Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition

Abstract

Viruses contribute to the mortality of marine microbes, consequentially altering biological species composition and system biogeochemistry. Although it is well established that host cells provide metabolic resources for virus replication, the extent to which infection reshapes host metabolism at a global level and the effect of this alteration on the cellular material released following viral lysis is less understood. To address this knowledge gap, the growth dynamics, metabolism and extracellular lysate of roseophage-infected Sulfitobacter sp. 2047 was studied using a variety of techniques, including liquid chromatography-tandem mass spectrometry (LC-MS/MS)-based metabolomics. Quantitative estimates of the total amount of carbon and nitrogen sequestered into particulate biomass indicate that phage infection redirects B75% of nutrients into virions. Intracellular concentrations for 82 metabolites were measured at seven time points over the infection cycle. By the end of this period, 71% of the detected metabolites were significantly elevated in infected populations, and stable isotope-based flux measurements showed that these cells had elevated metabolic activity. In contrast to simple hypothetical models that assume that extracellular compounds increase because of lysis, a profile of metabolites from infected cultures showed that 470% of the 56 quantified compounds had decreased concentrations in the lysate relative to uninfected controls, suggesting that these small, labile nutrients were being utilized by surviving cells. These results indicate that virus-infected cells are physiologically distinct from their uninfected counterparts, which has implications for microbial community ecology and biogeochemistry.

High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection

“…This is consistent with the results observed for the lytic roseophage (Φ2047B) infection in Sulfitobacter sp. 2047, where approximately 25% of the 82 measured metabolites were altered after a single infection cycle (60-120 min; Ankrah et al, 2014), confirming that host physiology is significantly altered upon phage infection in different host systems. Figure 1 Virus population network reveals distinct clusters within the Pseudomonas phage universe.…”

“…The last phage, PEV2 belongs to the same genus (N4likevirus) as roseophage Φ2047B, studied by Ankrah et al (2014). As both phages share a general genome organization, similarity in the host response was expected.…”

“…Current advances in the field of metabolomics, triggered by the progress in mass spectrometry (Rabinowitz, 2007), allow analysis of multiple time points during infection with high metabolite coverage (Timischl et al, 2008). Ankrah et al (2014) were the first to apply these approaches to investigate the phage infection of an environmentally relevant bacterium. Their results showed significant physiological differences between phage-infected and non-infected cells and raised the question if this response could be generalized to different phage-host systems.…”

A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes

“…First, it is essential to extend the current model to link increasingly strain-resolved information on microbial and viral diversity (Breitbart et al, 2002;Edwards and Rohwer, 2005;Allen et al, 2011) and interactions between viruses and their hosts (Flores et al, 2011;Deng et al, 2012;Weitz et al, 2013) the aggregated representation of virus-host interactions and nutrient feedbacks presented here (see the example of a calibrated model for dynamics including viruses of the algae Phaeocystis globosa; Ruardij et al, 2005). Strain-specific interactions also include the change in host physiology that occurs during infection, whether preceding lysis (Lindell et al, 2007;Ankrah et al, 2014) or during long-term associations with hosts, for example, lysogeny (McDaniel et al, 2008). Such extensions are analogous to the expanded representations of phytoplankton and zooplankton in terms of size-structured and/ or functional type groups (Follows et al, 2007;Stock et al, 2014).…”

“…Incorporating such delays into a multitrophic model requires resolving the likely heterogeneous distribution of latent periods in a given community (for example, see alternative representations of the delay in the models of Beretta and Kuang, 2001;Bonachela and Levin, 2014). In addition, inclusion of a pool of infected host cells also requires improved quantification of ocean processes, such as changes in nutrient uptake within infected cells (Bidle and Vardi, 2011;Ankrah et al, 2014) and grazing of infected cells by zooplankton.…”