Data from: Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects

Genomic decay is a common feature of intracellular bacteria that have entered into symbiosis with plant sap-feeding insects. This study of the whitefly Bemisia tabaci and two bacteria (Portiera aleyrodidarum and Hamiltonella defensa) cohoused in each host cell investigated whether the decay of Portiera metabolism genes is complemented by host and Hamiltonella genes, and compared the metabolic traits of the whitefly symbiosis with other sap-feeding insects (aphids, psyllids, and mealybugs). Parallel genomic and transcriptomic analysis revealed that the host genome contributes multiple metabolic reactions that complement or duplicate Portiera function, and that Hamiltonella may contribute multiple cofactors and one essential amino acid, lysine. Homologs of the Bemisia metabolism genes of insect origin have also been implicated in essential amino acid synthesis in other sap-feeding insect hosts, indicative of parallel coevolution of shared metabolic pathways across multiple symbioses. Further metabolism genes coded in the Bemisia genome are of bacterial origin, but phylogenetically distinct from Portiera, Hamiltonella and horizontally transferred genes identified in other sap-feeding insects. Overall, 75% of the metabolism genes of bacterial origin are functionally unique to one symbiosis, indicating that the evolutionary history of metabolic integration in these symbioses is strongly contingent on the pattern of horizontally acquired genes. Our analysis, further, shows that bacteria with genomic decay enable host acquisition of complex metabolic pathways by multiple independent horizontal gene transfers from exogenous bacteria. Specifically, each horizontally acquired gene can function with other genes in the pathway coded by the symbiont, while facilitating the decay of the symbiont gene coding the same reaction.

基因组衰减（Genomic decay）是与植物吸汁昆虫形成共生关系的胞内细菌的普遍特征。本研究以烟粉虱（Bemisia tabaci）及每个宿主细胞中共存的两种细菌（Portiera aleyrodidarum和Hamiltonella defensa）为对象，探究Portiera代谢基因的衰减是否由宿主及Hamiltonella基因互补，并将烟粉虱共生体系的代谢特征与其他吸汁昆虫（蚜虫、木虱和粉蚧）进行比较。平行基因组与转录组分析显示，宿主基因组参与多项代谢反应，以互补或复制Portiera的功能；Hamiltonella则可能提供多种辅因子及一种必需氨基酸——赖氨酸。烟粉虱中源自昆虫的代谢基因同源物，在其他吸汁昆虫宿主的必需氨基酸合成中也发挥作用，这表明跨多种共生体系的共享代谢通路存在平行协同进化。此外，烟粉虱基因组中编码的部分代谢基因源自细菌，但在系统发育上与Portiera、Hamiltonella及其他吸汁昆虫中已鉴定的水平转移基因存在显著差异。总体而言，75%源自细菌的代谢基因在功能上为某一共生体系所特有，这表明这些共生体系中代谢整合的进化历史强烈依赖于水平获得基因的模式。我们的分析进一步显示，具有基因组衰减的细菌可通过从外源细菌多次独立的水平基因转移，帮助宿主获得复杂代谢通路。具体而言，每个水平获得的基因可与共生体编码的通路中其他基因协同作用，同时促进共生体中编码相同反应的基因发生衰减。