Department of Botany and Plant Pathology, Oregon State Universitygrid.4391.f, Corvallis, Oregon, USA.
Department of Evolution, Ecology and Organismal Biology, University of California Riverside, Riverside, California, USA.
mBio. 2022 Jun 28;13(3):e0007422. doi: 10.1128/mbio.00074-22. Epub 2022 Apr 13.
Root nodulating rhizobia are nearly ubiquitous in soils and provide the critical service of nitrogen fixation to thousands of legume species, including staple crops. However, the magnitude of fixed nitrogen provided to hosts varies markedly among rhizobia strains, despite host legumes having mechanisms to selectively reward beneficial strains and to punish ones that do not fix sufficient nitrogen. Variation in the services of microbial mutualists is considered paradoxical given host mechanisms to select beneficial genotypes. Moreover, the recurrent evolution of non-fixing symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. Here, we deconstructed hundreds of genome sequences from genotypically and phenotypically diverse strains and revealed mechanisms that generate variation in symbiotic nitrogen fixation. We show that this trait is conferred by a modular system consisting of many extremely large integrative conjugative elements and few conjugative plasmids. Their transmissibility and propensity to reshuffle genes generate new combinations that lead to uncooperative genotypes and make individual partnerships unstable. We also demonstrate that these same properties extend beneficial associations to diverse host species and transfer symbiotic capacity among diverse strains. Hence, symbiotic nitrogen fixation is underpinned by modularity, which engenders flexibility, a feature that reconciles evolutionary robustness and instability. These results provide new insights into mechanisms driving the evolution of mobile genetic elements. Moreover, they yield a new predictive model on the evolution of rhizobial symbioses, one that informs on the health of organisms and ecosystems that are hosts to symbionts and that helps resolve the long-standing paradox. Genetic variation is fundamental to evolution yet is paradoxical in symbiosis. Symbionts exhibit extensive variation in the magnitude of services they provide despite hosts having mechanisms to select and increase the abundance of beneficial genotypes. Additionally, evolution of uncooperative symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. We analyzed genome sequences of bacteria that in symbioses with legume hosts, fix nitrogen, a nutrient essential for ecosystems. We show that genes for symbiotic nitrogen fixation are within elements that can move between bacteria and reshuffle gene combinations that change host range and quality of symbiosis services. Consequently, nitrogen fixation is evolutionarily unstable for individual partnerships, but is evolutionarily stable for legume- symbioses in general. We developed a holistic model of symbiosis evolution that reconciles robustness and instability of symbiosis and informs on applications of rhizobia in agricultural settings.
根瘤菌几乎普遍存在于土壤中，为包括主要农作物在内的数千种豆科植物提供关键的固氮服务。然而，尽管豆科植物有机制来选择性地奖励有益的菌株，并惩罚那些不能固定足够氮的菌株，但不同根瘤菌菌株提供的固定氮的数量差异很大。考虑到宿主选择有益基因型的机制，微生物共生体服务的这种变异性被认为是矛盾的。此外，非固氮共生体基因型的反复进化预计会使共生关系不稳定，但很少观察到崩溃。在这里，我们从表型和基因型多样的菌株中构建了数百个基因组序列，并揭示了导致共生固氮变异的机制。我们表明，这种特性是由一个由许多非常大的整合共轭元件和少数共轭质粒组成的模块化系统赋予的。它们的可传递性和重新排列基因的倾向产生了新的组合，导致了不合作的基因型，并使个体伙伴关系不稳定。我们还证明，这些相同的特性将有益的关联扩展到不同的宿主物种，并在不同的菌株之间转移共生能力。因此，共生固氮是由模块性支撑的，这赋予了灵活性，这一特征调和了进化的稳健性和不稳定性。这些结果为驱动移动遗传元件进化的机制提供了新的见解。此外，它们提供了一个关于根瘤菌共生关系进化的新预测模型，该模型为共生体宿主的生物体和生态系统的健康提供了信息，并有助于解决长期存在的悖论。遗传变异是进化的基础，但在共生关系中却是矛盾的。尽管宿主有机制选择和增加有益基因型的丰度，但共生体在提供服务的程度上表现出广泛的变异。此外，不合作的共生体基因型的进化预计会使共生关系不稳定，但很少观察到崩溃。我们分析了与豆科植物宿主共生时固定氮的细菌的基因组序列，氮是生态系统所必需的营养物质。我们表明，共生固氮的基因位于可以在细菌之间移动并重新排列基因组合的元件中，这些基因组合改变了宿主范围和共生服务的质量。因此，氮固定对于单个伙伴关系来说是进化上不稳定的，但对于一般的豆科植物-共生关系来说是进化上稳定的。我们提出了一个整体的共生进化模型，调和了共生的稳健性和不稳定性，并为农业中根瘤菌的应用提供了信息。
