Archaeal genome fluidity in the deep biosphere

Archaea have long been thought to reside solely in extreme environments like hot springs, volcanos, or salt lakes and this is reflected in the majority of their available isolates. However, culture-independent methods such as metagenomics have shown Archaea to be ubiquitous in the environment, though they typically are the minority compared to Bacteria with the exception of extreme environments. The terrestrial subsurface is one of the most important environments these techniques have made accessible, as it is poorly explored and yet hosts approximately 25 % of organisms on Earth. In this environment, characterized by both extremely low energy yields and limited dispersal, the extent of horizontal gene transfer influencing evolutionary adaptation as well as the growth parameters facilitating evolution are virtually unknown.

             In this thesis, we aimed to recover high quality archaeal genomes of uncultivated. Altiarchaeaota to investigate how they adapt to their deep terrestrial subsurface habitats. These Archaea dominate their moderate temperature environments, and thus identifying their adaptations, allowing them to gain an edge, is of particular interest. To accomplish this, we developed a workflow to recover archaeal genomes from metagenomes. One step frequently neglected in the recovery of genomes from metagenomes is the genome curation, due to it both being a manual task and there being a limited amount of available software. Hence, we developed the genome curation software uBin to fill this gap and enable easy, GUI-based curation of genomes. Bin curation using uBin improved the quality of 78.9 % of genomes of the CAMI dataset. Finally, we metagenomically characterized the CO2-geyser with the highest water fountain in the world, the Geyser Andernach, which was dominated by Ca. Altiarchaeum GA. We binned and curated hundreds of MAGs from this and other deep terrestrial subsurface sites. To estimate the growth potential of microbes in the deep terrestrial subsurface, we compared the Geyser Andernach ecosystem to these 16 other sites. Their sampling depth ranged from near-surface caves to samples up to 3 km in depth. We identified a trend of organisms being able to replicate faster the deeper their habitant but having less replication forks at the time of sampling, a possible adaptation to oscillating nutrient availabilities. Additionally, we compared newly binned with available Ca. Altiarchaea genomes and identified an extreme conservation of genetic content between Ca. Altiarchaea of the clade Alti-1. These genomes clustered biogeographically by continent, indicating plate tectonics as a possible route for dispersal. Their genetic repertoire showed a strong conservation of the core metabolism but differed in their peripheral genes, such as peptidases, with some showing signs of being horizontally transferred from the bacterial domain. I further substantiated these findings by using the complete Ca. Altiarchaeum GA genome recovered from the environment as a reference to identify sequence sections of genetic variability between populations of Ca. Altiarchaea. This analysis was congruent with prior biogeographic results and indicated that there is a lot more genome diversity in Ca. Altiarchaea than previously estimated. Some of these regions of genetic variability are likely caused by horizontal gene transfer, as evidenced by the presence of transposase genes. Thus, we conclude, that horizontal gene transfer may act to mitigate the otherwise very slow evolution within this phylum.

            In summary, this thesis provides a valuable workflow for the recovery of archaeal genomes from metagenomes, along with the new, easy to use genome curation tool uBin to ensure their quality, and gives valuable insights into the genetic diversity of one of the few dominant archaea in moderate temperature deep biosphere environments.


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