Origin Recognition Complex (ORC) Evolution Is Influenced by Global Gene Duplication/Loss Patterns in Eukaryotic Genomes

The conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the ancestral diversification of ORC in eukaryotes was accompanied by the neofunctionalization of some subunits, for example, role of ORC1 in centriole homeostasis. We have addressed these questions by reconstructing the distribution and evolutionary history of ORC1-5/CDC6 in a taxon-rich eukaryotic data set. First, we identified ORC subunits previously undetected in divergent lineages, which allowed us to propose a series of parsimonious scenarios for the origin of this multiprotein complex. Contrary to previous expectations, we found a global tendency in eukaryotes to increase or decrease the number of subunits as a consequence of genome duplications or streamlining, respectively. Interestingly, parasites show significantly lower number of subunits than free-living eukaryotes, especially those with the lowest genome size and gene content metrics. We also investigated the evolutionary origin of the ORC1 role in centriole homeostasis mediated by the PACT region in human cells. In particular, we tested the consequences of reducing ORC1 levels in the centriole-containing green alga Chlamydomonas reinhardtii. We found that the proportion of centrioles to flagella and nuclei was not dramatically affected. This, together with the PACT region not being significantly more conserved in centriole-bearing eukaryotes, supports the notion that this neofunctionalization of ORC1 would be a recent acquisition rather than an ancestral eukaryotic feature.

Phagocytosis-like cell engulfment by a planctomycete bacterium

Phagocytosis is a key eukaryotic feature, conserved from unicellular protists to animals, that enabled eukaryotes to feed on other organisms. It could also be a driving force behind endosymbiosis, a process by which α-proteobacteria and cyanobacteria evolved into mitochondria and plastids, respectively. Here we describe a planctomycete bacterium, ‘Candidatus Uab amorphum’, which is able to engulf other bacteria and small eukaryotic cells through a phagocytosis-like mechanism. Observations via light and electron microscopy suggest that this bacterium digests prey cells in specific compartments. With the possible exception of a gene encoding an actin-like protein, analysis of the ‘Ca. Uab amorphum’ genomic sequence does not reveal any genes homologous to eukaryotic phagocytosis genes, suggesting that cell engulfment in this microorganism is probably not homologous to eukaryotic phagocytosis. The discovery of this “phagotrophic” bacterium expands our understanding of the cellular complexity of prokaryotes, and may be relevant to the origin of eukaryotic cells.

An Important Role for Purifying Selection in Archaeal Genome Evolution

ABSTRACT The evolution of genome complexities is a fundamental question in biology. A hallmark of eukaryotic genome complexity is that larger genomes tend to have more noncoding sequences, which are believed to be minimal in archaeal and bacterial genomes. However, we found that archaeal genomes also possessed this eukaryotic feature while bacterial genomes did not. This could be predicted from our analysis of genetic drift, which showed relaxed purifying selection in larger archaeal genomes, also a eukaryotic feature. In contrast, the opposite was evident in bacterial genomes. As the null hypothesis of genome evolution, population genetic theory suggests that selection strength controls genome size. Through the process of genetic drift, this theory predicts that compact genomes are maintained by strong purifying selection while complex genomes are enabled by weak purifying selection. It offers a unifying framework that explains why prokaryotic genomes are much smaller than their eukaryotic counterparts. However, recent findings suggest that bigger prokaryotic genomes appear to experience stronger purifying selection, indicating that purifying selection may not dominate prokaryotic genome evolution. Since archaeal genomes were underrepresented in those studies, generalization of the conclusions to both archaeal and bacterial genomes may not be warranted. In this study, we revisited this matter by focusing on archaeal and bacterial genomes separately. We found that bigger bacterial genomes indeed experienced stronger purifying selection, but the opposite was observed in archaeal genomes. This new finding would predict an enrichment of noncoding sequences in large archaeal genomes, which was confirmed by an analysis of coding density. In contrast, coding density remained stable regardless of bacterial genome size. In conclusion, this study suggests that purifying selection may play a more important role in archaeal genome evolution than previously hypothesized, indicating that there could be a major difference between the evolutionary regimes of Archaea and Bacteria. IMPORTANCE The evolution of genome complexity is a fundamental question in biology. A hallmark of eukaryotic genome complexity is that larger genomes tend to have more noncoding sequences, which are believed to be minimal in archaeal and bacterial genomes. However, we found that archaeal genomes also possessed this eukaryotic feature while bacterial genomes did not. This could be predicted from our analysis on genetic drift, which showed a relaxation of purifying selection in larger archaeal genomes, also a eukaryotic feature. In contrast, the opposite was evident in bacterial genomes.