Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 52; pp. 26892 - 26899
• Main Authors: Light, Samuel H., Méheust, Raphaël, Ferrell, Jessica L., Cho, Jooyoung, Deng, David, Agostoni, Marco, Iavarone, Anthony T., Banfield, Jillian F., D’Orazio, Sarah E. F., Portnoy, Daniel A.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 26.12.2019
• Subjects: Bacteria; Biological Sciences; Cognitive science; Electron transfer; Electron transport; Electron transport chain; Enzymes; Flavin; Foodborne pathogens; Gram-positive bacteria; Life Sciences; Listeria; Listeria monocytogenes; Metabolism; Microorganisms; Phylogeny; Reductase; Reductases; Substrates; fumarate/urocanate; cellular respiration; bacterial pathogenesis; exoelectrogen; electromicrobiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1915678116

Mineral-respiring bacteria use a process called extracellular electron transfer to route their respiratory electron transport chain to insoluble electron acceptors on the exterior of the cell. We recently characterized a flavin-based extracellular electron transfer system that is present in the foodborne pathogen Listeria monocytogenes, as well as many other Gram-positive bacteria, and which highlights a more generalized role for extracellular electron transfer in microbial metabolism. Here we identify a family of putative extracellular reductases that possess a conserved posttranslational flavinylation modification. Phylogenetic analyses suggest that divergent flavinylated extracellular reductase subfamilies possess distinct and often unidentified substrate specificities. We show that flavinylation of a member of the fumarate reductase subfamily allows this enzyme to receive electrons from the extracellular electron transfer system and support L. monocytogenes growth. We demonstrate that this represents a generalizable mechanism by finding that a L. monocytogenes strain engineered to express a flavinylated extracellular urocanate reductase uses urocanate by a related mechanism and to a similar effect. These studies thus identify an enzyme family that exploits a modular flavin-based electron transfer strategy to reduce distinct extracellular substrates and support a multifunctional view of the role of extracellular electron transfer activities in microbial physiology.