Marine bacteria degrade viral particles as a source of nitrogen, phosphorus, and sulfur-rich dissolved organic matter

Abstract Viral particles are abundant in aquatic and soil environments and are operationally defined as part of dissolved organic matter (DOM) in nature. Virions are known to contain rich nitrogen, phosphorus, and sulfur, and they represent a special pool of DOM. Little is known about whether bacteria can use virion DOM to support their growth. In this study, we added purified phage particles to three non-host marine bacterial cultures to investigate how marine bacteria respond to the addition of purified virions. Upon adding virions, we monitored bacterial and viral abundance, bacterial extracellular enzymatic activities, and the composition of virion DOM. Bacterial growth increased with the addition of purified virions, and a large portion of the virions was degraded in the three bacterial cultures within 6 days of incubation. High activities of exocellular alkaline phosphatase and leucine aminopeptidase suggest these exoenzymes are involved in virion degradation. Using an ultra-high-resolution mass spectrometer, we obtained the first van Krevelen diagram of virion DOM molecules. A total of 508 DOM molecules derived from virions were detected, and 77 virion DOM molecules shared across all three bacterial cultures were not detected after 6 days. Together, our results show that bacteria tend to utilize nitrogen-, phosphorus-, and sulfur-rich DOM molecules resulting from virions. This study provides direct evidence that purified virions can serve as a DOM source to support bacterial growth, implying that viruses in the natural environment are a unique source of DOM, which would exert profound impacts on marine food webs and biogenic element cycling.