Deciphering the Virus Signal Within the Marine Dissolved Organic Matter Pool

Abstract

Viruses are ubiquitously distributed in the marine environment, influencing microbial population dynamics and biogeochemical cycles on a large scale. Due to their small size, they fall into the oceanographic size-class definition of dissolved organic matter (DOM; <0.7 μm). The purpose of our study was to investigate if there is a detectable imprint of virus particles in natural DOM following standard sample preparation and molecular analysis routines using ultrahigh-resolution mass spectrometry (FT-ICR-MS). Therefore, we tested if a molecular signature deriving from virus particles can be detected in the DOM fingerprint of a bacterial culture upon prophage induction and of seawater containing the natural microbial community. Interestingly, the virus-mediated lysate of the infected bacterial culture differed from the cell material of a physically disrupted control culture in its molecular composition. Overall, a small subset of DOM compounds correlated significantly with virus abundances in the bacterial culture setup, accounting for <1% of the detected molecular formulae and <2% of the total signal intensity of the DOM dataset. These were phosphorus- and nitrogen-containing compounds and they were partially also detected in DOM samples from other studies that included high virus abundances. While some of these formulae matched with typical biomolecules that are constituents of viruses, others matched with bacterial cell wall components. Thus, the identified DOM molecular formulae were probably not solely derived from virus particles but were partially also derived from processes such as the virus-mediated bacterial cell lysis. Our results indicate that a virus-derived DOM signature is part of the natural DOM and barely detectable within the analytical window of ultrahigh-resolution mass spectrometry when a high natural background is present.

Bottom-up and top-down controls on Alteromonas macleodii lead to different dissolved organic matter compositions

“…S6B), suggesting that the lysed material consisted of more high hydrogen saturated organic compounds. These results are opposed to recent studies in which viral lysis of a bacterial culture ( Rhodobacteraceae ) consisted of more aromatic and unsaturated formulas with higher O/C values [ 31 ], and Synechococcus viral lysates contained mainly unsaturated and oxygen-rich formulas [ 29 ]. Because different microbial groups were used in our and the previous studies, viral lysis of different groups will lead to the differences in the DOM composition.…”

“…Similarly, we demonstrate that the viral lysate from A. macleodii is enriched in N-containing saturated molecules. Although viruses themselves are enriched in N and P and they thereby can enrich the N- and P-containing formulas in the resulting DOM [ 31 , 74 ], more importantly, viruses are able to impact host metabolisms by changing substrate utilization and energy production in order to produce progeny [ 75 ]. Such virus-mediated changes have been shown to alter the host cellular metabolic state [ 76 ].…”

Phosphorus limitation determines the quality of dissolved organic matter released by marine heterotrophic prokaryotes

“…HP can release DOM as a direct by-product of their biosynthesis and growth (Kawasaki and Benner 2006) or by the imbalance between their anabolism and catabolism (Carlson et al 2007). Viral lysis and sloppy grazing by protozoans can also release DOM from HP (Nagata 2000;Middelboe and Jørgensen 2006) and alter its composition (Gruber et al 2006;Heinrichs et al 2022).…”