A Hybrid Extracellular Electron Transfer Pathway Enhances the Survival of Vibrio natriegens

• Published in: Applied and environmental microbiology 2020-09, Vol.86 (19), p.1
• Main Authors: Conley, Bridget E, Weinstock, Matthew T, Bond, Daniel R, Gralnick, Jeffrey A
• Format: Article
• Language: English
• Subjects: Adaptation; Bacteria; Bacterial Proteins - metabolism; Biotechnology; Citric acid; Electron transfer; Electron Transport; Electrons; Ferric Compounds - metabolism; Geomicrobiology; Glucosamine; Hydroquinone; Iron; Metabolism; Oxidation-Reduction; Phylogeny; Pyruvic acid; Shewanella; Survival; Vibrio - physiology; Vibrio natriegens; Vibrionaceae; Waterborne diseases
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.01253-20

is the fastest-growing microorganism discovered to date, making it a useful model for biotechnology and basic research. While it is recognized for its rapid aerobic metabolism, less is known about anaerobic adaptations in or how the organism survives when oxygen is limited. Here, we describe and characterize extracellular electron transfer (EET) in , a metabolism that requires movement of electrons across protective cellular barriers to reach the extracellular space. performs extracellular electron transfer under fermentative conditions with gluconate, glucosamine, and pyruvate. We characterized a pathway in that requires CymA, PdsA, and MtrCAB for Fe(III) citrate and Fe(III) oxide reduction, which represents a hybrid of strategies previously discovered in and Expression of these genes functionally complemented mutants. Phylogenetic analysis of the inner membrane quinol dehydrogenases CymA and NapC in gammaproteobacteria suggests that CymA from diverged from CymA and NapC. Analysis of sequenced revealed that the genetic potential to perform EET is conserved in some members of the Harveyi and Vulnificus clades but is more variable in other clades. We provide evidence that EET enhances anaerobic survival of , which may be the primary physiological function for EET in Bacteria from the genus occupy a variety of marine and brackish niches with fluctuating nutrient and energy sources. When oxygen is limited, fermentation or alternative respiration pathways must be used to conserve energy. In sedimentary environments, insoluble oxide minerals (primarily iron and manganese) are able to serve as electron acceptors for anaerobic respiration by microorganisms capable of extracellular electron transfer, a metabolism that enables the use of these insoluble substrates. Here, we identify the mechanism for extracellular electron transfer in , which uses a combination of strategies previously identified in and We show that extracellular electron transfer enhanced survival of under fermentative conditions, which may be a generalized strategy among spp. predicted to have this metabolism.