Nechitaylo Taras Y, Sandoval-Calderón Mario, Engl Tobias, Wielsch Natalie, Dunn Diane M, Goesmann Alexander, Strohm Erhard, Svatoš Aleš, Dale Colin, Weiss Robert B, Kaltenpoth Martin
Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, 55128 Mainz, Germany.
Proc Natl Acad Sci U S A. 2021 Apr 27;118(17). doi: 10.1073/pnas.2023047118.
Genome erosion is a frequently observed result of relaxed selection in insect nutritional symbionts, but it has rarely been studied in defensive mutualisms. Solitary beewolf wasps harbor an actinobacterial symbiont of the genus that provides protection to the developing offspring against pathogenic microorganisms. Here, we characterized the genomic architecture and functional gene content of this culturable symbiont using genomics, transcriptomics, and proteomics in combination with in vitro assays. Despite retaining a large linear chromosome (7.3 Mb), the wasp symbiont accumulated frameshift mutations in more than a third of its protein-coding genes, indicative of incipient genome erosion. Although many of the frameshifted genes were still expressed, the encoded proteins were not detected, indicating post-transcriptional regulation. Most pseudogenization events affected accessory genes, regulators, and transporters, but "" also experienced mutations in central metabolic pathways, resulting in auxotrophies for biotin, proline, and arginine that were confirmed experimentally in axenic culture. In contrast to the strong A+T bias in the genomes of most obligate symbionts, we observed a significant G+C enrichment in regions likely experiencing reduced selection. Differential expression analyses revealed that-compared to in vitro symbiont cultures-"" in beewolf antennae showed overexpression of genes for antibiotic biosynthesis, the uptake of host-provided nutrients and the metabolism of building blocks required for antibiotic production. Our results show unusual traits in the early stage of genome erosion in a defensive symbiont and suggest tight integration of host-symbiont metabolic pathways that effectively grants the host control over the antimicrobial activity of its bacterial partner.
基因组退化是昆虫营养共生体中松弛选择常见的结果，但在防御性共生关系中却鲜有研究。独居的狼蜂携带一种放线菌共生体，该共生体为发育中的后代提供保护，使其免受病原微生物侵害。在此，我们结合体外试验，运用基因组学、转录组学和蛋白质组学对这种可培养共生体的基因组结构和功能基因内容进行了表征。尽管保留了一条大型线性染色体（7.3 Mb），但黄蜂共生体在其三分之一以上的蛋白质编码基因中积累了移码突变，这表明其基因组已开始退化。尽管许多发生移码的基因仍在表达，但未检测到所编码的蛋白质，这表明存在转录后调控。大多数假基因化事件影响辅助基因、调节因子和转运蛋白，但“”在中心代谢途径中也发生了突变，导致生物素、脯氨酸和精氨酸营养缺陷，这在无菌培养中得到了实验证实。与大多数专性共生体基因组中强烈的A+T偏向不同，我们在可能经历选择减少的区域观察到显著的G+C富集。差异表达分析显示，与体外共生体培养相比，狼蜂触角中的“”显示出抗生素生物合成基因、宿主提供营养物质的摄取以及抗生素生产所需构件代谢相关基因的过表达。我们的研究结果显示了防御性共生体基因组退化早期的异常特征，并表明宿主-共生体代谢途径紧密整合，有效地使宿主能够控制其细菌伙伴的抗菌活性。
