Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University, Mainz, Germany.
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, 305-8566, Japan.
ISME J. 2023 Jul;17(7):1029-1039. doi: 10.1038/s41396-023-01415-y. Epub 2023 Apr 21.
Many insects engage in stable nutritional symbioses with bacteria that supplement limiting essential nutrients to their host. While several plant sap-feeding Hemipteran lineages are known to be simultaneously associated with two or more endosymbionts with complementary biosynthetic pathways to synthesize amino acids or vitamins, such co-obligate symbioses have not been functionally characterized in other insect orders. Here, we report on the characterization of a dual co-obligate, bacteriome-localized symbiosis in a family of xylophagous beetles using comparative genomics, fluorescence microscopy, and phylogenetic analyses. Across the beetle family Bostrichidae, most investigated species harbored the Bacteroidota symbiont Shikimatogenerans bostrichidophilus that encodes the shikimate pathway to produce tyrosine precursors in its severely reduced genome, likely supplementing the beetles' cuticle biosynthesis, sclerotisation, and melanisation. One clade of Bostrichid beetles additionally housed the co-obligate symbiont Bostrichicola ureolyticus that is inferred to complement the function of Shikimatogenerans by recycling urea and provisioning the essential amino acid lysine, thereby providing additional benefits on nitrogen-poor diets. Both symbionts represent ancient associations within the Bostrichidae that have subsequently experienced genome erosion and co-speciation with their hosts. While Bostrichicola was repeatedly lost, Shikimatogenerans has been retained throughout the family and exhibits a perfect pattern of co-speciation. Our results reveal that co-obligate symbioses with complementary metabolic capabilities occur beyond the well-known sap-feeding Hemiptera and highlight the importance of symbiont-mediated cuticle supplementation and nitrogen recycling for herbivorous beetles.
许多昆虫与细菌形成稳定的营养共生关系，这些细菌为其宿主补充有限的必需营养素。虽然有几个吸食植物汁液的半翅目昆虫谱系同时与两种或更多具有互补生物合成途径的共生菌相关联，以合成氨基酸或维生素，但其他昆虫目中尚未对这种共同必需的共生关系进行功能表征。在这里，我们使用比较基因组学、荧光显微镜和系统发育分析，报道了一个木质甲虫科的双重共同必需的细菌共生体的特征。在甲虫科的 Bostrichidae 中，大多数被研究的物种都携带了细菌共生体 Shikimatogenerans bostrichidophilus，它在其严重简化的基因组中编码莽草酸途径，以产生酪氨酸前体，可能补充了甲虫的角质层生物合成、硬化和黑化。Bostrichid 甲虫的一个分支还容纳了共同必需的共生菌 Bostrichicola ureolyticus，它通过回收尿素和提供必需氨基酸赖氨酸来补充 Shikimatogenerans 的功能，从而在氮素贫瘠的饮食中提供额外的益处。这两个共生体代表了 Bostrichidae 中的古老共生关系，随后经历了基因组侵蚀和与宿主的协同进化。虽然 Bostrichicola 被反复丢失，但 Shikimatogenerans 一直保留在整个家族中，并表现出完美的协同进化模式。我们的研究结果表明，具有互补代谢能力的共同必需共生关系不仅存在于广为人知的吸食植物汁液的半翅目昆虫中，还突出了共生体介导的角质层补充和氮回收对食草甲虫的重要性。
