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The Candidate phylum "Termite Group". Diversity, distribution, metabolism and evolution of representatives of an unexplored bacterial phylum
This thesis summarizes a series of studies of the phylum Elusimicrobia (formerly candidate phylum "Termite Group"). The environmental distribution of members of this phylum, and the genome sequence of the first and only cultivated representative, Elusimicrobium minutum, were the focus of t...
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| Format: | Dissertation |
| Sprache: | Englisch |
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Philipps-Universität Marburg
2009
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| Zusammenfassung: | This thesis summarizes a series of studies of the phylum Elusimicrobia (formerly candidate phylum "Termite Group"). The environmental distribution of members of this phylum, and the genome sequence of the first and only cultivated representative, Elusimicrobium minutum, were the focus of these studies. In addition, a comparative genome analysis of the endosymbiotic representatives from this phylum was conducted.
Intestinal tracts of insects harbor several novel deep-rooting lineages of hitherto uncultivated bacteria, whose physiology is obscure. One of these groups is the phylum Elusimicrobia. Originally, the Elusimicrobia were represented only by the so-called endomicrobia, which had been identified as endosymbionts of flagellate protists of lower termites and wood-feeding cockroaches, but public databases contain a growing number of distantly related 16S rRNA gene sequences that fall into the radiation of the Elusimicrobia phylum. In the first study, group-specific primers were used to demonstrate that members of the Elusimicrobia are widespread in the environment and, in addition to the endomicrobia, comprise numerous other monophyletic lineages occurring in various habitats.
One of these lineages consisted of sequences obtained from various intestinal habitats. It comprised also the 16S rRNA gene of Elusimicrobium minutum, the first cultivated representative of the Elusimicrobia phylum, which was isolated from the gut of the scarab beetle larva Pachnoda ephippiata. This pure culture was the basis for the second study, which included the physiological and morphological characterization of E. minutum and the analysis of its genome. The genome allowed reconstruction of the metabolic pathways for the most important growth substrates (glucose, fructose, N-acetyl-glucosamine), revealing all genes required for uptake and fermentation of sugars via the Embden-Meyerhoff pathway and production of ethanol, acetate, H2, and CO2. Based on the genome, it could be predicted that a [NiFe] hydrogenase is responsible for the production of hydrogen, depending on the hydrogen partial pressure. This enzyme probably couples the production of hydrogen with the generation of a proton-motive force (energy-converting hydrogenase). At low hydrogen partial pressure, hydrogen production may shift to a [FeFe] hydrogenase that synergistically uses NADH and reduced ferredoxin to produce hydrogen. In addition the genome also encodes for an unusual peptide degradation pathway that comprises transamination reactions and leads to the formation of alanine from pyruvate, an explanation for why E. minutum excretes alanine in substantial amounts. The function of the exceptionally high number of pilE genes in the genome is still elusive, and since electron micrographs showed no cell appendages, their participation in pilus assembly is uncertain. The presence of a rubredoxin:oxygen oxidoreductase operon in the genome of E. minutum indicated that the strictly anaerobic bacterium may also be able to reduce small amounts of molecular oxygen, which is also in accordance with physiological observations.
The phylogenetic analysis of 22 concatenated single-copy marker genes from the genome reinforced the phylum-level status of Elusimicrobia and confirmed the reproducible relationship between E. minutum and endomicrobia (represented by Candidatus "Endomicrobium trichonymphae" strain Rs-D17) as already predicted at the 16S rRNA level. This analysis was possible because of the recent publication of the genome of strain Rs-D17 from Trichonympha agilis. In parallel, a metagenome library from an enriched CET population derived from diverse flagellates of Zootermopsis nevadensis was prepared. The last part of this thesis consists of a comparative analysis of the large genome fragments from the metagenome library with the genome of strain Rs-D17. It revealed parallel evolution of endomicrobia strains in different termites and indicated the presence of genome rearrangements. The genome rearrangements suggest the ability for homologous recombination, which could be facilitated by the horizontal transfer of endosymbionts between Trichonympha species during occasional sexual reproduction.
Together, these studies contribute fundamental insights into the diversity, distribution, metabolism, and evolution of representatives from the phylum Elusimicrobia. The genome revealed along with the metabolic capacities of E. minutum numerous genes with only hypothetical functions, e.g., polyketide synthesis, indicating the presence of hitherto undiscovered physiological traits which could be the subject for further investigations. The detailed annotation of E. minutum will also serve as reference for future annotations of other closely related members of this phylum.
Together, these studies contribute fundamental insights into the diversity, distribution, metabolism and evolution of representatives from the phylum Elusimicrobia. The genome revealed along with the metabolic capacities of
E. minutum numerous genes with only hypothetical functions, e.g., polyketide synthesis indicating the presence of hitherto undiscovered physiological traits which could be the subject for further investigation. The detailed annotation of E. minutum will also serve as reference for future annotations of other closely related members of this phylum. |
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| Umfang: | 188 Seiten |
| DOI: | 10.17192/z2009.0705 |