Environment-dependent evolution drives divergent adaptive strategies and parasite dynamics in a minimal community

Prophages, phage genomes integrated into bacterial chromosomes, are widespread, yet, the extent to which these resident parasites contribute to host fitness and shape evolutionary trajectories, particularly in polymicrobial environments, remains unclear. Here, we use an experimental evolution approach in which a polylysogenic bacterial strain carrying phages on both its chromosome and plasmids evolves under environmental conditions that modulate the costs and benefits of prophage carriage. By tracking bacterial growth and phage production over time, we uncover divergent, environment-dependent adaptive strategies among lysogens. Some populations evolve dramatically increased phage production, with titers rising over 1,000-fold, whereas in environments where phages impose strong fitness costs, prophages are either purged or domesticated. Across all evolved populations, adaptation is accompanied by defects in cellular segmentation arising from mutations in the divisome and Tat translocation pathways. Whole-genome sequencing revealed shifts in lysate composition, suggesting altered interactions among co-occurring prophages, alongside the loss of plasmid- encoded prophage antibiotic resistance genes and reduced resistance to two distinct antibiotic classes. Together, our results demonstrate that prophages are dynamic evolutionary players whose interactions with host genomes and ecological context jointly shape bacterial adaptation, in complex communities, with implications for exploiting phage-antibiotic trade-offs in therapeutic design.