Prophage enhances the ability of deep-sea bacterium Shewanella psychrophila WP2 to utilize D-amino acid

Prophages are prevalent in the marine bacterial genomes and reshape the physiology and metabolism of their hosts. However, whether and how prophages influence the microbial degradation of D-amino acids (D-AAs), which is one of the widely distributed recalcitrant dissolved organic matters (RDOMs) in the ocean, remain to be explored. In this study, we addressed this issue in a representative marine bacterium, Shewanella psychrophila WP2 (WP2), and its integrated prophage SP1. Notably, compared to the WP2 wild-type strain, the SP1 deletion mutant of WP2 (WP2 Delta SP1) exhibited a significantly lower D-glutamate (D-Glu) consumption rate and longer lag phase when D-Glu was used as the sole nitrogen source. The subsequent transcriptome analysis identified 1,523 differentially expressed genes involved in diverse cellular processes, especially that multiple genes related to inorganic nitrogen metabolism were highly upregulated. In addition, the dynamic profiles of ammonium, nitrate, and nitrite were distinct between the culture media of WP2 and WP2 Delta SP1. Finally, we provide evidence that SP1 conferred a competitive advantage to WP2 when D-Glu was used as the sole nitrogen source and SP1-like phages may be widely distributed in the global ocean. Taken together, these findings offer novel insight into the influences of prophages on host metabolism and RDOM cycling in marine environments.