Extracellular electron transfer increases fermentation in lactic acid bacteria via a hybrid metabolism
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Evaluation Summary:
The metabolic, genetic, genomic, and electrochemical experiments described for lactic acid bacteria expand on the recent discovery of extracellular electron transfer in Gram Positive bacteria. The ability to shift and/or accelerate metabolism of lactic acid bacteria capable of extracellular electron transfer may have interesting biotechnological applications, but to what extent this impacts their native physiology is not yet clear.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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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 use of extracellular electron transfer for energy conservation in 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 is dependent on a type-II NADH dehydrogenase (Ndh2) and conditionally requires a flavin-binding extracellular lipoprotein (PplA) under laboratory conditions. It confers increased fermentation product yield, metabolic flux, and environmental acidification in laboratory media and during kale juice fermentation. The discovery of a single pathway that simultaneously blends features of fermentation and respiration in a primarily fermentative microorganism expands our knowledge of energy conservation and provides immediate biotechnology applications.
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Evaluation Summary:
The metabolic, genetic, genomic, and electrochemical experiments described for lactic acid bacteria expand on the recent discovery of extracellular electron transfer in Gram Positive bacteria. The ability to shift and/or accelerate metabolism of lactic acid bacteria capable of extracellular electron transfer may have interesting biotechnological applications, but to what extent this impacts their native physiology is not yet clear.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
In support of the hypothesis that electrons from intracellular metabolism can be diverted to compounds outside the cell, independent experiments quantify electrons transferred to both iron and electrodes (via soluble shuttles), link the process to specific genes, and finds evidence for the ability in related genomes. When poorly fermentable sugar is the substrate, use of external acceptors alters intracellular NAD:NADH and ATP levels dramatically, and at least 20% of the electrons produced from mannitol oxidation can be recovered at electrodes. Extracellular electron transfer also alters fermentation when extracts from raw food (kale) are the substrate. The paper supplies extensive supplementary experiments testing competing hypotheses and related strains.
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Reviewer #2 (Public Review):
Tejedor-Sanz et al. describe the physiology of extracellular electron transfer in lactic acid bacteria. This work builds on previous work in Listeria that identified and characterized a flavin-dependent mechanism for exporting electrons to the cell exterior, which appears to be a widely conserved mechanism in many Gram-positive bacteria. Curiously, extracellular electron transfer does not seem to directly result in cell growth in experiments with L. plantarum, though some aspects of metabolism are accelerated. The ability to shift and/or accelerate metabolism of lactic acid bacteria capable of extracellular electron transfer may have interesting biotechnological applications, but if and to what extent this impacts their native physiology is unclear.
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Reviewer #3 (Public Review):
The authors describe a metabolic strategy in the lactic acid bacterium Lactiplantibacillus plantarum, a primarily fermentative organism, wherein L. plantarum utilizes extracellular electron transfer (EET) to increase its fermentative flux, ATP yield, and growth. The primary claim of the paper is that a novel metabolic strategy has been observed that combines elements of respiratory and fermentative pathways. The authors recently published a study describing flavin-based EET ("FLEET") in the bacterium Listeria monocytogenes and also defined a gene cluster, which is found in diverse bacteria, that is required for this activity. In the current study, the authors describe several experiments, convincingly demonstrating L. plantarum EET, the consequential increase in fermentation, and the requirement for one of …
Reviewer #3 (Public Review):
The authors describe a metabolic strategy in the lactic acid bacterium Lactiplantibacillus plantarum, a primarily fermentative organism, wherein L. plantarum utilizes extracellular electron transfer (EET) to increase its fermentative flux, ATP yield, and growth. The primary claim of the paper is that a novel metabolic strategy has been observed that combines elements of respiratory and fermentative pathways. The authors recently published a study describing flavin-based EET ("FLEET") in the bacterium Listeria monocytogenes and also defined a gene cluster, which is found in diverse bacteria, that is required for this activity. In the current study, the authors describe several experiments, convincingly demonstrating L. plantarum EET, the consequential increase in fermentation, and the requirement for one of the genes in the FLEET cluster--ndh2 (encoding a membrane-bound NADH dehydrogenase)--for EET to occur. However, some of the other findings in the paper are less substantiated. For example, the claim that EET proceeds completely independently of respiration may be overstated, as the experimental methods do not rule out the possibility of other respiratory components playing some role. Additionally, we suggest that the authors minimize the use of the term "FLEET" to describe the L. plantarum system since only a single gene within the proposed FLEET locus (ndh2) is strictly necessary for the mechanism they are studying. Finally, we note that while the physiological relevance is questionable (due to the continuous requirement of an exogenous quinone, even in the kale juice fermentation assay), this study does have broad applications in food science and biotechnology.
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