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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In this study, we designed a microbial electrochemical fluidized bed reactor (ME-FBR), with an electroconductive anodic bed made of activated carbon particles for treating a brewery wastewater. Under a batch operating mode, acetate and propionate consumption rates were 13-fold and 2.4-fold higher, respectively, when the fluidized anode was polarized (0.2 V) with respect to open circuit conditions. Operating in a continuous mode, this system could effectively treat the brewery effluent at organic loading rates (OLR) over 1.7 kg m-3NRV d-1 and with removal efficiencies of 95 ± 1.4% (hydraulic retention time of 1 day and an influent of 1.7 g-COD L-1). The coulombic efficiency values highly depended upon the OLR applied, and varied from a 56 ± 15% to 10 ± 1%. Fluorescence in situ hybridization (FISH) analysis revealed a relative high abundance of Geobacter species (ca. 20%), and clearly showed a natural microbial stratification. Interestingly, the Geobacter cluster was highly enriched in the innermost layers of the biofilm (thickness of 10 μm), which were in contact with the electroconductive particles of bed, whereas the rest of bacteria were located in the outermost layers. To our knowledge, this is the first time that such a clear microbial stratification has been observed on an anode-respiring biofilm. Our results revealed the relevant role of Geobacter in switching between the electrode and other microbial communities performing metabolic reactions in the outermost environment of the biofilm.

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.

Cellular respiration is essential for multiple bacterial pathogens and a validated antibiotic target. In addition to driving oxidative phosphorylation, bacterial respiration has a variety of ancillary functions that obscure its contribution to pathogenesis. We find here that the intracellular pathogen Listeria monocytogenes encodes two respiratory pathways which are partially functionally redundant and indispensable for pathogenesis. Loss of respiration decreased NAD+ regeneration, but this could be specifically reversed by heterologous expression of a water-forming NADH oxidase (NOX). NOX expression fully rescued intracellular growth defects and increased L. monocytogenes loads >1,000-fold in a mouse infection model. Consistent with NAD+ regeneration maintaining L. monocytogenes viability and enabling immune evasion, a respiration-deficient strain exhibited elevated bacteriolysis within the host cytosol and NOX expression rescued this phenotype. These studies show that NAD+ regeneration represents a major role of L. monocytogenes respiration and highlight the nuanced relationship between bacterial metabolism, physiology, and pathogenesis.

We have explored a new concept in bacteria-electrode interaction based on the use of fluid-like electrodes and planktonic living cells. We show for the first time that living in a biofilm is not a strict requirement for Geobacter sulfurreducens to exchange electrons with an electrode. The growth of planktonic electroactive G. sulfurreducens could be supported by a fluid-like anode as soluble electron acceptors and with electron transfer rates similar to those reported for electroactive biofilms. This growth was maintained by uncoupling the charge (catabolism) and discharge (extracellular respiration) processes of the cells. Our results reveal a novel method to culture electroactive bacteria in which every single cell in the medium could be instantaneously wired to a fluid-like electrode. Direct extracellular electron transfer is occurring but with a new paradigm behind the bacteria-electrode interaction.

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We investigated the adaptation of a classical oxic–anoxic chamber configuration to a microbial electrochemical system in order to remove both nitrogen and organic matter from low COD effluents.