Symbiotic mutualisms of bacteria and animals are ubiquitous in nature, running a continuum from facultative to obligate from the perspectives of both partners. The loss of functions required for living independently but not within a host gives rise to reduced genomes in many symbionts. Although the phenomenon of genome reduction can be explained by existing evolutionary models, the initiation of the process is not well understood. Here, we describe the microbiome associated with the eggs of the beetle Lagria villosa, consisting of multiple bacterial symbionts related to Burkholderia gladioli, including a reduced-genome symbiont thought to be the exclusive producer of the defensive compound lagriamide. We show that the putative lagriamide-producing symbiont is the only member of the microbiome undergoing genome reduction and that it has already lost the majority of its primary metabolism and DNA repair pathways. The key step preceding genome reduction in the symbiont was likely the horizontal acquisition of the putative lagriamide lga biosynthetic gene cluster. Unexpectedly, we uncovered evidence of additional horizontal transfers to the symbiont's genome while genome reduction was occurring and despite a current lack of genes needed for homologous recombination. These gene gains may have given the genome-reduced symbiont a selective advantage in the microbiome, especially given the maintenance of the large lga gene cluster despite ongoing genome reduction.IMPORTANCE Associations between microorganisms and an animal, plant, or fungal host can result in increased dependence over time. This process is due partly to the bacterium not needing to produce nutrients that the host provides, leading to loss of genes that it would need to live independently and to a consequent reduction in genome size. It is often thought that genome reduction is aided by genetic isolation-bacteria that live in monocultures in special host organs, or inside host cells, have less access to other bacterial species from which they can obtain genes. Here, we describe exposure of a genome-reduced beetle symbiont to a community of related bacteria with nonreduced genomes. We show that the symbiont has acquired genes from other bacteria despite going through genome reduction, suggesting that isolation has not yet played a major role in this case of genome reduction, with horizontal gene gains still offering a potential route for adaptation.

中文翻译：

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水平基因转移到多部分甲虫微生物组中基因组减少的防御性共生体。

细菌和动物的共生共生在自然界中无处不在，从双方的角度来看，从兼性到必然，存在着一个连续体。独立生活所需的功能丧失，而不是在宿主体内，导致许多共生体的基因组减少。尽管基因组减少现象可以用现有的进化模型来解释，但该过程的启动尚不清楚。在这里，我们描述了与甲虫 Lagria villosa 卵相关的微生物组，由与剑兰伯克霍尔德氏菌相关的多种细菌共生体组成，其中包括一种基因组减少的共生体，被认为是防御性化合物拉格酰胺的唯一生产者。我们表明，假定的产生拉格酰胺的共生体是微生物组中唯一经历基因组减少的成员，并且它已经失去了大部分主要代谢和 DNA 修复途径。共生体中基因组减少之前的关键步骤可能是假定的拉格酰胺 lga 生物合成基因簇的水平获取。出乎意料的是，我们发现了在基因组减少的同时，尽管目前缺乏同源重组所需的基因，但共生体基因组发生额外水平转移的证据。这些基因增益可能使基因组减少的共生体在微生物组中具有选择性优势，特别是考虑到尽管基因组不断减少，但大型 lga 基因簇的维持。 重要性 微生物与动物、植物或真菌宿主之间的关联可能导致随着时间的推移产生依赖性。这一过程的部分原因是细菌不需要产生宿主提供的营养，导致其独立生活所需的基因丢失，并导致基因组大小随之减小。人们通常认为，基因组减少是通过基因分离来帮助的——生活在特殊宿主器官或宿主细胞内的单一培养物中的细菌，很少有机会接触其他细菌物种，从而获得基因。在这里，我们描述了将基因组减少的甲虫共生体暴露于具有非减少基因组的相关细菌群落。我们表明，尽管经历了基因组减少，共生体还是从其他细菌获得了基因，这表明隔离在这种基因组减少中尚未发挥主要作用，水平基因增益仍然提供了潜在的适应途径。