabolic elements that are required to maintain the growth advantage conferred by respiration metabolism and has potential uses in strain optimization for industrial and biomedical applications.

FOOTNOTES

    • Received 27 April 2018.
    • Accepted 6 July 2018.
    • Accepted manuscript posted online 20 July 2018.
  • Address correspondence to Philippe Gaudu, philippe.gaudu{at}jouy.inra.fr.
  • ↵* Present address: Martin B. Pedersen, R&D, Sacco SRL, Cadorago, Italy.

  • Citation Cesselin B, Garrigues C, Pedersen MB, Roussel C, Gruss A, Gaudu P. 2018. Task distribution between acetate and acetoin pathways to prolong growth in Lactococcus lactis under respiration conditions. Appl Environ Microbiol 84:e01005-18. https://doi.org/10.1128/AEM.01005-18.

  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01005-18.

  • Copyright © 2018 American Society for Microbiology.

All Rights Reserved.

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Task Distribution between Acetate and Acetoin Pathways To Prolong Growth in Lactococcus lactis under Respiration Conditions
Bénédicte Cesselin, Christel Garrigues, Martin B. Pedersen, Célia Roussel, Alexandra Gruss, Philippe Gaudu
Appl. Environ. Microbiol. Aug 2018, 84 (18) e01005-18; DOI: 10.1128/AEM.01005-18

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Task Distribution between Acetate and Acetoin Pathways To Prolong Growth in Lactococcus lactis under Respiration Conditions
Bénédicte Cesselin, Christel Garrigues, Martin B. Pedersen, Célia Roussel, Alexandra Gruss, Philippe Gaudu
Appl. Environ. Microbiol. Aug 2018, 84 (18) e01005-18; DOI: 10.1128/AEM.01005-18
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KEYWORDS

Lactococcus lactis
respiration
acetate
acetoin
biomass yield
survival
lactic acid bacteria
transcriptome

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