PDF(Pubmed)
Abstract：
Bacterial endosymbionts of eukaryotic hosts typically experience massive genome reduction, but the underlying evolutionary processes are often obscured by the lack of free-living relatives. Endomicrobia, a family-level lineage of host-associated bacteria in the phylum Elusimicrobiota that comprises both free-living representatives and endosymbionts of termite gut flagellates, are an excellent model to study evolution of intracellular symbionts. We reconstructed 67 metagenome-assembled genomes (MAGs) of Endomicrobiaceae among more than 1,700 MAGs from the gut microbiota of a wide range of termites. Phylogenomic analysis confirmed a sister position of representatives from termites and ruminants, and allowed to propose eight new genera in the radiation of Endomicrobiaceae. Comparative genome analysis documented progressive genome erosion in the new genus Endomicrobiellum, which comprises all flagellate endosymbionts characterized to date. Massive gene losses were accompanied by the acquisition of new functions by horizontal gene transfer, which led to a shift from a glucose-based energy metabolism to one based on sugar phosphates. The breakdown of glycolysis and many anabolic pathways for amino acids and cofactors in several subgroups was compensated by the independent acquisition of new uptake systems, including an ATP/ADP antiporter, from other gut microbiota. The putative donors are mostly flagellate endosymbionts from other bacterial phyla, including several, hitherto unknown lineages of uncultured Alphaproteobacteria, documenting the importance of horizontal gene transfer in the convergent evolution of these intracellular symbioses. The loss of almost all biosynthetic capacities in some lineages of Endomicrobiellum suggests that their originally mutualistic relationship with flagellates is on its decline.IMPORTANCEUnicellular eukaryotes are frequently colonized by bacterial and archaeal symbionts. A prominent example are the cellulolytic gut flagellates of termites, which harbor diverse but host-specific bacterial symbionts that occur exclusively in termite guts. One of these lineages, the so-called Endomicrobia, comprises both free-living and endosymbiotic representatives, which offers the unique opportunity to study the evolutionary processes underpinning the transition from a free-living to an intracellular lifestyle. Our results revealed a progressive gene loss in energy metabolism and biosynthetic pathways, compensated by the acquisition of new functions via horizontal gene transfer from other gut bacteria, and suggest the eventual breakdown of an initially mutualistic symbiosis. Evidence for convergent evolution of unrelated endosymbionts reflects adaptations to the intracellular environment of termite gut flagellates.
摘要：
真核宿主的细菌内共生体通常会经历大量的基因组减少，但是潜在的进化过程往往被缺乏自由生活的亲属所掩盖。天麻,门中宿主相关细菌的家族级别谱系，包括白蚁肠鞭毛虫的自由生活代表和内共生体，是研究细胞内共生体进化的极好模型。我们从各种白蚁的肠道微生物群的1,700多个MAG中重建了67个内生菌的宏基因组组装基因组（MAG）。系统发育分析证实了白蚁和反刍动物代表的姐妹地位，并允许在内生菌科的辐射中提出八个新属。比较基因组分析记录了新属的进行性基因组侵蚀。其中包括迄今为止表征的所有鞭毛内共生体。大量基因丢失伴随着通过水平基因转移获得新功能，这导致从基于葡萄糖的能量代谢转变为基于糖磷酸盐的能量代谢。糖酵解的分解和氨基酸和辅因子的许多合成代谢途径在几个亚组中通过独立获得新的摄取系统来补偿。包括ATP/ADP反转录因子,来自其他肠道微生物群。推定的供体大多是来自其他细菌门的鞭毛内共生体，包括几个,迄今为止未知的未培养的阿尔法变形杆菌谱系，记录水平基因转移在这些细胞内共生的融合进化中的重要性。在某些家族中，几乎所有生物合成能力的丧失表明，它们与鞭毛虫的原始互惠关系正在下降。重要细胞真核生物经常被细菌和古细菌共生体定殖。一个突出的例子是白蚁的纤维分解肠鞭毛，它们藏有多种但宿主特异性的细菌共生体，只发生在白蚁肠道中。其中一个血统，所谓的Endomichibia,包括自由生活和内共生的代表，这为研究从自由生活向细胞内生活方式过渡的进化过程提供了独特的机会。我们的结果揭示了能量代谢和生物合成途径中的基因进行性丢失，通过从其他肠道细菌的水平基因转移获得新功能来补偿，并暗示了最初互惠共生的最终崩溃。无关内共生体趋同进化的证据反映了对白蚁肠鞭毛虫细胞内环境的适应。
