Microbial symbionts associate with multicellular organisms on a continuum from facultative associations to mutual codependency. In the oldest intracellular symbioses there is exclusive vertical symbiont transmission, and co-diversification of symbiotic partners over millions of years. Such symbionts often undergo genome reduction due to low effective population sizes, frequent population bottlenecks, and reduced purifying selection. Here, we describe multiple independent acquisition events of closely related defensive symbionts followed by genome erosion in a group of Lagriinae beetles. Previous work in Lagria villosa revealed the dominant genome-eroded symbiont of the genus Burkholderia produces the antifungal compound lagriamide, protecting the beetle’s eggs and larvae from antagonistic fungi. Here, we use metagenomics to assemble 11 additional genomes of lagriamide-producing symbionts from seven different host species within Lagriinae from five countries, to unravel the evolutionary history of this symbiotic relationship. In each host, we detected one dominant genome-eroded Burkholderia symbiont encoding the lagriamide biosynthetic gene cluster. However, we did not find evidence for host-symbiont co-diversification, or for monophyly of the lagriamide-producing symbionts. Instead, our analyses support a single ancestral acquisition of the gene cluster followed by at least four independent symbiont acquisitions and subsequent genome erosion in each lineage. By contrast, a clade of plant-associated relatives retained large genomes but secondarily lost the lagriamide gene cluster. Our results, therefore, reveal a dynamic evolutionary history with multiple independent symbiont acquisitions characterized by a high degree of specificity, and highlight the importance of the specialized metabolite lagriamide for the establishment and maintenance of this defensive symbiosis.

中文翻译：

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在 Lagriinae 甲虫中重复水平采集产生 lagriamide 的共生体


微生物共生体与多细胞生物结合，从兼性关联到相互依赖。在最古老的细胞内共生体中，存在着排他性的垂直共生体传递，以及数百万年来共生伙伴的共同多样化。由于有效种群规模低、种群瓶颈频繁和纯化选择减少，这种共生体通常会经历基因组减少。在这里，我们描述了一组 Lagriinae 甲虫中密切相关的防御共生体的多个独立获取事件，然后是基因组侵蚀。先前在 Lagria villosa 中的工作揭示了 Burkholderia 属的主要基因组侵蚀共生体产生抗真菌化合物 lagriamide，保护甲虫的卵和幼虫免受拮抗真菌的侵害。在这里，我们使用宏基因组学组装了来自 5 个国家的 Lagriinae 中 7 个不同宿主物种的 11 个产生 lagriamide 共生体的另外基因组，以揭示这种共生关系的进化历史。在每个宿主中，我们检测到一个编码 lagriamide 生物合成基因簇的显性基因组侵蚀伯克霍尔德氏体共生体。然而，我们没有发现宿主-共生体共多样化或产生 lagriamide 共生体的单系证据。相反，我们的分析支持基因簇的单个祖先获得，然后每个谱系中至少进行四个独立的共生体获得和随后的基因组侵蚀。相比之下，植物相关亲缘系的一个分支保留了大基因组，但次要丢失了 lagriamide 基因簇。 因此，我们的结果揭示了一个动态的进化历史，具有多个独立的共生体获得，具有高度特异性的特点，并强调了特化代谢物 lagriamide 对于建立和维持这种防御性共生的重要性。