Cellulose-fueled extracellular electron transfer in termite gut microbes

Abstract

ABSTRACT Termites decompose billions of tons of lignocellulosic material annually through the cellulolytic metabolism of their gut microbiota. However, the mechanisms by which cellulose degradation drives anaerobic metabolism of the gut microbiome remain poorly understood. Here, we demonstrate cellulose-driven extracellular electron transfer (EET) in both a termite gut-derived gram-positive cellulolytic bacterium, Ruminiclostridium cellobioparum subsp. termitidis CT1112, and the termite gut microbiome. CT1112 cells produced current in the presence of cellulose or cellobiose as the electron donor under potentiostatic conditions. This activity was strongly dependent on self-secreted redox mediators. EET was markedly impaired when stationary-phase CT1112 developed a thickened, multilayered cell wall, reducing accessibility to exogenously added redox mediators, such as riboflavin, and small redox-active molecules, such as diaminobenzidine. As a proof of concept, current production from cellulose was also observed in the termite gut microbiome, together with increases in the relative abundances of Bacillota, Bacteroidota, and Pseudomonadota. These results support the presence of EET-capable bacteria in the termite gut and suggest that EET contributes to redox balance within the steep redox gradients of the gut. Our study expands the environmental relevance of EET in carbon cycling and highlights termite-derived microbiomes as promising platforms for bioelectrochemical applications, including cellulolytic microbial fuel cells. IMPORTANCE Termites play major roles in carbon cycling in tropical ecosystems by decomposing lignocellulosic biomass with the help of their gut microbiota. However, the microbial physiology underlying this highly efficient cellulose conversion remains poorly understood. Here, we show that both a cellulolytic termite gut isolate and the termite gut microbiome are capable of extracellular electron transfer (EET) using cellulose and its derivatives as electron donors. These findings suggest that cellulose degradation in the termite gut is coupled to extracellular redox processes, expanding our understanding of how this globally important process proceeds in anaerobic environments. They also raise the possibility that EET contributes to redox homeostasis within the gut microenvironment and open new avenues for investigating the electrochemical physiology of termite gut microbes, including their ability to reduce dietary iron(III) minerals and their potential to participate in syntrophic interspecies electron transfer. Moreover, this work highlights termite-derived microbes as promising platforms for developing efficient cellulose-to-electricity conversion technologies. Termites play major roles in carbon cycling in tropical ecosystems by decomposing lignocellulosic biomass with the help of their gut microbiota. However, the microbial physiology underlying this highly efficient cellulose conversion remains poorly understood. Here, we show that both a cellulolytic termite gut isolate and the termite gut microbiome are capable of extracellular electron transfer (EET) using cellulose and its derivatives as electron donors. These findings suggest that cellulose degradation in the termite gut is coupled to extracellular redox processes, expanding our understanding of how this globally important process proceeds in anaerobic environments. They also raise the possibility that EET contributes to redox homeostasis within the gut microenvironment and open new avenues for investigating the electrochemical physiology of termite gut microbes, including their ability to reduce dietary iron(III) minerals and their potential to participate in syntrophic interspecies electron transfer. Moreover, this work highlights termite-derived microbes as promising platforms for developing efficient cellulose-to-electricity conversion technologies.