Evolution of biological systems linked to complex cell architectures in Planctomycetota

• The eukaryotic cells have a nucleus and membrane-enclosed organelles for functions such as energy production, whereas the prokaryotic cells have a cell wall but no intracellular membrane-bound structures. Species of the Planctomycetota phylum are classified as bacteria but have diverse and complex cell architectures. For example, members of the Gemmataceae have highly invaginated cytoplasmic membranes, the anammox bacteria have a membrane-bound organelle for energy production, and one species, “Candidatus Uabimicrobium amorphum”, can form digestive vacuoles during phagocytotic-like engulfment of other cells.In this thesis, we have performed comparative genomics and evolutionary analyses of bacteria in the Planctomycetota to learn more about the evolution of cellular complexity. The thesis also presents a new workflow to facilitate the assembly of datasets for comparative and evolutionary analysis of prokaryotic species.Comparative analyses of several novel genomes in the Gemmatacea family showed that new protein families have evolved by massive paralogization and fusion of prokaryotic-like domains with eukaryotic-like domains. The analyses showed no strict boundary between prokaryotic and eukaryotic genomes regarding gene lengths, gene paralogy and protein domain composition patterns.Analysis of the “Candidatus Uabimicrobium amorphum” genome revealed an extreme expansion of genes for serine/threonine protein kinases, possibly related to the predatory lifestyle of this species. However, the associated domains differed from those of serine/threonine protein kinases in eukaryotes, suggesting that the expansion and diversification process has occurred independently in eukaryotes and Planctomycetota.Evolutionary studies of the enzymes in the anammox pathway showed that the central enzyme, hydrazine synthase, previously of unknown origin, has homologs in other bacteria, including other members of the Planctomycetota. However, the homologs lacked key residues involved in the formation of hydrazine, suggesting that the anammox reaction has only originated once. Other enzymes in this pathway have been acquired by horizontal gene transfer events followed by duplication and divergence. Further, by studying the evolution of the heme biosynthesis pathway in this phylum, we show that this pathway has been replaced in the anammox bacteria with a strictly anaerobic pathway following horizontal gene transfers from archaea and other bacteria.Thus, although members of the Planctomycetota share many traits with eukaryotes, such as the same types of protein domains and similarities in cellular structures, our analyses show that these features have independent origins and reflect convergent evolution. The results have implications for our understanding of the origin of cellular complexity.

Subject headings

NATURVETENSKAP  -- Biologi -- Evolutionsbiologi (hsv//swe)

NATURAL SCIENCES  -- Biological Sciences -- Evolutionary Biology (hsv//eng)

Keyword

Planctomcyetota;Cellular complexity;Gemmataceae;Phagocytocis;Serine/Threonine kinase;Anammox;Hydrazine Synthase;Hydroxylamine oxidoreductase;Heme biosynthesis;Phylogenetics

Biologi med inriktning mot molekylär evolution

Biology with specialization in Molecular Evolution

Publication and Content Type

vet (subject category)

dok (subject category)