Friar Liam, Keepers Kyle, Garber Arkadiy I, McCutcheon John P, Wing Boswell, Kane Nolan C
Department of Geological Sciences, University of Colorado, Boulder, CO, USA.
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
Mol Biol Evol. 2025 Jul 30;42(8). doi: 10.1093/molbev/msaf181.
Vertically inherited symbionts experience different physical, chemical, and population genetic environments than free-living organisms. As a result, they can experience long-term reductions in effective population size (Ne) and weaker purifying selection on genes that are less important in the host-associated environment. Over time, these forces result in gene loss. A comparative genomic approach using independently evolved symbiotic bacteria and free-living relatives can reveal which genes are important in the symbiotic state. We apply this approach to understand why some diazotrophic cyanobacteria evolving as vertically inherited symbionts of photosynthetic eukaryotic hosts have lost their ancestral capacity for photosynthesis while others have retained that capacity. We look specifically at Trichormus azollae, a diazotrophic cyanobacterium that remains photosynthetic after 50 to 90 Ma as a vertically inherited symbiont of Azolla ferns. We show that gene loss is ongoing, with different genes lost across the eight T. azollae strains examined. We apply molecular evolutionary models to genomes of T. azollae and free-living relatives, finding genome-wide signatures of drift in T. azollae consistent with long-term reductions in Ne. Ribosomal proteins and proteins from the energy-capturing photosynthetic light reactions are under stronger purifying selection than genes from other pathways, including nitrogen fixation and photosynthetic carbon fixation. Strong purifying selection is expected for the ribosome given its extraordinary levels of conservation, even in ancient vertically inherited symbionts. That genes in the light reactions are under strong purifying selection and never lost in any strain suggests that energy capture, likely required for energy-intensive nitrogen fixation, remains important to this symbiont.
与自由生活的生物体相比，垂直遗传的共生体经历着不同的物理、化学和群体遗传环境。因此，它们的有效种群大小（Ne）可能会长期减小，并且对在宿主相关环境中不太重要的基因的纯化选择也会减弱。随着时间的推移，这些因素会导致基因丢失。使用独立进化的共生细菌及其自由生活的亲缘种进行比较基因组学研究，可以揭示哪些基因在共生状态下很重要。我们应用这种方法来理解为什么一些作为光合真核宿主的垂直遗传共生体进化的固氮蓝细菌丧失了其祖先的光合作用能力，而其他一些则保留了这种能力。我们特别关注满江红鱼腥藻，这是一种固氮蓝细菌，在作为满江红蕨类植物的垂直遗传共生体经历了50至90百万年后仍保持光合作用能力。我们发现基因丢失仍在继续，在所检测的8个满江红鱼腥藻菌株中不同的基因发生了丢失。我们将分子进化模型应用于满江红鱼腥藻及其自由生活亲缘种的基因组，发现满江红鱼腥藻全基因组存在漂变特征，这与有效种群大小的长期减小一致。核糖体蛋白以及来自捕获能量的光合光反应的蛋白比来自其他途径（包括固氮和光合碳固定）的基因受到更强的纯化选择。鉴于核糖体具有极高的保守性，即使在古老的垂直遗传共生体中也是如此，因此预计核糖体基因会受到强烈的纯化选择。光反应中的基因受到强烈的纯化选择且在任何菌株中都从未丢失，这表明能量捕获可能是能量密集型固氮所必需的，对这种共生体仍然很重要。
