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

Tejedor-Sanz, Sara; Et, Stevens; Finnegan, Peter; Nelson, James T.; Knoessen, A; Sh, Light; Ajo‐Franklin, Caroline M.; Marco, Maria L.

doi:10.1101/2021.05.26.445846

Cited by 9 publications

(27 citation statements)

References 114 publications

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“…Dynamic binding between eDNA and electron shuttles in oxidized or reduced states accelerates electron exchange. During food fermentation, some LAB, including Lactiplantibacillus plantarum , were found to use a hybrid strategy to conserve energy, in that the LAB used extracellular electron transfer to increase the NAD+/NADH ratio and then generated more ATP through substrate‐level phosphorylation (Tejedor‐Sanz et al., 2022). This suggested a regulatory approach using extracellular electron transfer to modulate the microbial biomass, metabolic flux, product yield, and flavor profiles of fermented foods.…”

Section: Microbial Interactions In Multispecies Biofilmsmentioning

confidence: 99%

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

Yao

Hao

Zhou

et al. 2022

Comp Rev Food Sci Food Safe

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Food fermentation is driven by microorganisms, which usually coexist as multispecies biofilms. The activities and interactions of functional microorganisms and pathogenic bacteria in biofilms have important implications for the quality and safety of fermented foods. It was verified that the biofilm lifestyle benefited the fitness of microorganisms in harsh environments and intensified the cooperation and competition between biofilm members. This review focuses on multispecies biofilm formation, microbial interactions and communication in biofilms, and the application of multispecies biofilms in food fermentation. Microbial aggregation and adhesion are important steps in the early stage of multispecies biofilm formation. Different biofilm-forming abilities and strategies among microorganisms lead to several types of multispecies biofilm formation. The spatial distribution of multispecies biofilms reflects microbial interactions and biofilm function. Then, we discuss the intrinsic factors and external manifestations of multispecies biofilm system succession. Several typical interspecies cooperation and competition modes and mechanisms of microbial communication were reviewed in this review. The main limitations of the studies included in this review are the relatively small number of studies of biofilms formed by functional microorganisms during fermentation and the lack of direct evidence for the formation process of multispecies biofilms and microbial interactions and communication within biofilms. This review aims to provide the food industry with a sufficient understanding of multispecies biofilms in food fermentation.

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Section: Microbial Interactions In Multispecies Biofilmsmentioning

confidence: 99%

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

Yao

Hao

Zhou

et al. 2022

Comp Rev Food Sci Food Safe

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“…This allowed us and others to identify other Gram-positive microbes capable of EET, including Enterococcus faecalis and Lactiplantibacillus plantarum . 5,7–9 At present, however, it is not understood how exclusively fermentative microbes, such as L. plantarum and E. faecalis , can utilize and maintain an EET pathway, especially when a traditional respiratory system is not maintained. Elucidating this phenomenon and its influence on organismal physiology is of great importance due to the prevalence of these Gram-positive bacteria in agriculture, bioremediation, food production, gut health, and opportunistic human infections.…”

Section: Introductionmentioning

confidence: 99%

“…We recently showed that the genus Lactiplantibacillus has a highly conserved FLEET locus and many of its members exhibit EET activity. 9 The FLEET locus encodes a type-II NADH dehydrogenase (Ndh2), flavin transport proteins (FmnA/B and ATPase1/2), membrane demethylmenaquinone (DMK) synthesis proteins (DmkA and EetB/DmkB), and electron transfer proteins (PplA and EetA). 7–9 An exogenous menaquinone (MK) precursor, 1,4-dihydroxy-2-naphthoate (DHNA), was added to allow the microbe to synthesize MK or DMK.…”

Section: Introductionmentioning

confidence: 99%

“…9 The FLEET locus encodes a type-II NADH dehydrogenase (Ndh2), flavin transport proteins (FmnA/B and ATPase1/2), membrane demethylmenaquinone (DMK) synthesis proteins (DmkA and EetB/DmkB), and electron transfer proteins (PplA and EetA). 7–9 An exogenous menaquinone (MK) precursor, 1,4-dihydroxy-2-naphthoate (DHNA), was added to allow the microbe to synthesize MK or DMK. When both an electron acceptor (ferric iron or an artificial electrode) and DHNA were provided, EET activity was observed in L. plantarum .…”

Section: Introductionmentioning

confidence: 99%

“…Closer analysis of the FLEET locus across L. plantarum strains found that transposon insertions in either ndh2 or pplA caused a loss of EET activity. 9 While establishing the importance of riboflavin and DHNA in EET in L. plantarum , the precise role of these molecules in extracellular electron transfer remains unclear.…”

Section: Introductionmentioning

confidence: 99%

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The differing roles of flavins and quinones in extracellular electron transfer in Lactiplantibacillus plantarum

Tolar

Ajo‐Franklin

2022

Preprint

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Lactiplantibacillus plantarum is a homofermentative lactic acid bacteria that is commonly found in the human gut and fermented food products. Despite its overwhelmingly fermentative metabolism, this microbe can perform extracellular electron transfer (EET) when provided with an exogenous quinone, 1,4-dihydroxy-2-naphthoic acid (DHNA) and riboflavin. However, the separate roles of DHNA and riboflavin in EET in L. plantarum has remained unclear. Here we seek to understand the role of quinones and flavins for EET by monitoring iron and anode reduction in the presence and absence of these small molecules. We found that either addition of DHNA or riboflavin can support robust iron reduction, indicating electron transfer to extracellular iron occurs through both flavin-dependent and DHNA-dependent routes. Using genetic mutants of L. plantarum, we found that flavin-dependent iron reduction requires Ndh2 and EetA, while DHNA-dependent iron reduction largely relies on Ndh2 and PplA. In contrast to iron reduction, DHNA-containing media supported more robust anode reduction than riboflavin-containing media, suggesting electron transfer to an anode proceeds most efficiently through the DHNA-dependent pathway. Furthermore, we found that flavin-dependent anode reduction requires EetA, Ndh2, and PplA, while DHNA-dependent anode reduction requires Ndh2 and PplA. Taken together, we identify multiple EET routes utilized by L. plantarum and show that the EET route depends on access to environmental biomolecules and on the extracellular electron acceptor. This work expands our molecular-level understanding of EET in Gram-positive microbes and provides additional opportunities to manipulate EET for biotechnology.

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Distinct energy-coupling factor transporter subunits enable flavin acquisition and extracytosolic trafficking for extracellular electron transfer inListeria monocytogenes

Rivera‐Lugo

Huang

Lee

et al. 2022

Preprint

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A variety of electron transfer mechanisms link bacterial cytosolic electron pools with functionally diverse redox activities in the cell envelope and extracellular space. InListeria monocytogenes, the ApbE-like enzyme FmnB catalyzes extracytosolic protein flavinylation, covalently linking a flavin cofactor to proteins that transfer electrons to extracellular acceptors.L. monocytogenesuses an energy-coupling factor (ECF) transporter complex that contains distinct substrate-binding, transmembrane, ATPase A, and ATPase A' subunits (RibU, EcfT, EcfA, and EcfA') to import environmental flavins, but the basis of extracytosolic flavin trafficking for FmnB flavinylation remains poorly defined. In this study, we show that the proteins EetB and FmnA are related to ECF transporter substrate-binding and transmembrane subunits, respectively, and are essential for exporting flavins from the cytosol for flavinylation. Comparisons of the flavin import versus export capabilities ofL. monocytogenesstrains lacking different ECF transporter subunits demonstrates a strict directionality of substrate-binding subunit transport but partial functional redundancy of transmembrane and ATPase subunits. Based on these results, we propose that ECF transporter complexes with different subunit compositions execute directional flavin import/export through a broadly conserved mechanism. Finally, we present genomic context analyses which show that related ECF exporter genes are distributed across the Firmicutes phylum and frequently co-localize with genes encoding flavinylated extracytosolic proteins. These findings clarify the basis of ECF transporter export and extracytosolic flavin cofactor trafficking in Firmicutes.

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

Cited by 9 publications

References 114 publications

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

The differing roles of flavins and quinones in extracellular electron transfer in Lactiplantibacillus plantarum

Distinct energy-coupling factor transporter subunits enable flavin acquisition and extracytosolic trafficking for extracellular electron transfer inListeria monocytogenes

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