Prophage maintenance is determined by environment-dependent selective sweeps rather than mutational availability
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Date
2024-04-22
Publication Type
Journal Article
ETH Bibliography
yes
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Abstract
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.
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Publication status
published
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Book title
Journal / series
Volume
34 (8)
Pages / Article No.
1739 - 17490000000
Publisher
Cell Press
Event
Edition / version
Methods
Software
Geographic location
Date collected
Date created
Subject
lysogeny; prophage maintenance; temperate phages; experimental evolution; social resistance; sequential evolution; stochastic modeling
Organisational unit
09497 - Hall, Alex / Hall, Alex
09497 - Hall, Alex / Hall, Alex
02720 - Institut für Integrative Biologie / Institute of Integrative Biology
Notes
Funding
179743 - Evolution and Spread of Antibiotic Resistance Encoded by Prophages (SNF)
19-2 FEL-74 - Dynamics of phage Iysis systems and their evolutionary advantages (ETHZ)
19-2 FEL-74 - Dynamics of phage Iysis systems and their evolutionary advantages (ETHZ)