Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies
Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies
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DOI：
10.1186/1471-2164-11-449
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发表时间：
2010-07-22
期刊：
影响因子：
4.4
通讯作者：
Silva, Francisco J.
中科院分区：
文献类型：
--
作者：
Belda, Eugeni;Moya, Andres;Silva, Francisco J.
背景：基因组减少是共生菌和致病菌共同的进化过程。这一过程在昆虫的细菌内共生体中得到了广泛的表征，其中初级互利共生细菌代表了基因组减少的最极端情况，这是它们从自由生活的祖先进化过程中基因失活和丢失的大规模过程的结果。舌蝇Sodalis glossinidius是舌蝇的次级内共生体，在共生关系的最初阶段包含了为数不多的完整的细菌基因组之一，因此可以评估移动的遗传元件增殖和基因失活对这种细菌内共生体的结构和功能能力的相对影响。移动的遗传元件和假基因的详细表征揭示了大量存在的不同类型的原噬菌体元件连同5个不同的家庭的IS元件，已在不同水平的基因组中的Sodalis glossinidius的增殖。此外，对基因间区域的详细调查允许表征1501个假基因，比原始注释中描述的972个假基因的数量高得多。假基因结构揭示了基因失活过程中移动的遗传元件增殖的微小影响，大多数假基因起源于多个移码突变和过早的终止密码子。基于它们的全基因和假基因库，对Sodalis glossinidius和采采蝇主要内共生体Wigglesophoria glossinidia的代谢谱的比较揭示了Sodalis glossinidius中途径失活的新情况，精氨酸生物合成，以及与Wigglesophoria glossinidia对硫胺素生物合成的代谢互补的可能情况。对Sodalis glossinidius基因组序列的完整重新分析揭示了从自由生活的祖先到依赖宿主的生活方式的进化过渡的新见解，主要是噬菌体来源的移动的遗传元件的大量增殖，尽管在该细菌基因组中发生的基因失活过程中具有较小的影响。对采采蝇整个内共生菌群的代谢分析揭示了一种可能的初级和次级内共生菌之间的代谢互补现象，这有助于解释采采蝇宿主环境中两种细菌内共生菌的共存。
Background: Genome reduction is a common evolutionary process in symbiotic and pathogenic bacteria. This process has been extensively characterized in bacterial endosymbionts of insects, where primary mutualistic bacteria represent the most extreme cases of genome reduction consequence of a massive process of gene inactivation and loss during their evolution from free-living ancestors. Sodalis glossinidius, the secondary endosymbiont of tsetse flies, contains one of the few complete genomes of bacteria at the very beginning of the symbiotic association, allowing to evaluate the relative impact of mobile genetic element proliferation and gene inactivation over the structure and functional capabilities of this bacterial endosymbiont during the transition to a host dependent lifestyle.Results: A detailed characterization of mobile genetic elements and pseudogenes reveals a massive presence of different types of prophage elements together with five different families of IS elements that have proliferated across the genome of Sodalis glossinidius at different levels. In addition, a detailed survey of intergenic regions allowed the characterization of 1501 pseudogenes, a much higher number than the 972 pseudogenes described in the original annotation. Pseudogene structure reveals a minor impact of mobile genetic element proliferation in the process of gene inactivation, with most of pseudogenes originated by multiple frameshift mutations and premature stop codons. The comparison of metabolic profiles of Sodalis glossinidius and tsetse fly primary endosymbiont Wiglesworthia glossinidia based on their whole gene and pseudogene repertoires revealed a novel case of pathway inactivation, the arginine biosynthesis, in Sodalis glossinidius together with a possible case of metabolic complementation with Wigglesworthia glossinidia for thiamine biosynthesis.Conclusions: The complete re-analysis of the genome sequence of Sodalis glossinidius reveals novel insights in the evolutionary transition from a free-living ancestor to a host-dependent lifestyle, with a massive proliferation of mobile genetic elements mainly of phage origin although with minor impact in the process of gene inactivation that is taking place in this bacterial genome. The metabolic analysis of the whole endosymbiotic consortia of tsetse flies have revealed a possible phenomenon of metabolic complementation between primary and secondary endosymbionts that can contribute to explain the co-existence of both bacterial endosymbionts in the context of the tsetse host.