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Abstract

The symbiotic gut microbiota of termites plays important roles in lignocellulose digestion and host nutrition. In contrast to the higher (evolutionarily advanced) termites, whose gut microbiota is largely prokaryotic, the capacity of lower (primitive) termites to digest wood depends on the cellulolytic gut flagellates housed in their enlarged hindgut paunch. The flagellates initiate a microbial feeding chain driven by the primary fermentations of carbohydrates to short-chain fatty acids, the major energy source of the host. Hydrogen, a central intermediate in the hindgut fermentations, is efficiently recycled by homoacetogenic spirochetes. They prevail over methanogenic archaea, which are restricted to particular microniches at the hindgut wall or within the flagellates. The spatial separation of microbial populations and metabolic activities gives rise to steep gradients of metabolites. The continuous influx of oxygen into the hindgut affects microbial metabolism in the microoxic periphery, and the anoxic status of the gut center is maintained only by the rapid reduction of oxygen by both aerobic and anaerobic microorganisms. Moreover, the gut microbiota also compensates for the low nitrogen content of wood by fixing atmospheric nitrogen, assimilating ammonia, providing essential amino acids and vitamins, and efficiently recycling nitrogenous wastes. The microorganisms responsible for these reactions are mostly unknown, but recent studies have implicated the bacterial symbionts of termite gut flagellates in these processes. These symbionts specifically colonize either the surface or the cytoplasm of the flagellates and represent novel bacterial lineages that occur exclusively in the hindgut of termites, often cospeciating with their respective hosts. Genome information indicates that the uncultivated symbionts of flagellates play a major role in the nitrogen metabolism of this tripartite symbiosis.