An Eco-evolutionary Model on Surviving Lysogeny Through Grounding and Accumulation of Prophages

Temperate phages integrate into the bacterial genomes propagating along with the bacterial genomes. Multiple phage elements, representing diverse prophages, are present in most bacterial genomes. The evolutionary events and the ecological dynamics underlying the accumulation of prophage elements in bacterial genomes have yet to be understood. Here, we show that the local wastewater had 7% of lysogens (hosting mitomycin C-inducible prophages), and they showed resistance to superinfection by their corresponding lysates. Genomic analysis of four lysogens and four non-lysogens revealed the presence of multiple prophages (belonging to Myoviridae and Siphoviridae) in both lysogens and non-lysogens. For large-scale comparison, 2180 Escherichia coli genomes isolated from various sources across the globe and 523 genomes specifically isolated from diverse wastewaters were analyzed. A total of 15,279 prophages were predicted among 2180 E. coli genomes and 2802 prophages among 523 global wastewater isolates, with a mean of similar to 5 prophages per genome. These observations indicate that most putative prophages are relics of past bacteria-phage conflicts; they are grounded prophages that cannot excise from the bacterial genome. Prophage distribution analysis based on the sequence homology suggested the random distribution of E. coli prophages within and between E. coli clades. The independent occurrence pattern of these prophages indicates extensive horizontal transfers across the genomes. We modeled the eco-evolutionary dynamics to reconstruct the events that could have resulted in the prophage accumulation accounting for infection, superinfection immunity, and grounding. In bacteria-phage conflicts, the bacteria win by grounding the prophage, which could confer superinfection immunity.

Automated summary

This study investigates the accumulation of prophage elements in bacterial genomes and analyzes the associated environmental factors. The results indicate that most prophages are relics of past bacteria-phage conflicts, and their distribution within bacterial genomes is random with extensive horizontal transfers.