Many phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction between microbe, insect, and plant. Here, we focus on two bacterial symbionts of the darkling beetle Lagria villosa that belong to the genus Burkholderia; the culturable strain B. gladioli Lv-StA and the reduced-genome strain Burkholderia Lv-StB. The strains can be transmitted vertically and confer protection to the beetle’s eggs, but Lv-StA can also proliferate in plants, and both symbiont strains have presumably evolved from plant pathogens. Notably, little is known about the role of the environment for the transmission dynamics and the maintenance of the symbionts. Through manipulative assays, we demonstrate the transfer of the symbionts from the beetle to wheat, rice and soybean plants, as well as leaf litter. In addition, we confirm that aposymbiotic larvae can pick up Lv-StA from dry leaves and the symbiont can successfully establish in the beetle’s symbiotic organs. Also, we show that the presence of plants and soil in the environment improves symbiont maintenance. These results indicate that the symbionts of L. villosa beetles are still capable of interacting with plants despite signatures of genome erosion and suggest that a mixed-mode of bacterial transmission is likely key for the persistence of the symbiosis.

许多植食性昆虫携带共生细菌，可以从亲本垂直传播给后代，或从无关宿主或环境中水平获得。在后一种情况下，植物是共生体转移的潜在途径，因此可以促进微生物、昆虫和植物之间的三方相互作用。在这里，我们专注于暗甲虫的两种细菌共生体拉格里亚维洛萨 属于该属的 伯克霍尔德菌; 可培养菌株剑兰 Lv-StA 和基因组减少的菌株 伯克霍尔德菌Lv-StB。这些菌株可以垂直传播并为甲虫的卵提供保护，但 Lv-StA 也可以在植物中增殖，并且两种共生菌株可能都是从植物病原体进化而来的。值得注意的是，人们对环境对传播动力学和共生体维持的作用知之甚少。通过操纵性分析，我们证明了共生体从甲虫转移到小麦、水稻和大豆植物以及落叶中。此外，我们确认无共生体幼虫可以从干叶中提取 Lv-StA，并且共生体可以在甲虫的共生器官中成功建立。此外，我们表明环境中植物和土壤的存在改善了共生体的维持。这些结果表明共生体L. villosa 尽管有基因组侵蚀的特征，甲虫仍然能够与植物相互作用，并表明细菌传播的混合模式可能是共生持续存在的关键。