Centre National de la Recherche Scientifique UMR 6556 Ecologie, Evolution, Symbiose, Université de Poitiers, Poitiers, France.
Mol Biol Evol. 2011 Jan;28(1):685-97. doi: 10.1093/molbev/msq238. Epub 2010 Sep 6.
The streamlined genomes of ancient obligate endosymbionts generally lack transposable elements, as a consequence of their intracellular confinement. Yet, the genomes of Wolbachia, one of the most abundant bacterial endosymbionts on Earth, are littered with transposable elements, in particular insertion sequences (ISs). This paradox raises the question of whether or not such a mobile DNA proliferation reflects a special feature of ISs. In this study, we focused on another class of transposable elements, group II introns, and conducted an in-depth analysis of their content and the microevolutionary processes responsible for their dynamics within Wolbachia genomes. We report an exceptionally high intron abundance and striking differences in copy numbers between Wolbachia strains as well as between intron families. Our bioinformatics and experimental results provide strong evidence that intron diversity is mainly caused by recent (and perhaps ongoing) mobility and horizontal transfers. Our data also support several temporally independent intron invasions during Wolbachia evolution. Furthermore, group II intron spread in some Wolbachia strains may be regulated through gene conversion-mediated inactivation of intron copies. Finally, we found introns to be involved in numerous genomic rearrangements. This underscores the high recombinogenic potential of group II introns, contrary to general expectations. Overall, our study represents the first comprehensive analysis of group II intron evolutionary dynamics in obligate intracellular bacteria. Our results show that bacterial endosymbionts with reduced genomes can sustain high loads of mobile group II introns, as hypothesized for the endosymbiont ancestor of mitochondria during early eukaryote evolution.
古生的专性内共生体的基因组通常缺乏转座元件，这是由于它们的细胞内限制。然而，沃尔巴克氏体（Wolbachia）的基因组却充斥着转座元件，特别是插入序列（ISs）。这一悖论引发了这样一个问题：这种移动 DNA 的增殖是否反映了 ISs 的一个特殊特征。在这项研究中，我们专注于另一类转座元件，即第二类内含子，并对它们在沃尔巴克氏体基因组中的内容和负责其动态的微进化过程进行了深入分析。我们报告了内含子含量极高和沃尔巴克氏体菌株之间以及内含子家族之间惊人的拷贝数差异。我们的生物信息学和实验结果提供了强有力的证据，表明内含子多样性主要是由近期（可能正在进行）的移动性和水平转移引起的。我们的数据还支持沃尔巴克氏体进化过程中发生的几个时间独立的内含子入侵。此外，一些沃尔巴克氏体菌株中第二类内含子的传播可能受到基因转换介导的内含子拷贝失活的调节。最后，我们发现内含子参与了许多基因组重排。这突显了第二类内含子的高重组潜力，与普遍预期相反。总的来说，我们的研究代表了对专性细胞内细菌中第二类内含子进化动态的首次全面分析。我们的结果表明，基因组较小的细菌内共生体可以维持大量的移动第二类内含子，这与早期真核生物进化过程中线粒体内共生体祖先的假说一致。
