Unveiling lignocellulolytic potential: a genomic exploration of bacterial lineages within the termite gut.

Background: The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT.

Results: We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall.

Conclusions: The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT. Video Abstract.