Evolution of Prokaryote-Animal Symbiosis from a Genomics Perspective

Abstract

Methanogenesis in the enlarged hindgut compartments of termites is a product of symbiotic digestion, fueled by hydrogen and reduced one-carbon com- pounds formed during the fermentative breakdown of plant fiber and humus. Methanogens are not always the predominant hydrogenotrophic microorganisms, especially in wood-feeding termites, but are restricted to particular microhabitats within the gut. The methanogens in lower termites belong to different lineages of Methanobacteriales that either are endosymbionts of flagellate protists or colonize the periphery of the hindgut, a habitat that is not fully anoxic. The oxygen-reducing capacities of the few isolates so far available indicate that they are well adapted to the continuous influx of oxygen across the gut wall. Higher termites, which lack gut flagellates, often have highly compartmented guts with highly dynamic physico- chemical conditions, including redox and pH. The differences between the micro- environments are most pronounced in the soil-feeding species, where each compartment houses a characteristic archaeal community, comprising Methano- bacteriales, Methanosarcinales, Methanomicrobiales, and a novel, deep-branching lineage of putative methanogens distantly related to the Thermoplasmatales. All clades form distinct phylogenetic clusters unique to the intestinal tract of insects, but with the exception of several Methanobrevibacter species, none of these archaea have been isolated in pure culture. The high methane emissions of termites, together with their enormous biomass in the tropics, make them a significant natural source of this important greenhouse gas.