Deep sea anaerobic microbial community couples the degradation of insoluble chitin to extracellular electron transfer

Chitin is a major structural component of arthropod exoskeletons, and an important carbon and nitrogen source in marine environments. In anoxic sediments, its degradation generates chitooligosaccharides and N-acetylglucosamine (GlcNAc), which are fermented into smaller organic molecules and oxidized anaerobically using soluble electron acceptors or insoluble ones such as metal oxides. To date, many aspects of chitin degradation in deep-sea anoxic sediments have been overlooked, including the potential coupling of insoluble chitin degradation to metal oxide reduction, the involvement of extracellular electron transfer (EET), and the spatial organization of the microorganisms involved. Using anoxic deep-sea sediments recovered from a whale fall site, we developed an innovative workflow based on electrochemical reactors, to characterize chitin degradation in these environments. Sediment samples enriched on poorly crystalline iron oxides, and subsequently transferred into an electrochemical reactor poised at +0.22 V vs SHE, showed active anodic current production when supplied with chitin, which increased 2-fold when amended with GlcNAc. Chitin reactors were dominated by Vallitalea (Firmicutes), Spirochaetota, Gammaproteobacteria and Desulfobacterota. Exoenzyme activity assays, metabolite profiling, and continued anodic current production confirmed ongoing chitin degradation linked to EET. We observed metabolic associations between chitin degraders and secondary consumers using in situ imaging (16S rRNA gene FISH coupled with BONCAT and nanoSIMS). These microbial partners, within the electrode-attached community, required close proximity to the poised electrode ([≤] 10 {micro}m) to remain metabolically active. Supporting these observations, cultured isolates of Vallitalea sp. and Trichloromonas sp. recovered from the whale fall site exhibited chitin degradation and electrochemical activity, respectively. When co-cultured in an bioelectrochemical reactor, the acetate produced by Vallitalea sp. during chitin degradation fueled Trichloromonas sp., which facilitated EET, hereby demonstrating that syntrophic interactions are used to couple anoxic chitin degradation to EET in deep-sea sediments. These findings exemplify the interspecies interactions and resource optimization occurring in hard-to-reach and largely unknown deep-sea ecosystems.