Wood fibers in the hindgut of a wood-feeding beetle supports a specific bacterial community that facilitates cellulose digestion

Saproxylophagous insects, which ingest dead wood, rely on complex gut microbiomes for lignocellulose digestion. The symbiotic digestion of lignocellulose has been best studied in termites, but a similar but poorly understood mechanism has evolved in members of Passalidae (Coleoptera). Recent surveys of the horned passalus Odontotaenius disjunctus have shown its gut microbiome to be complex and spatially stratified to reflect the compartmentation and steep physicochemical gradients in its gut, indicating the presence of microhabitat-specific communities in the passalid gut. Plant material in the intestinal tracts of herbivorous mammals and termites has been shown to be colonized by specific microbial members of the gut microbiome, but nothing is known about the existence of a fiber-associated community in passalids or its role in lignocellulose digestion. In this study, we assayed different gut sections of O. disjunctus for cellulase and xylanase activity, and sequenced relevant fiber-associated microbiomes using 16S rRNA amplicon sequencing. We identified a structurally unique, cellulolytic, fiber-associated microbiome in the anterior hindgut of O. disjunctus. The midgut of O. disjunctus has the highest overall enzymatic activity, most of which is likely endogenous. Using qPCR, we observed the anterior hindgut to have a higher bacterial density than the midgut, confirming its importance as a major site of microbial lignocellulose digestion by a fiber-digesting bacterial community of specific composition. The colonization of wood particles in the anterior hindgut of O. disjunctus by a specific bacterial community suggests that passalid beetles have evolved a mechanism of symbiotic digestion analogous to that in wood-feeding termites.