A flavin-based extracellular electron transfer strategy in a novel gram-positive microbe Microbacterium deferre sp. nov. strain A1-JK, isolated from cable bacteria enrichments

Abstract

Microbacteriaceae are a class of metabolically versatile gram-positive bacteria found in diverse environments. In sediments populated with filamentous cable bacteria, electric interspecies interactions between microbes and cable bacteria have been suggested. A novel, gram-positive bacterium, Microbacterium deferre strain A1-JK was isolated from the vicinity of a cable bacterium filament, capable of extracellular electron transfer (EET) to Fe(III) oxides and electrodes. Electrochemical experiments with pure cultures of M.deferre A1-JK in three-electrode cells revealed the presence of soluble mediators diffusing through the cell wall, identified through HPLC analysis as flavins. Genomic analyses further uncovered the complete riboflavin synthesis pathway, with heightened flavin production observed under oxygen-limited conditions to facilitate EET. M. deferre A1-JK encodes the periplasmic cytochrome FccA, responsible for transferring electrons on flavin carriers. M. deferre A1-JK exhibited a fast switch from aerobic metabolism to EET-based metabolism, aside from demonstrating weak electroactivity in alkaline (pH 8-10) and saline (4% NaCl) conditions. These results underscore its adaptability to use EET as an efficient survival strategy to deal with rapidly fluctuating sediment environments. These results hold promise for elucidating metabolic dynamics at oxic-anoxic interfaces along with further understanding of biogeochemical cycling in sediments.