Bacterial symbionts of termite gut flagellates

In the gut metabolism of lower termites, molecular hydrogen plays a central role. Hydrogen is a major product of lignocellulose digestion by a dense community of anaerobic flagellates, which are found exclusively in termites and occupy the bulk of the hindgut volume. During the past years, we have been studying the prokaryotic symbionts that colonize both surface and cytoplasm of these unique protists (Brune and Ohkuma, 2011; Ohkuma and Brune, 2011).

For a number of years, we have been concentrating on the Endomicrobia—a unique lineage of bacterial endosymbionts in a novel bacterial phylum (Stingl et al., 2005; Ikeda et al., 2007), whose first representative has been cultivated and genome-sequenced in our lab (Geissinger et al., 2009; Herlemann et al., 2009). We have shown that Endomicrobia were acquired by flagellates of the genus Trichonympha long after the establishment of the flagellate–termite symbiosis and that Endomicrobia since then have cospeciated with their flagellate host (Ikeda-Ohtsubo and Brune, 2009). A study of artificially defaunated termites identified basal lineages of Endomicrobia that represent putatively free-living ancestors of the intracellular symbionts (Ikeda-Ohtsubo et al., 2010).

In a collaborative project with the group of Renate Radek at the Free University of Berlin, we have studied the molecular phylogeny and ultrastructure of different lineages of uncultivated Bacteroidales that colonize the cell surface of certain flagellates in dry-wood termites. We have shown that the ectosymbionts of the flagellate genus Devescovina are strictly cospeciating with their host (Desai et al., 2010). This cospeciation indicates an intimate metabolic relationship between the bacteria and the flagellates and an important role of the bacteria in the symbiosis. Further investigation revealed that these symbionts possess—in addition to a nifH homolog probably present in all Cluster-V Bacteroidales—-also a second homolog (anfH) that is preferentially expressed in all termite species that harbor flagellates with such symbionts (Desai and Brune, 2012). In another dry-wood termite, in which the conventional nifH homolog was expressed, flagellates of the genus Joenia are associated with different lineages of Bacteroidales (Strassert et al., 2010).

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