Mobile genetic elements

Mobile genetic elements (MGE, viruses and plasmids) play a key role in microbial diversity and in the major biogeochemical cycles. Viruses would even be the main component of biosphere and cellular organisms would literally be immersed in a viral ocean. Most of our knowledge in that field result of decades of intensive work on Bacteria and eukaryotes. However, little is known on viruses and plasmids from the third domain, Archaea. The first investigations in that emerging field are rather recent and highlighted an unexpected diversity, especially in Creanarchaea, as shown by the group of David Prangishvili and before by Wolfram Zillig.
Recently, three major conclusions emerged from comparative genomics:

 

-The first one is the discovery of unexpected homologies between viruses infecting cellular hosts belonging to the 3 domains, Archaea, Bacteria and Eukarya, suggesting that the virosphere is extremely ancient. The existence of different viral analogous protein systems involved in DNA metabolism (3R mechanisms: replication, repair and recombination), that would have initially been recruited in the RNA world, then independently transferred laterally to cellular lineages , strengthens the hypothesis according which DNA invention and its replication mechanisms would have their origin in the ancestral virosphere (see Patrick Forterre papers). In parallel, the hypothesis that the cell nucleus origin would be an archaean virus close to the Poxvirus infecting Eukaryotes suggests ancestrality or at least pre-eminence of the viral world.
Ancestrality of plasmids is also evidenced as well as their tight links with the viral world. As a matter of fact, the presence of homologous genes between plasmids and viruses but unknown in genomes of cellular organisms, suggests that plasmids would derived from capsid defective viruses.

- The second point is the importance, in prokaryotes, of horizontal gene transfer. Microbial genomes would evolve notably through gene fluxes (gain, loss and re-arrangement) for which plasmids and viruses are simultaneously the reservoir and the natural vectors. Facilitating lateral gene transfers and exchanges, these mobile genetic elements (MGE) actively contribute to microbial communities adaptation to changing environments, and on long term basis to diversification and evolution.

- The third conclusion is that the number of orphan genes in prokaryotic genomes stands at a high level and does not decrease despite the sequencing of more than 400 genomes. Those genes, with unknown functions, could well be ancient plasmidic or viral genes that invaded cellular genomes. In fact, archaean MGE genomes display a higher percentage of orphan genes than the average found in cellular genomes. Genome sequencing of uncultured viral communities directly sampled from marine environments have shown that more than two third of sequences are completely new (more information is available at Forest Rohwer website). In addition, plasmidic and viral genomes of thermacidophilic archaean communities from continental hot springs display an unprecedented 85% content of orphan genes.

Taken together, these observations suggest that viral and plasmidic genomes, that could have evolved since the origin of life, represent a huge reservoir of novel genes and proteins with unknown functions and properties. Some of them could be functional analogs of already known enzymes, but a lot more could encode for novel biological functions. Due to their universal ability to propagate through cellular communities and to transfer novel functions to infected cells, viruses and plasmids could modify the fitness of their hosts and consequently impact the structure and functioning of corresponding ecosystems.

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Our laboratory has initiated a research programme dedicated to plasmidic and viral diversity of hydrothermal vents. The first step consists in the isolation and characterization of novel mobile genetic elements. The second step aims at deciphering MGE genomes, comparing them, thanks to comparative and structural genomic tools. Our favourite biological material is the group of MGE hosted by the Euryarchaean hyperthermophilic order of Thermococcales that contains 5 species with sequenced genomes available. This work should provide new information on biodiversity, origin and evolution of MGE and on their contribution to genome diversification and evolution.

This work is done in close cooperation with national and international laboratories involved in that field and funded by regional grants (PhD funded by the Brittany regional council), national grants (ACI CNRS HotVir 2004-2007; ANR GenoArchaea 2006-2008; ANR Modulome 2006-2008) and European (NoE Marine genomics Europe, 2005-2008).

The main results of the laboratory during the 2004-2007 period are:

  • the isolation of PAV1, the first Virus-Like particle isolated from a hyperthermophilic Euryarchaea, Pyrococcus abyssi, its genome analysis and the evidence of a high content in completely unknown genes ;
  • the demonstration that plasmids are very common mobile genetic elements in Thermoccocales, with more than 2/3 of the isolates positive
  • the evidence that viruses, plasmids and integrated viral elements share a common organization and pool of genes.

PAV1 genome