Redox Gene Regulator Rex Diverts Fermentation In Concert with Low Charge Export in Streptococcus mutans

Abstract

Microbial current production (MCP) coupled with fermentation metabolism emerges as critical for microbial electrochemical technologies. Unlike MCP associated with anaerobic respiration, a low amount of electron flux via MCP can impact the fermentation pathway and product yield. However, understanding the machinery for such an intriguing impact of MCP on fermentation remains unclear. Here, we report that the redox regulator protein (Rex), found in many Gram-positive bacteria, was activated by a low microbial current generation and affected the fermentation balance via pyruvate dehydrogenase upregulation in Streptococcus mutans. Although the coulombic efficiency of MCP was less than 0.02%, a significant shift in fermentation balance from ethanol to lactate production occurred in association with MCP to an electrode and with the reduction of a soluble electron acceptor flavin. Modeling metabolic flux in the wild type and the Δrex strains based on transcriptomics suggested that Rex protein was responsible for the shift in fermentation pathway through pyruvate dehydrogenase modification, resulting in increased ethanol concentration in the absence of MCP. Accordingly, deletion of the rex gene resulted in the loss of MCP-alteration of fermentation metabolic switch. Given that the rex gene is widely distributed in electrogenic bacteria, gene upregulation by MCP might be a prevalent mechanism.