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Extracellular electron transfer increases fermentation in lactic acid bacteria via a hybrid metabolism

View ORCID ProfileSara Tejedor-Sanz, Eric T. Stevens, Peter Finnegan, James Nelson, Andre Knoessen, View ORCID ProfileSamuel H. Light, View ORCID ProfileCaroline M. Ajo-Franklin, View ORCID ProfileMaria L. Marco
doi: https://doi.org/10.1101/2021.05.26.445846
Sara Tejedor-Sanz
1Department of Biosciences, Rice University, Houston, United States
2Biological Nanostructures Facility, The Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, United States
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Eric T. Stevens
3Department of Food Science & Technology, University of California-Davis, Davis, United States
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Peter Finnegan
3Department of Food Science & Technology, University of California-Davis, Davis, United States
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James Nelson
4Department of Electrical and Computer Engineering, University of California-Davis, Davis, United States
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Andre Knoessen
4Department of Electrical and Computer Engineering, University of California-Davis, Davis, United States
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Samuel H. Light
5Department of Microbiology, University of Chicago, Chicago, United States
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Caroline M. Ajo-Franklin
1Department of Biosciences, Rice University, Houston, United States
2Biological Nanostructures Facility, The Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, United States
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Maria L. Marco
3Department of Food Science & Technology, University of California-Davis, Davis, United States
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  • For correspondence: [email protected] [email protected]
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ABSTRACT

Energy conservation in microorganisms is classically categorized into respiration and fermentation, however recent work shows some species can use mixed or alternative bioenergetic strategies. We explored the utility of a flavin-based extracellular electron transport (FLEET) system for energy conservation within diverse lactic acid bacteria (LAB), microorganisms that mainly rely on fermentative metabolism and are important in food fermentations. The LAB Lactiplantibacillus plantarum uses extracellular electron transfer to increase its NAD+/NADH ratio, generate more ATP through substrate-level phosphorylation and accumulate biomass more rapidly. This novel, hybrid metabolism was dependent on a type-II NADH dehydrogenase (Ndh2) and conditionally required a flavin-binding extracellular lipoprotein (PplA) in the FLEET system to confer increased fermentation yield, metabolic flux, and environmental acidification in both laboratory media and food fermentation. The discovery of a single pathway that blends features of fermentation and respiration expands our knowledge of energy conservation metabolism and provides immediate biotechnology applications.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://dataverse.harvard.edu/dataset.xhtml?persistentId=doi:10.7910/DVN/IHKI0C

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 26, 2021.
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Extracellular electron transfer increases fermentation in lactic acid bacteria via a hybrid metabolism
Sara Tejedor-Sanz, Eric T. Stevens, Peter Finnegan, James Nelson, Andre Knoessen, Samuel H. Light, Caroline M. Ajo-Franklin, Maria L. Marco
bioRxiv 2021.05.26.445846; doi: https://doi.org/10.1101/2021.05.26.445846
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Extracellular electron transfer increases fermentation in lactic acid bacteria via a hybrid metabolism
Sara Tejedor-Sanz, Eric T. Stevens, Peter Finnegan, James Nelson, Andre Knoessen, Samuel H. Light, Caroline M. Ajo-Franklin, Maria L. Marco
bioRxiv 2021.05.26.445846; doi: https://doi.org/10.1101/2021.05.26.445846

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