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

Tejedor-Sanz, Sara; Stevens, Eric; Li, Siliang; Finnegan, Peter; Nelson, James T.; Knoesen, A.; Light, S.H.; Ajo‐Franklin, Caroline M.; Marco, Maria L.

doi:10.7554/elife.70684

Cited by 49 publications

(88 citation statements)

References 119 publications

(131 reference statements)

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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: Cross-respiration and Extracellular Electron Transfermentioning

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: Cross-respiration and Extracellular Electron Transfermentioning

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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“…Lactic acid bacteria represent a family of non-pathogenic, non-sporulating, microaerophilic, Gram-positive bacteria that produce lactic acid as the major end resultant during carbohydrate fermentation and have been employed in food supplements, medicines, and cosmetics for ages to promote modern human civilization [1,2]. LAB are generally recognized as safe (GRAS) and due to this status, these food-grade Gram-positive bacteria have been used as starter cultures for food fermentation and as cell factories for the production of various macromolecules, enzymes, and relevant metabolites in the food, pharmaceutical, and dietary supplement industries [3][4][5][6][7].…”

Section: Introductionmentioning

confidence: 99%

Plasmid-Based Gene Expression Systems for Lactic Acid Bacteria: A Review

et al. 2022

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Lactic acid bacteria (LAB) play a very vital role in food production, preservation, and as probiotic agents. Some of these species can colonize and survive longer in the gastrointestinal tract (GIT), where their presence is crucially helpful to promote human health. LAB has also been used as a safe and efficient incubator to produce proteins of interest. With the advent of genetic engineering, recombinant LAB have been effectively employed as vectors for delivering therapeutic molecules to mucosal tissues of the oral, nasal, and vaginal tracks and for shuttling therapeutics for diabetes, cancer, viral infections, and several gastrointestinal infections. The most important tool needed to develop genetically engineered LABs to produce proteins of interest is a plasmid-based gene expression system. To date, a handful of constitutive and inducible vectors for LAB have been developed, but their limited availability, host specificity, instability, and low carrying capacity have narrowed their spectrum of applications. The current review discusses the plasmid-based vectors that have been developed so far for LAB; their functionality, potency, and constraints; and further highlights the need for a new, more stable, and effective gene expression platform for LAB.

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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][8][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.…”

mentioning

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][8][9] An exogenous menaquinone (MK) precursor, 1,4-dihydroxy-2naphthoate (DHNA), was added to allow the microbe to synthesize MK or DMK.…”

mentioning

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][8][9] An exogenous menaquinone (MK) precursor, 1,4-dihydroxy-2naphthoate (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.…”

mentioning

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

Cited by 49 publications

References 119 publications

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

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

Plasmid-Based Gene Expression Systems for Lactic Acid Bacteria: A Review

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

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