Mason Charles J, Peiffer Michelle, Chen Bosheng, Hoover Kelli, Felton Gary W
Department of Entomology, The Pennsylvania State Universitygrid.29857.31, University Park, Pennsylvania, USA.
College of Advanced Agricultural Sciences, Zhejiang A&F University, Lin'an Hangzhou, People's Republic of China.
Microbiol Spectr. 2022 Aug 31;10(4):e0194122. doi: 10.1128/spectrum.01941-22. Epub 2022 Jun 27.
Gut microbiota can have diverse impacts on hosts, the nature of which often depend on the circumstances. For insect gut microbes, the quality and nature of host diets can be a significant force in swinging the pendulum from inconsequential to functionally important. In our study, we addressed whether beneficial microbes in one species impart similar functions to related species under identical conditions. Using fall armyworm (Spodoptera frugiperda), beet armyworm (Spodoptera exigua), and other noctuid hosts, we implemented an axenic rearing strategy and manipulated gut bacterial populations and dietary conditions. Our results revealed that some gut and Enterobacter isolates can facilitate utilization of a poor diet substrate by fall armyworm, but this was not the case for other more optimized diets. While provided benefits to fall armyworm, it was decidedly antagonistic to beet armyworm (Spodoptera exigua) under identical conditions. Unique isolates and bacterial introductions at early growth stages were critical to how both larval hosts performed. Our results provide robust evidence of the roles in which bacteria support lepidopteran larval growth, but also indicate that the directionality of these relationships can differ among congener hosts. Insects have intimate relationships with gut microbiota, where bacteria can contribute important functions to their invertebrate hosts. Lepidopterans are important insect pests, but how they engage with their gut bacteria and how that translates to impacts on the host are lacking. Here we demonstrate the facultative nature of gut microbiota in lepidopteran larvae and the importance of diet in driving mutualistic or antagonistic relationships. Using multiple lepidopteran species, we uncover that the same bacteria that can facilitate exploitation of a challenging diet in one host severely diminishes larval performance of another larval species. Additionally, we demonstrate the beneficial functions of gut microbiota on the hosts are not limited to one lineage, but rather multiple isolates can facilitate the exploitation of a suboptimal diet. Our results illuminate the context-dependent nature of the gut microbiomes in invertebrates, and how host-specific microbial engagement can produce dramatically different interactions.
肠道微生物群对宿主可能产生多种影响，其性质往往取决于具体情况。对于昆虫肠道微生物而言，宿主饮食的质量和性质可能是一个重要因素，能使微生物从无关紧要转变为具有重要功能。在我们的研究中，我们探讨了在相同条件下，一个物种中的有益微生物是否能赋予相关物种类似的功能。我们以草地贪夜蛾（Spodoptera frugiperda）、甜菜夜蛾（Spodoptera exigua）和其他夜蛾科宿主为研究对象，实施了无菌饲养策略，并对肠道细菌种群和饮食条件进行了调控。我们的结果表明，一些肠道菌和肠杆菌分离株能够促进草地贪夜蛾对劣质饮食底物的利用，但对于其他更优质的饮食则并非如此。虽然这些菌对草地贪夜蛾有益，但在相同条件下，它们对甜菜夜蛾（Spodoptera exigua）却具有明显的拮抗作用。在早期生长阶段引入独特的分离株和细菌对两种幼虫宿主的表现至关重要。我们的结果有力地证明了细菌在支持鳞翅目幼虫生长中所起的作用，但也表明这些关系的方向性在同属宿主之间可能存在差异。昆虫与肠道微生物群有着密切的关系，细菌可以为其无脊椎动物宿主发挥重要功能。鳞翅目昆虫是重要的害虫，但它们如何与肠道细菌相互作用以及这如何转化为对宿主的影响尚不清楚。在这里，我们证明了鳞翅目幼虫肠道微生物群的兼性本质以及饮食在驱动互利或拮抗关系中的重要性。通过使用多种鳞翅目物种，我们发现，在一个宿主中能够促进对具有挑战性饮食利用的相同细菌，会严重降低另一种幼虫物种的幼虫表现。此外，我们证明了肠道微生物群对宿主的有益功能并不局限于一个谱系，而是多种分离株都可以促进对次优饮食的利用。我们的结果揭示了无脊椎动物肠道微生物群的环境依赖性本质，以及宿主特异性微生物相互作用如何产生截然不同的相互作用。
