Protist impacts on marine cyanovirocell metabolism

Abstract

The fate of oceanic carbon and nutrients depends on interactions between viruses, prokaryotes, and unicellular eukaryotes (protists) in a highly interconnected planktonic food web. To date, few controlled mechanistic studies of these interactions exist, and where they do, they are largely pairwise, focusing either on viral infection (i.e., virocells) or protist predation. Here we studied population-level responses of Synechococcus cyanobacterial virocells (i.e., cyanovirocells) to the protist Oxyrrhis marina using transcriptomics, endo- and exo-metabolomics, photosynthetic efficiency measurements, and microscopy. Protist presence had no measurable impact on Synechococcus transcripts or endometabolites. The cyanovirocells alone had a smaller intracellular transcriptional and metabolic response than cyanovirocells co-cultured with protists, displaying known patterns of virus-mediated metabolic reprogramming while releasing diverse exometabolites during infection. When protists were added, several exometabolites disappeared, suggesting microbial consumption. In addition, the intracellular cyanovirocell impact was largest, with 4.5- and 10-fold more host transcripts and endometabolites, respectively, responding to protists, especially those involved in resource and energy production. Physiologically, photosynthetic efficiency also increased, and together with the transcriptomics and metabolomics findings suggest that cyanovirocell metabolic demand is highest when protists are present. These data illustrate cyanovirocell responses to protist presence that are not yet considered when linking microbial physiology to global-scale biogeochemical processes.

Early viral infection of cyanobacteria drives bacterial chemotaxis in the oceans

“…Within the first 6 h post infection, four compounds were enriched in the extracellular fraction indicating pre-lysis metabolite release, and three compounds were depleted indicating either reduced release or increased uptake, relative to uninfected cells. Polar exometabolite analyses conducted on these same samples revealed 10 identified metabolites enriched in phage-infected cultures relative to the uninfected control and one metabolite depleted during the pre-lysis or latent phase of infection [19]. Thus, phage infection led to both increases and decreases of particular metabolites relative to uninfected cell cultures, and these exometabolite enrichments or depletions varied over the time course of infection.…”

“…1). Adapted from [19]. (b) Metabolite peak heights (Methods) for two metabolites significantly enriched during the infection cycle, individual data points shown as dots, error bars indicate standard error (SE).…”

“…From the pool of both polar [19] and non-polar exometabolites (Fig. 1c) identified candidate compounds responsible for changes in bacterial chemotactic behaviour were selected based on both the level of enrichment in phage-infected cultures and ecological relevance.…”

“…While such lysis events are ephemeral and generally insufficient to support motile bacterial populations in non-bloom conditions [12], the viral infection cycle of host cells is prolonged over hours. Bacterial aggregation around intact, virus-infected microbes has been observed [14], during which viruses alter host cell metabolism [15] leading to both changes in metabolite composition and increased metabolite release from intact, infected cells [16– 18], including potential chemoattractants in the case of Synechococcus [19]. However, a dearth of direct experimental quantification persists.…”

Multiplexed microfluidic screening of bacterial chemotaxis

“…Viral infection of microbes augments this process and is a principle mechanism [21, 23] for transforming live biomass to readily available organic matter. Lysis [24] and exudation [25] by virus infected cells releases a diverse range and concentration of metabolite and organic material [21]. Furthermore, chemotaxis is essential in initiating bacterial infections and pathogenicity for both animals and plants [26].…”