Deep-sea anaerobic microbial communities couple degradation of insoluble chitin to extracellular electron transfer.

Chitin, a major structural component of arthropod exoskeletons, is an abundant carbon and nitrogen source in marine ecosystems. While its degradation is well studied in oxic waters, the microbial processes and interactions that mediate its anaerobic breakdown in deep-sea sediments remain poorly understood. Iron oxides are predicted to be energetically favorable electron acceptors for anaerobic chitin degradation, yet the spatial separation of insoluble substrates and the required microbial partnerships in sediments are not well defined. Here, we used potentiostatically controlled bioelectrochemical reactors poised at +0.22 V vs. Standard Hydrogen Electrode, mimicking iron-reducing conditions, to enrich and characterize a chitin-degrading, metal-reducing microbial community from an anoxic deep-sea whale-fall sediment. Amendment with crystalline chitin generated stable anodic currents, which increased upon addition of chitin-associated metabolites (N-acetylglucosamine, glucose, acetate). 16S rRNA gene sequencing revealed a deep-sea affiliated assemblage dominated by Firmicutes (Vallitalea), Spirochaetota, Gammaproteobacteria, and Desulfobacterota (Trichloromonas). Exoenzyme assays, metabolite profiling, and current measurements confirmed that active chitin degradation provided substrate(s) for extracellular electron transfer (EET). Single-cell analyses using FISH-BONCAT and nanoSIMS showed that Vallitalea (primary degrader) and electrode-respiring Desulfobacterota exhibited highest activity within the electrode biofilm, particularly within ca.10 μm of the surface. We isolated a chitin-degrading Vallitalea sp. and an iron-reducing, electrogenic Trichloromonas sp., and demonstrated that, when reconstituted in co-culture, they cooperatively degrade chitin via acetate cross-feeding coupled to EET. This integrated electrochemical and ecophysiological study reveals microbial interactions linking chitin degradation with iron-oxide respiration in deep-sea sediments and provides a defined electrogenic model community for future syntrophy research.