MacLean R Craig, Lood Cédric, Wheatley Rachel M
University of Oxford, Department of Biology, 11a Mansfield Rd., Oxford OX1 3SZ, United Kingdom.
All Souls College, High Street, Oxford OX1 4AL, United Kingdom.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf091.
Plasmids are a ubiquitous feature of bacterial genomes, but the forces driving genes and phenotypes to become associated with plasmids are poorly understood. To address this problem, we compared the fitness effects of chromosomal and plasmid genes in the plant symbiont Rhizobium leguminosarum. The relative abundance of beneficial genes on plasmids was very low compared to the chromosome across niches that reflect key steps in plant colonization. Two lines of evidence support the hypothesis that this pattern emerges because evolutionary processes drive beneficial genes to move from plasmids to the bacterial chromosome. First, weakly beneficial genes that increased fitness in a single niche were evenly distributed between plasmids and the chromosome, whereas the chromosome was enriched for strongly beneficial genes that increased fitness across multiple niches. Second, beneficial genes were more prevalent on recently acquired plasmids compared to ancient plasmids. Our findings support a model in which bacterial lineages initially acquire plasmids due to the beneficial genes that they carry, but the movement of beneficial genes to the chromosome gradually erodes the ecological value of plasmids. These findings reconcile existing models of plasmids and highlight the challenge of understanding how plasmids can persist over the long term.
质粒是细菌基因组中普遍存在的特征，但驱动基因和表型与质粒相关联的力量却鲜为人知。为了解决这个问题，我们比较了植物共生菌豆科根瘤菌中染色体基因和质粒基因的适合度效应。在反映植物定殖关键步骤的不同生态位中，与染色体相比，质粒上有益基因的相对丰度非常低。有两条证据支持这样一种假说，即这种模式的出现是因为进化过程驱使有益基因从质粒转移到细菌染色体上。首先，在单个生态位中提高适合度的弱有益基因在质粒和染色体之间均匀分布，而染色体则富集了在多个生态位中提高适合度的强有益基因。其次，与古老质粒相比，有益基因在最近获得质粒上更为普遍。我们的研究结果支持了这样一个模型，即细菌谱系最初由于携带的有益基因而获得质粒，但有益基因向染色体的转移逐渐削弱了质粒的生态价值。这些发现调和了现有的质粒模型，并突出了理解质粒如何长期存在的挑战。
