Origin and Evolution of Rickettsial Plasmids

Khalid El Karkouri , Pierre Pontarotti (1) , Didier Raoult (2) , Pierre-Edouard Fournier (2)

1 I2M - Institut de Mathématiques de Marseille
2 URMITE - Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes

Background Rickettsia species are strictly intracellular bacteria that have undergone a reductive genomic evolution. Despite their allopatric lifestyle, almost half of the 26 currently validated Rickettsia species have plasmids. In order to study the origin, evolutionary history and putative roles of rickettsial plasmids, we investigated the evolutionary processes that have shaped 20 plasmids belonging to 11 species, using comparative genomics and phylogenetic analysis between rickettsial, microbial and non-microbial genomes. Results Plasmids were differentially present among Rickettsia species. The 11 species had 1 to 4 plasmid (s) with a size ranging from 12 kb to 83 kb. We reconstructed pRICO, the last common ancestor of the current rickettsial plasmids. pRICO was vertically inherited mainly from Rickettsia/Orientia chromosomes and diverged vertically into a single or multiple plasmid(s) in each species. These plasmids also underwent a reductive evolution by progressive gene loss, similar to that observed in rickettsial chromosomes, possibly leading to cryptic plasmids or complete plasmid loss. Moreover, rickettsial plasmids exhibited ORFans, recent gene duplications and evidence of horizontal gene transfer events with rickettsial and non-rickettsial genomes mainly from the alpha/gamma-proteobacteria lineages. Genes related to maintenance and plasticity of plasmids, and to adaptation and resistance to stress mostly evolved under vertical and/or horizontal processes. Those involved in nucleotide/carbohydrate transport and metabolism were under the influence of vertical evolution only, whereas genes involved in cell wall/membrane/envelope biogenesis, cycle control, amino acid/lipid/coenzyme and secondary metabolites biosynthesis, transport and metabolism underwent mainly horizontal transfer events. Conclusion Rickettsial plasmids had a complex evolution, starting with a vertical inheritance followed by a reductive evolution associated with increased complexity via horizontal gene transfer as well as gene duplication and genesis. The plasmids are plastic and mosaic structures that may play biological roles similar to or distinct from their co-residing chromosomes in an obligate intracellular lifestyle.

Mots clés: Evolutionary genetics; Genome evolution; Microbial evolution; Rickettsia; Horizontal gene transfer; Phylogenetic analysis; Phylogenetics; Ticks

Domaines: Maladies infectieuses

Khalid El Karkouri, Pierre Pontarotti, Didier Raoult, Pierre-Edouard Fournier. Origin and Evolution of Rickettsial Plasmids. PLoS ONE, 2016, 11 (2), pp.e0147492. ⟨10.1371/journal.pone.0147492⟩. ⟨hal-01459537⟩