Hydrogen metabolism in the hindgut of lower termites.

This thesis summarizes a series of studies concerning the quantitative analysis of lignocellulose degradation in the hindgut of lower termites. Emphasis was put on the intermediates of symbiotic digestion, especially hydrogen, and the processes as well as microorganisms involved in their turnover. The termites Reticulitermes santonensis, Zootermopsis nevadensis, and Cryptotermes secundus, which represent the three lower termite families with the highest species numbers, were used as model organisms. The three species showed pronounced differences in the degree of hydrogen accumulation in their hindguts, ranging from almost no accumulation in C. secundus to nearly saturation in Z. nevadensis. Despite these differences in accumulation, hydrogen was the most important intermediate of the metabolic network in the three termites. About 22–26% of the total electron flow proceeded through the hydrogen pool. Reductive acetogenesis was identified as the dominating hydrogen-utilizing process, whereas hydrogenotrophic methanogenesis, aerobic hydrogen oxidation, and loss of hydrogen by emission from the termite played only a minor or no role. Moreover, an underestimation of gross methanogenesis by methane oxidation was explicitly ruled out by the finding that neither aerobic methane oxidizing bacteria nor archaea involved in anaerobic methane oxidation were active or even present in the hindgut. Further experiments identified lactate as second important intermediate in the studied termites. Formate played a role as additional intermediate in C. secundus only, where it was used in formate-dependent reductive acetogenesis. Based on these carbon and electron flux measurements, quantitative models of the degradation processes in the different termites were proposed. Using the functional marker gene fhs, which encodes the formyl tetrahydrofolate synthetase, the identity and diversity of homoacetogens was assessed. In all studied termites, fhs genes were dominating that fell into the “Termite Treponeme cluster”. Subsequent expression analyses revealed that only fhs genes of the “Termite Treponeme cluster” were transcribed. The cumulative evidence of this study together with the previous isolation of a homoacetogenic spirochete from the termite hindgut strongly indicate that spirochetes of the genus Treponema are responsible for reductive acetogenesis in the hindgut of lower termites. In summary, the structure and function of the homoacetogenic populations in the termite hindgut were successfully elucidated. Spirochetes were shown to be responsible for the efficient recycling of hydrogen by reductive acetogenesis thereby making the termite hindgut to one of the most efficient bioreactors in nature.