Evolutionary transitions across the tree of life : Phylogenomic case studies in environmental archaea, bacteria and eukaryotes

Sammanfattning: Microbes form the majority of life on Earth, but have been systematically underrepresented in historical research. The sequencing revolutions of the last two decades have completely changed the way we can study microbial genomic information, giving us the means to probe ever deeper into their evolution. In a first study, we developed a new approach to screen large short-read datasets for the presence of lineages and genes of interest. By using gene-centric assembly and phylogenetic placement, we integrate the strengths of reference-based with phylogenetic screening methods to efficiently reconstruct gene sequences and label them taxonomically. This will enable researchers to more efficiently select datasets which are likely to contain desired lineages and genes.In the second study, we recover five metagenome-assembled genomes from the previously uncharacterized Hikarchaeia. We infer them to be the closest relatives of haloarchaea and study the evolution of genome content since the last common ancestor of these two aerobic groups with anaerobic methanogens. We detect patterns of gradual evolutionary transition, including the early loss of methanogenesis-related genes and the acquisition of the genetic basis for aerobic respiration. Furthermore, genomes of haloarchaea underwent significant expansion, mostly through transfers from diverse groups of bacteria, whereas Hikarchaeia display genome streamlining typical of marine prokaryotes.In a third study, we reconstructed two new bacterial families, Mitibacteraceae and Athabascaceae, that branch as sister clades to all previously known Rickettsiales. Their genomes lack the characteristic reduction of rickettsial bacteria but resemble free-living alphaproteobacteria. However, they contain several conserved features, such as the rvh type 4 secretion system. We reconstructed the last common ancestor of all Rickettsiales and inferred it as a free-living organism associated with marine biofilms. Further, we propose a model for the transition towards host-association found in all classical Rickettsiales.The fourth study explores the diversity and evolution of the eukaryotic orphan lineage Picozoa. With the help of 43 new single amplified genomes, Picozoa are placed within the supergroup Archaeplastida, in a clade together with red algae and the predatory rhodelphids. In contrast to other archaeplastids, picozoan genomes show no sign of a (cryptic) plastid or plastid-associated gene transfers. This suggests that Picozoa completely lost the primary plastid early in their evolution, or that in fact they never possessed it. These findings raise further questions about the acquisition of the plastid in the archaeplastidal ancestor and the frequency of plastid loss.In summary, this thesis explores several important evolutionary transitions across the tree of life using environmental genome reconstruction, phylogenomics and ancestral state reconstruction approaches.