Abstract
Lysogeny was frequently detected in marine ecosystems, while how temperate phage genomes (prophages) impact marine microbial population or individual dynamics remained poorly understood. Using marine Citromicrobium strain collection as a model system, we revealed that 58% (22/38) were lysogens harboring 31 prophages that can be grouped into five novel genera (φA-φE). Prophage-encoded genes constituted 9% of host accessory genome, significantly expanding the microdiversity among citromicrobial clonal strains. Metagenomic abundance correlations indirectly supported the "Piggyback-the-Winner" dynamics for φA/φE, evidenced by their sublinear growth pattern with increasing host abundance. Most prophages were capable of spontaneous induction and exhibited high lytic activity when triggered by mitomycin C. Importantly, host-range profiling revealed these prophages deployed a dual "Kill-the-Relatives" and "Colonize-the-Relatives" strategy, and meanwhile, they protected parental host strains through superinfection immunity and enhanced phage resistance with greater prophage carriage. Sequencing data showed the dominance of Mu-like phages over non-Mu-like partners upon induced from the double lysogens. Our analysis further hinted at a unique Mu-type within-host competitive strategy: selectively targeting genes of co-resident prophages and host hypothetical genes, while avoiding self-damage and host metabolic genes potentially essential for phage lytic growth or progeny release. Collectively, this work establishes prophages as key architects of bacterial adaptation and provides new perspectives for prophage-driven evolution in marine bacterial hosts.