Okinawa Institute of Science and Technologygrid.250464.1 Graduate University, Okinawa, Japan.
RIKEN Bioresource Research Centre, Tsukuba, Japan.
Microbiol Spectr. 2022 Oct 26;10(5):e0277922. doi: 10.1128/spectrum.02779-22. Epub 2022 Sep 12.
Many insects harbor bacterial endosymbionts that supply essential nutrients and enable their hosts to thrive on a nutritionally unbalanced diet. Comparisons of the genomes of endosymbionts and their insect hosts have revealed multiple cases of mutually-dependent metabolic pathways that require enzymes encoded in 2 genomes. Complementation of metabolic reactions at the pathway level has been described for hosts feeding on unbalanced diets, such as plant sap. However, the level of collaboration between symbionts and hosts that feed on more variable diets is largely unknown. In this study, we investigated amino acid and vitamin/cofactor biosynthetic pathways in Blattodea, which comprises cockroaches and termites, and their obligate endosymbiont Blattabacterium cuenoti (hereafter ). In contrast to other obligate symbiotic systems, we found no clear evidence of "collaborative pathways" for amino acid biosynthesis in the genomes of these taxa, with the exception of collaborative arginine biosynthesis in 2 taxa, and . Nevertheless, we found that several gaps specific to in the folate biosynthetic pathway are likely to be complemented by their host. Comparisons with other insects revealed that, with the exception of the arginine biosynthetic pathway, collaborative pathways for essential amino acids are only observed in phloem-sap feeders. These results suggest that the host diet is an important driving factor of metabolic pathway evolution in obligate symbiotic systems. The long-term coevolution between insects and their obligate endosymbionts is accompanied by increasing levels of genome integration, sometimes to the point that metabolic pathways require enzymes encoded in two genomes, which we refer to as "collaborative pathways". To date, collaborative pathways have only been reported from sap-feeding insects. Here, we examined metabolic interactions between cockroaches, a group of detritivorous insects, and their obligate endosymbiont, , and only found evidence of collaborative pathways for arginine biosynthesis. The rarity of collaborative pathways in cockroaches and contrasts with their prevalence in insect hosts feeding on phloem-sap. Our results suggest that host diet is a factor affecting metabolic integration in obligate symbiotic systems.
许多昆虫体内都携带有细菌内共生体，这些共生体能为宿主提供必要的营养物质，使它们能够在营养不均衡的饮食中茁壮成长。比较内共生体及其昆虫宿主的基因组揭示了许多相互依赖的代谢途径，这些途径需要在两个基因组中编码的酶。已经描述了在以不均衡饮食（如植物汁液）为食的宿主中代谢反应在途径水平上的互补。然而，以更可变的饮食为食的共生体和宿主之间的合作程度在很大程度上是未知的。在这项研究中，我们研究了 Blattodea（包含蟑螂和白蚁）及其专性内共生体 Blattabacterium cuenoti（以下简称）中的氨基酸和维生素/辅因子生物合成途径。与其他专性共生系统不同，我们在这些分类群的基因组中没有发现明显的氨基酸生物合成“协作途径”的证据，除了 2 个分类群中的协作精氨酸生物合成外， 和 。尽管如此，我们发现，在叶酸生物合成途径中， 的几个特定于 的间隙很可能由其宿主来补充。与其他昆虫的比较表明，除了精氨酸生物合成途径外，必需氨基酸的协作途径仅在韧皮部-汁液取食者中观察到。这些结果表明，宿主的饮食是专性共生系统中代谢途径进化的一个重要驱动因素。昆虫与其专性内共生体之间的长期共同进化伴随着基因组整合水平的提高，有时代谢途径需要在两个基因组中编码的酶，我们称之为“协作途径”。迄今为止，协作途径仅在取汁液的昆虫中报道过。在这里，我们研究了蟑螂（一组碎屑食性昆虫）与其专性内共生体之间的代谢相互作用，只发现了精氨酸生物合成的协作途径的证据。蟑螂和 中协作途径的罕见性与它们在以韧皮部汁液为食的昆虫宿主中的普遍性形成对比。我们的结果表明，宿主的饮食是影响专性共生系统中代谢整合的一个因素。
