Despite the presence of many carbohydrolytic activities in insects, their cellulolytic mechanisms are poorly understood. Whereas cellulase genes are absent from the genomes of Drosophila melanogaster or Bombyx mori, other insects such as termites produce their own cellulases. Recent studies using molecular biological techniques have brought new insights into the mechanisms by which the insects and their microbial symbionts digest cellulose in the small intestine. DNA sequences of cellulase and associated genes, as well as physiological and morphological information about the digestive systems of cellulase-producing insects, may allow the efficient use of cellulosic biomass as a sustainable energy source.

Symbiotic digestion of lignocellulose in wood-feeding higher termites (family Termitidae) is a two-step process that involves endogenous host cellulases secreted in the midgut and a dense bacterial community in the hindgut compartment. The genomes of the bacterial gut microbiota encode diverse cellulolytic and hemicellulolytic enzymes, but the contributions of host and bacterial symbionts to lignocellulose degradation remain ambiguous. Our previous studies ofNasutitermesspp. documented that the wood fibers in the hindgut paunch are consistently colonized not only by uncultured members of Fibrobacteres, which have been implicated in cellulose degradation, but also by unique lineages of Spirochaetes. Here, we demonstrate that the degradation of xylan, the major component of hemicellulose, is restricted to the hindgut compartment, where it is preferentially hydrolyzed over cellulose. Metatranscriptomic analysis documented that the majority of glycoside hydrolase (GH) transcripts expressed by the fiber-associated bacterial community belong to family GH11, which consists exclusively of xylanases. The substrate specificity was further confirmed by heterologous expression of the gene encoding the predominant homolog. Although the most abundant transcripts of GH11 inNasutitermes takasagoensiswere phylogenetically placed among their homologs of Firmicutes, immunofluorescence microscopy, compositional binning of metagenomics contigs, and the genomic context of the homologs indicated that they are encoded by Spirochaetes and were most likely obtained by horizontal gene transfer among the intestinal microbiota. The major role of spirochetes in xylan degradation is unprecedented and assigns the fiber-associatedTreponemaclades in the hindgut of wood-feeding higher termites a prominent part in the breakdown of hemicelluloses.