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Co-evolution of viruses, plasmids and cells in Archaea: pattern and process

Final Report Summary - EVOMOBIL (Co-evolution of viruses, plasmids and cells in Archaea: pattern and process)

The aim of the EVOMOBIL project was to understand how interactions between cells, viruses and plasmids have influenced the evolution of life on earth. Many of the initial experiments focused on identifying and characterizing viruses, plasmids, and other mobile elements, using bioinformatic techniques. All these identifiable viruses and plasmids are being collated into a database that will allow to identify further viruses and plasmids, and thus better understand the structure and evolution of such elements. At the moment, we have already made available on the web a first public database, called WASP, for Web assisted Symbolic Plasmid Syntheny, that includes all known plasmids in the three domains of life. Our genomes data mining led to the discovery of two new families of mobile genetic elements, Casposons and Pipolins. Casposons may represent an intermediate in the evolution of the much-publicized CRISPR elements whereas Pipolins encode the first DNA polymerase that can synthesize DNA without primer. We also identified new protein families specifically encoded by mobile elements such as new DNA polymerases and new DNA topoisomerases. As an important “by-product” of these analyses, we discovered that some viruses can encode ribosomal proteins.

Analysis of several families of mobile genetic elements reveals that they have undergone extensive intra-phylum horizontal gene transfer but little inter-phylum transfer, potentially contributing to the phylogenetic isolation of the major cellular lineages. However, we also identified some cases of inter-phylum transfer in the case of conjugative plasmids. Hence, phylogenetic analysis of conjugative plasmids in Archaea suggests that they may have originated by horizontal gene transfer from Firmicute bacteria. These results indicate that cells and mobile element generally co-evolved and that most DNA transfer take place from mobile elements to cell, but with some major exception.

To study in more details the mechanisms of co-evolution between mobile elements and cell at the level of order. We have performed a large-scale sequencing project of complete (closed) genomes. The complete sequencing of 69 new genomes of hyperthermophilivc archaea of the order Thermococcales led to the discovery of several new mobile elements. In particular, we identified the first conjugative plasmid in hyperthermophilic archaea and we show that this plasmid can perform “hot sex”, i.e. conjugation at temperatures up to 100°C. We manipulated this plasmid and derivatives as efficient genetic tools to transfer genes between distantly related archaea and to transform archaea for which there was no genetic tools available. We also shown that site-specific integrases encoded by mobile elements can catalyze the inversion of large sections of DNA, consistent with the rapid and frequent genomic rearrangements observed in Thermococcales. Surprisingly, we found that one of these integrases exhibit homologous recombination activity.

In order to compare the history of plasmid/virus co-evolution with Archaea, we have updated the archaeal phylogeny and the position of Archaea in the universal tree of life. Our result strongly supports to root the archaeal domain in the branch leading to a clade grouping Thaumarchaeota, Aigarchaeota and Bathyarchaeota. This has important implication for the interpretation of all our observations, such as the relative isolation of plasmids and viruses of Thaumarchaeota from other Archaea and the timing of transfer of bacterial conjugative plasmids to Archaea. Importantly, this work also allowed us to place a major group of cosmopolitan viruses in the tree of life. We thus demonstrate that large and giant DNA viruses diversified before the last eukaryotic common ancestor and co-evolved with proto-eukaryotes. Our result also emphasizes that the archaeal mobilomes resemble more to the bacterial mobilome than to the eukaryotic mobilome, despite the close evolutionary relationships of Archaea and Eukarya.

We have shown that hyperthermophilic archaea produce both membrane vesicles and nanotubes, both of them apparently containing DNA. Some of these vesicles can be involved in sulfur or heavy metal detoxification whereas others, especially plasmidions, could be involved in DNA transfer. Unfortunately, we failed to identify mutants affected in vesicle production and to detect inter-species DNA transfer by these vesicles. However, we have observed a novel and surprising type of interaction between Thermococcales and Thermotoga maritima. We observed that T. maritima apparently engulfs Thermococcus within its large periplasm. We wonder if this unusual interaction may be involved in the extensive inter-domain horizontal gene transfer between hyperthermophilic archaea and bacteria that was revealed by comparative genomic analyses.