Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite

Wood-feeding higher termites are a very successful group, important in facilitating carbon turnover in the environment. It is not the termites themselves that perform the key reactions that makes their lifestyle possible, but the lignocellulase-degrading symbiotic bacteria found in their hindgut. A metagenomic analysis of gut microbes from over 150 tree-living termites from a Costa Rican rainforest has revealed a diverse range of bacterial cellulase and xylan hydrolase genes, as well as genes important in other symbiotic functions. The data set includes about 1,000 bacterial lignocellulose hydrolase enzymes, some of them expressed in situ, in living termites. This work shows that termites are a rich reservoir of bacterial enzymes that might be used in the conversion of woody material into biofuels. Wood-feeding 'higher' termites rely on their hindgut symbionts for the intitial steps in cellulose degradation. Metagenomic analysis of this microbial community reveals a diverse range of bacterial cellulase and hydrolase genes, as well as genes important in other metabolic functions, such as H2 metabolism, CO2-reductive acetogenesis and N2 fixation. From the standpoints of both basic research and biotechnology, there is considerable interest in reaching a clearer understanding of the diversity of biological mechanisms employed during lignocellulose degradation. Globally, termites are an extremely successful group of wood-degrading organisms1 and are therefore important both for their roles in carbon turnover in the environment and as potential sources of biochemical catalysts for efforts aimed at converting wood into biofuels. Only recently have data supported any direct role for the symbiotic bacteria in the gut of the termite in cellulose and xylan hydrolysis2. Here we use a metagenomic analysis of the bacterial community resident in the hindgut paunch of a wood-feeding ‘higher’ Nasutitermes species (which do not contain cellulose-fermenting protozoa) to show the presence of a large, diverse set of bacterial genes for cellulose and xylan hydrolysis. Many of these genes were expressed in vivo or had cellulase activity in vitro, and further analyses implicate spirochete and fibrobacter species in gut lignocellulose degradation. New insights into other important symbiotic functions including H2 metabolism, CO2-reductive acetogenesis and N2 fixation are also provided by this first system-wide gene analysis of a microbial community specialized towards plant lignocellulose degradation. Our results underscore how complex even a 1-μl environment can be.