Comparative transcriptomes reveal differential effects on host metabolism reprogramming in two different pelagiphage-SAR11 infection systems

As the most dominant microorganism in the marine environment, SAR11 bacteria contribute significantly to global carbon and nutrient cycling. Pelagiphages, viruses that infect SAR11, are potential drivers in structuring the communities, shaping the evolution, and reprogramming the metabolism of SAR11. However, interactions between SAR11 and pelagiphages remain poorly understood. In this study, we investigated and compared the transcriptional dynamics of the SAR11 strain, Candidatus Pelagibacter communis HTCC1062, under independent infection with two phylogenetically distinct pelagiphages: the temperate HTVC019P-type pelagiphage HTVC022P and the lytic HTVC023P-type pelagiphage HTVC027P. These two pelagiphages exhibit distinct infection kinetics, with HTVC022P showing a shorter latent period and a faster host takeover. Transcriptome profiling revealed that infection with HTVC022P and HTVC027P led to the differential expression of 136 and 460 host genes, respectively. Compared to the uninfected control, both pelagiphage infections enhanced host transcription, with the majority of differentially expressed genes (DEGs) being upregulated. Both pelagiphages induced the upregulation of host genes involved in DNA metabolism, transcription, translation, central carbon and nitrogen metabolism. Notably, HTVC027P infection led to the upregulation of 56 genes involved in phosphate, sulfur, and iron metabolism, as well as oxidative phosphorylation and one-carbon metabolism. In contrast, HTVC022P had minimal effects on these pathways. These results suggest that distinct pelagiphages exert unique effects on host metabolic processes, implying divergent ecological implications. Collectively, our study provides new insights into SAR11-pelagiphage interactions, enhancing our understanding on the metabolic states of phage-infected SAR11 bacteria and the ecological functions of phages in marine systems.