Reductive genome evolution from the mother of Rickettsia.

Reductive genome evolution from the mother of Rickettsia.
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DOI:
10.1371/journal.pgen.0030014
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发表时间:
2007-01-19
期刊:
影响因子:
4.5
通讯作者:
Raoult, Didier
Raoult, Didier
中科院分区:
生物学2区
文献类型:
--
作者:
Blanc, Guillaume;Ogata, Hiroyuki;Robert, Catherine;Audic, Stephane;Suhre, Karsten;Vestris, Guy;Claverie, Jean-Michel;Raoult, Didier

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立克次体属是一组专性的胞内α蛋白细菌,代表了一种还原进化的范例。在这里,我们研究形成该属基因组的进化过程。祖先基因组的重建表明,他们最后一个共同的祖先包含了更多的基因,但已经拥有了与细胞寄生相关的大部分特征。现代立克次体之间基因谱系的差异主要是由于祖先的差异基因丢失造成的。我们使用计算机模拟证明,在这个过程中,丢失的倾向在不同的基因之间是可变的。我们还分析了非同义与同义变化的比率(Ka/Ks),计算为大基因集上的平均值,以测试作用于立克次体、无浆体科和自由生活的γ变形杆菌基因组的选择强度。总体趋势是,Ka/Ks随基因组间差异的增大而减小。近缘基因组的高Ka/Ks可能是由于自然选择去除轻微有害的非同义突变的滞后所致。有趣的是,我们还观察到基因丢失率随着分歧的增加而降低,这表明在去除轻微有害的假基因等位基因方面也存在类似的滞后。对于较大的差异(Ks>0.2),Ka/Ks趋于相似的值,这表明细胞内的α蛋白细菌和它们的自由生活近亲的选择水平大致相同。这与专性细胞内微生物往往由于选择有效性降低而进化更快的观点形成对比,并表明背景突变率的提高在专性细胞内α蛋白细菌中的快速蛋白质分歧中发挥了重要作用。基因组的缩小和快速的序列分化经常出现在只生活在高等真核生物细胞内的细菌中。然而,这些过程对微生物基因组多样性的驱动力和贡献仍然知之甚少。立克次体是一组人类特有的小细胞内病原体,为研究基因组缩小化过程提供了一个有趣的模型。在这篇文章中,我们利用7个立克次体基因组重建了它们祖先的基因组,并推测了在当今物种中发现的基因的起源和命运。我们认为基因丢失的过程是该属内基因组多样化的主要原因,并表明基因丢失率、序列差异和基因组重排在不同的立克次体谱系中有很大的差异。这种异质性可能反映了专化对不同节肢动物寄主的复杂影响和基因谱系的关键变化,如DNA修复基因的丢失和可移动基因的扩增。相反,我们没有找到证据表明种群规模的减少对序列进化的长期加速所起的作用。总体而言,本文提供的数据为驱动专性细胞内细菌进化的基本进化过程提供了新的线索。
The Rickettsia genus is a group of obligate intracellular α-proteobacteria representing a paradigm of reductive evolution. Here, we investigate the evolutionary processes that shaped the genomes of the genus. The reconstruction of ancestral genomes indicates that their last common ancestor contained more genes, but already possessed most traits associated with cellular parasitism. The differences in gene repertoires across modern Rickettsia are mainly the result of differential gene losses from the ancestor. We demonstrate using computer simulation that the propensity of loss was variable across genes during this process. We also analyzed the ratio of nonsynonymous to synonymous changes (Ka/Ks) calculated as an average over large sets of genes to assay the strength of selection acting on the genomes of Rickettsia, Anaplasmataceae, and free-living γ-proteobacteria. As a general trend, Ka/Ks were found to decrease with increasing divergence between genomes. The high Ka/Ks for closely related genomes are probably due to a lag in the removal of slightly deleterious nonsynonymous mutations by natural selection. Interestingly, we also observed a decrease of the rate of gene loss with increasing divergence, suggesting a similar lag in the removal of slightly deleterious pseudogene alleles. For larger divergence (Ks > 0.2), Ka/Ks converge toward similar values indicating that the levels of selection are roughly equivalent between intracellular α-proteobacteria and their free-living relatives. This contrasts with the view that obligate endocellular microorganisms tend to evolve faster as a consequence of reduced effectiveness of selection, and suggests a major role of enhanced background mutation rates on the fast protein divergence in the obligate intracellular α-proteobacteria. Genome downsizing and fast sequence divergence are frequently observed in bacteria living exclusively within the cells of higher eukaryotes. However, the driving forces and contributions of these processes to the genome diversity of the microorganisms remain poorly understood. The genus Rickettsia, a group of small obligate intracellular pathogens of humans, provides a fascinating model to study the genome downsizing process. In this article, we used seven Rickettsia genomes to reconstruct the genome of their ancestor and inferred the origin and fate of the genes found in today's species. We identify the process of gene loss as the main cause of genome diversification within the genus and show that the rate of gene loss, sequence divergence, and genome rearrangements are highly variable across the various Rickettsia lineages. This heterogeneity likely reflects the intricate effects of specialization to distinct arthropod hosts and critical alterations of the gene repertoire, such as the losses of DNA repair genes and the amplification of mobile genes. In contrast, we did not find evidence for the role of reduced population sizes on the long-term acceleration of sequence evolution. Overall, the data presented in this article shed new light on the fundamental evolutionary processes that drive the evolution of obligate intracellular bacteria.
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