Early viral infection of cyanobacteria drives bacterial chemotaxis in the oceans

Abstract

Interactions among marine microbes primarily occur through exudation and sensing of dissolved chemical compounds, which ultimately control ecosystem-scale processes such as biomass production, nutrient cycling, carbon fixation, and remineralization. Prior to lysis, viruses alter host metabolism, stimulating the release of dissolved chemical cues from intact plankton. However, the nature and degree of interactions between prelysis, virus-infected cells and neighbouring microbes remain unquantified. Here, we determine the impact of viral infection on dissolved metabolite pools from the marine cyanobacterium Synechococcus and the subsequent chemotactic response of heterotrophic bacteria using time-resolved metabolomics and microfluidics. Metabolites released from intact, virus-infected Synechococcus elicited vigorous chemoattractive responses from heterotrophic bacteria (Vibrio alginolyticus and Pseudoalteromonas haloplanktis), with the strongest responses occurring in the early infection stages and following cell lysis. We provide the first experimental observations of sustained chemotaxis towards live, infected Synechococcus, which is contrasted by no discernible chemotaxis toward uninfected Synechococcus. Finally, metabolite compounds and concentrations driving chemotactic responses were identified using a novel high-throughput microfluidic device. Our findings establish that prior to cell lysis, virus-infected picophytoplankton release compounds that significantly attract motile heterotrophic bacteria, illustrating a viable mechanism for resource transfer to chemotactic bacteria with implications for our understanding of carbon and nutrient flux across trophic levels.