Genome evolution at the genus level: Comparison of three complete genomes of hyperthermophilic Archaea

We have compared three complete genomes of closely related hyperthermophili c species of Archaea belonging to the Pyrococcus genus: Pyrococcus abyssi, Pyrococcus horikoshii, and Pyrococcus furiosus. At the genomic level, the c omparison reveals a differential conservation among Four regions of the Pyr ococcus chromosomes correlated with the location of generic elements mediat ing DNA reorganization. This discloses the relative contribution of the maj or mechanisms that promote genomic plasticity in these Archaea, namely rear rangements linked to the replication terminus, insertion sequence-mediated recombinations, and DNA integration within tRNA genes. The combination of t hese mechanisms leads to a high level of genomic plasticity in these hypert hermophilic Archaea, at least comparable to the plasticity observed between closely related bacteria. At the proteomic level, the comparison of the th ree Pyrococcus species sheds light on specific selection pressures acting b oth on their coding capacities and evolutionary rates. Indeed, thanks to tw o independent methods, the "reciprocal best hits" approach and a new distan ce ratio analysis, we detect the false orthology relationships within the P yrococcus lineage. This reveals a high amount of differential gains and los ses of genes since the divergence of the three closely related species. The resulting polymorphism is probably linked to an adaptation of these free-l iving organisms to differential environmental constraints. As a corollary, we delineate the set of orthologous genes shared by the three species, that is, the genes that may characterize the Pyrococcus genus. In this conserve d core, the amino acid substitution rate is equal between P. abyssi and P. horikoshii for most of their shared proteins, even for fast-evolving ones. In contrast, strong discrepancies exist among the substitution rates observ ed in P. furiosus relative to the two other species, which is in disagreeme nt with the molecular clock hypothesis.