Most insects harbour influential, yet non-essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi-species nature raises intriguing questions on roles for symbiont-symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species-defined symbiont community structure across US populations of the pea aphid, Acyrthosiphon pisum. Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co-infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co-infection trends. To test whether within-host metabolic interactions predict common versus rare strain-defined communities, we leveraged the high relatedness of our dominant, community-defined symbiont strains vs. 12 pea aphid-derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts-Serratia symbiotica and Rickettsiella viridis. Applying the expansion network algorithm, through additional use of pea aphid and obligate Buchnera symbiont genomes, Serratia and Rickettsiella emerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi-party mutualism within their nutrient-limited, phloem-feeding hosts. Recent, complementary gene inactivation, within the biotin pathways of Serratia and Rickettsiella, raises further questions on the origins of mutualisms and host-symbiont interdependencies.

中文翻译：

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豌豆蚜可遗传兼性共生体之间的隐秘群落结构和代谢相互作用。

大多数昆虫的血腔中都含有有影响力但非必需的可遗传微生物。这些共生体的群落表现出较低的多样性。但它们频繁的多物种性质引发了关于共生体-共生体协同作用在宿主适应中的作用以及共生体群落本身的稳定性的有趣问题。在这项研究中，我们基于美国豌豆蚜 Acyrthosiphon pisum 种群中物种定义的共生群落结构的知识。通过广泛的共生体基因分型，我们表明可以在共生体菌株水平上更精确地定义豌豆蚜的微生物组，菌株变异性决定了先前报道的九种共感染趋势中的五种。现场数据提供了协同适应性效应和共生搭便车的证据，揭示了这些共同感染趋势的原因和后果。为了测试宿主内代谢相互作用是否可以预测常见和稀有菌株定义的群落，我们利用了我们的优势、群落定义的共生菌株与 12 种豌豆蚜衍生的 Gammaproteobacteria 和基因组测序的高度相关性。使用代谢互补性指数的基因组推断揭示了一对共生体——共生沙雷氏菌和绿色立克次体之间的高度合作潜力。应用扩展网络算法，通过额外使用豌豆蚜和专性 Buchnera 共生体基因组，沙雷氏菌和立克次体成为唯一需要双方扩展全生物代谢的共生体群落。通过生物素生物合成途径的共同扩展，这些共生体可能跨越缺失的间隙，在营养有限、以韧皮部为食的宿主内创造多方共生。最近，沙雷氏菌和立克次体生物素途径中的互补基因失活引发了关于互利共生和宿主-共生体相互依赖性的起源的进一步问题。