Comparison of microbial diversity and carbohydrate-active enzymes in the hindgut of two wood-feeding termites, Globitermes sulphureus (Blattaria: Termitidae) and Coptotermes formosanus (Blattaria: Rhinotermitidae).

Abstract

Wood-feeding termites have been employed as sources of novel and highly efficient lignocellulolytic enzymes due to their ability to degrade lignocellulose efficiently. As a higher wood-feeding termite, Globitermes sulphureus (Blattaria: Termitidae) plays a crucial role as a decomposer in regions such as Vietnam, Singapore, Myanmar, and Yunnan, China. However, the diversity of its gut microbiome and carbohydrate-active enzymes (CAZymes) remains unexplored. Here, we analyzed the diversity of hindgut microbial communities and CAZymes in a higher wood-feeding termite, G. sulphureus, and a lower wood-feeding termite, Coptotermes formosanus (Blattaria: Rhinotermitidae). 16S rRNA sequencing revealed that Spirochaetota, Firmicutes, and Fibrobacterota were the dominant microbiota in the hindgut of the two termite species. At the phylum level, the relative abundances of Proteobacteria and Bacteroidota were significantly greater in the hindgut of C. formosanus than in G. sulphureus. At the genus level, the relative abundances of Candidatus_Azobacteroides and Escherichia-Shigella were significantly lower in the hindgut of G. sulphureus than in C. formosanus. Metagenomic analysis revealed that glycoside hydrolases (GHs) with cellulases and hemicellulases functions were not significantly different between G. sulphureus and C. formosanus. Interestingly, the cellulases in G. sulphureus were mainly GH5_2, GH5_4, GH6, GH9, and GH45, while the hemicellulases were mainly GH11, GH8, GH10, GH11, GH26, and GH53. In C. formosanus, the cellulases were mainly GH6 and GH9, and the hemicellulases were mainly GH5_7, GH5_21, GH10, GH12, and GH53. In addition, β-glucosidase, exo-β-1,4-glucanase, and endo-β-1,4-glucanase activities did not differ significantly between the two termite species, while xylanase activity was higher in G. sulphureus than in C. formosanus. The bacteria encoding GHs in G. sulphureus were mainly Firmicutes, Fibrobacterota, and Proteobacteria, whereas Bacteroidota and Spirochaetota were the main bacteria encoding GHs in C. formosanus. Our findings characterized the microbial composition and differences in the hindgut microbiota of G. sulphureus and C. formosanus. Compared to C. formosanus, G. sulphureus is enriched in genes encoding for hemicellulase and debranching enzymes. It also highlights the rich diversity of GHs in the hindgut microbiota of G. sulphureus, including the GH5 subfamily, GH6, and GH48, with the GH6 and GH48 not previously reported in other higher termites. These results strengthen the understanding of the diversity of termite gut microbiota and CAZymes.