Institute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland.
Institute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland; Division of Evolution, Infection and Genomics, School of Biological Sciences, University of Manchester, Manchester M13 9PL, UK.
Curr Biol. 2024 Apr 22;34(8):1739-1749.e7. doi: 10.1016/j.cub.2024.03.025. Epub 2024 Apr 9.
Prophages, viral sequences integrated into bacterial genomes, can be beneficial and costly. Despite the risk of prophage activation and subsequent bacterial death, active prophages are present in most bacterial genomes. However, our understanding of the selective forces that maintain prophages in bacterial populations is limited. Combining experimental evolution with stochastic modeling, we show that prophage maintenance and loss are primarily determined by environmental conditions that alter the net fitness effect of a prophage on its bacterial host. When prophages are too costly, they are rapidly lost through environment-specific sequences of selective sweeps. Conflicting selection pressures that select against the prophage but for a prophage-encoded accessory gene can maintain prophages. The dynamics of prophage maintenance additionally depend on the sociality of this accessory gene. Prophage-encoded genes that exclusively benefit the lysogen maintain prophages at higher frequencies compared with genes that benefit the entire population. That is because the latter can protect phage-free "cheaters," reducing the benefit of maintaining the prophage. Our simulations suggest that environmental variation plays a larger role than mutation rates in determining prophage maintenance. These findings highlight the complexity of selection pressures that act on mobile genetic elements and challenge our understanding of the role of environmental factors relative to random chance events in shaping the evolutionary trajectory of bacterial populations. By shedding light on the key factors that shape microbial populations in the face of environmental changes, our study significantly advances our understanding of the complex dynamics of microbial evolution and diversification.
噬菌体是整合到细菌基因组中的病毒序列，它们可能对细菌有益，也可能带来成本。尽管噬菌体的激活和随后的细菌死亡风险存在，但大多数细菌基因组中都存在活跃的噬菌体。然而，我们对维持细菌种群中噬菌体的选择压力的理解是有限的。通过结合实验进化和随机建模，我们表明噬菌体的维持和丢失主要取决于改变噬菌体对其细菌宿主净适应度的环境条件。当噬菌体成本过高时，它们会通过特定环境序列的选择清扫迅速丢失。选择压力相互矛盾，一方面选择对抗噬菌体，但另一方面选择噬菌体编码的辅助基因，这可以维持噬菌体。噬菌体维持的动态还取决于这个辅助基因的社会性。与仅有益于溶源菌的噬菌体编码基因相比，有益于整个种群的噬菌体编码基因可以维持噬菌体的更高频率。这是因为后者可以保护没有噬菌体的“作弊者”，从而降低了维持噬菌体的好处。我们的模拟表明，环境变化在决定噬菌体维持方面比突变率起着更大的作用。这些发现强调了作用于可移动遗传元件的选择压力的复杂性，并挑战了我们对环境因素相对于随机机会事件在塑造细菌种群进化轨迹中的作用的理解。通过阐明面对环境变化塑造微生物种群的关键因素，我们的研究大大提高了我们对微生物进化和多样化的复杂动态的理解。
