Phylogeny and metabolism of novel spirochetes from cockroaches and evolutionary origin of reductive acetogenesis in termite gut treponemes
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Philipps-Universität Marburg
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Abstract
Spirochetes (phylum Spirochaetota or Spirochaetes) are widely distributed in various environments but most densely colonize the gut of termites, where they can make up even more than half of the prokaryotic population. Most termite gut spirochetes belong to the so-called “termite (Treponema) cluster I”, a highly diverse but monophyletic clade that occurs exclusively in termite guts. The functional roles of this cluster are largely unelucidated because most members are still uncultured. During my doctoral thesis, I investigated evolutionary history and metabolic potential of symbiotic spirochetes in the gut of termites and their closest relatives, cockroaches, combining cultivation with comparative genomic and phylogenomic approaches. The results have been partially published and are reported in this cumulative thesis.
While termite gut spirochetes have received considerable attention during the past decades, almost nothing is known about the cockroach gut spirochetes. Here, I isolated Breznakiella homolactica, the first representative of the termite cluster I from cockroaches. Its basal position in the entire cluster indicates that representatives of this clade were present already in the omnivorous cockroach ancestor of termites and have coevolved with their termite host. Breznakiella homolactica is a homolactic bacterium that produces acetate only in the presence of oxygen. Moreover, it is not capable of reductive acetogenesis – the most intriguing property among termite gut spirochetes – because it lacks genes encoding key enzymes of the Wood–Ljungdahl pathway, i.e., hydrogen dependent CO2 reductase (HDCR) and CO dehydrogenase and acetyl-CoA synthase (CODH/ACS). This provides strong evidence that the ancestral form of termite cluster I was not a CO2-reducing acetogen.
Using 292 metagenome-assembled genomes (MAGs) reconstructed from 22 lower and 21 higher termite species, I was able to assess the distribution of CO2-reducing acetogens also among the numerous, so far uncultured lineages of termite cluster I. A complete Wood–Ljungdahl pathway (WLP), the prerequisite for reductive acetogenesis, is encoded only by certain lineages from lower termites, whereas all MAGs from higher termites (fam. Termitidae) lack key genes of the pathway. This suggests that members of termite cluster I contribute to the gut reductive acetogenesis only in lower termites but not in higher termites. Phylogenies of HDCR and CODH/ACS indicate that the capacity for reductive acetogenesis in this cluster was acquired multiple times by a lateral transfer of genes originating from Firmicutes. My analyses of the distribution of the WLP in all other bacterial MAGs from termite guts suggests that the high activities for reductive acetogenesis in higher termites are caused by members of a lineage of uncultured deltaproteobacteria, Candidatus Adiutricaceae. In addition, the apical, non-homoacetogenic lineages of termite cluster I from higher termites possess numerous genes encoding putatively secreted carbohydrate-activated enzymes (CAZymes) for xylan degradation, which indicates that they have occupied the new niche in gut of higher termites that opened after the loss of the (hemi)cellulolytic protists.
So far, members of termite cluster I have been classified into the genus Treponema (fam. Treponemataceae). Based on a detailed phylogenomic analysis, we documented that current members of the family represent two separate family-level clades and reclassified the clade that includes members of termite cluster I into a new family, Breznakiellaceae. However, also Treponemataceae comprise uncultured representatives from insect guts. I isolated Brucepasteria parasyntrophica, the closest relative of Treponema zuelzerae, from the gut of a cockroach. It is a mixed-acid fermenter but unlike its relative, inhibited by high H2 partial pressures. However, its growth improved considerably when H2 was removed from the headspace or in the presence of a hydrogen-consuming partner. These findings provide new insights into the diversity of Treponemataceae and the metabolic adaptation of spirochetes to the intestinal environment, where hydrogen production and consumption are strongly coupled.
The results of my research shed new light on the evolutionary history of symbiotic spirochetes in the guts of termites and cockroaches and their metabolic adaptations to an environment characterized by the rapid turnover of molecular hydrogen. The coevolution of termite cluster I and their apparently originated already in the omnivorous cockroach ancestor of termites, whereas the capacity for H2-dependent CO2-reductive acetogenesis evolved later during the radiation of the host.
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Created: 2022Issued: 2025-06-23Updated: 2025-06-23
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Fachbereich Biologie
Publisher
Philipps-Universität Marburg
Language
eng
Data types
DoctoralThesis
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570
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Song, Yulin: Phylogeny and metabolism of novel spirochetes from cockroaches and evolutionary origin of reductive acetogenesis in termite gut treponemes. : Philipps-Universität Marburg 2025-06-23. DOI: https://doi.org/10.17192/z2022.0104.
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This item has been published with the following license: In Copyright