El Karkouri Khalid, Pontarotti Pierre, Raoult Didier, Fournier Pierre-Edouard
Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS7278, IRD198, INSERMU1095, Institut Hospitalo-Universitaire Méditerranée-Infection, Aix-Marseille Université, Faculté de Médecine, 27 boulevard Jean Moulin, 13385 Marseille cedex 5, France.
Aix Marseille Université, CNRS, Centrale Marseille, I2M UMR 7373, Equipe Evolution Biologique et Modélisation, Marseille, France.
PLoS One. 2016 Feb 11;11(2):e0147492. doi: 10.1371/journal.pone.0147492. eCollection 2016.
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.
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 α/γ-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.
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.
立克次氏体属细菌是严格的细胞内寄生菌，经历了基因组的简化进化。尽管它们过着异域生活方式，但在目前已确认的26种立克次氏体中，近一半拥有质粒。为了研究立克次氏体质粒的起源、进化历史及假定作用，我们利用立克次氏体、微生物和非微生物基因组之间的比较基因组学和系统发育分析，研究了塑造属于11个物种的20种质粒的进化过程。
立克次氏体物种间质粒的存在情况各不相同。这11个物种拥有1至4个质粒，大小从12 kb到83 kb不等。我们重建了当前立克次氏体质粒的最后一个共同祖先pRICO。pRICO主要从立克次氏体/东方体染色体垂直遗传而来，并在每个物种中垂直分化为单个或多个质粒。这些质粒也通过渐进的基因丢失经历了简化进化，类似于在立克次氏体染色体中观察到的情况，这可能导致隐蔽质粒或完全质粒丢失。此外，立克次氏体质粒表现出孤儿基因、近期的基因重复以及与主要来自α/γ-变形菌谱系的立克次氏体和非立克次氏体基因组发生水平基因转移事件的证据。与质粒维持和可塑性以及适应和抗应激相关的基因大多在垂直和/或水平过程中进化。那些参与核苷酸/碳水化合物转运和代谢的基因仅受垂直进化的影响，而参与细胞壁/膜/包膜生物合成、周期控制、氨基酸/脂质/辅酶和次生代谢物生物合成、转运和代谢的基因主要经历水平转移事件。
立克次氏体质粒经历了复杂的进化，始于垂直遗传，随后是与通过水平基因转移以及基因重复和产生而增加的复杂性相关的简化进化。这些质粒是可塑性和镶嵌性结构，在专性细胞内生活方式中可能发挥与其共存染色体相似或不同的生物学作用。
