Rapid diversification of coevolving marine Synechococcus and a virus

Abstract

Marine viruses impose a heavy mortality on their host bacteria, whereas at the same time the degree of viral resistance in marine bacteria appears to be high. Antagonistic coevolution--the reciprocal evolutionary change of interacting species--might reconcile these observations, if it leads to rapid and dynamic levels of viral resistance. Here we demonstrate the potential for extensive antagonistic coevolution between the ecologically important marine cyanobacterium Synechococcus and a lytic virus. In a 6-mo-long replicated chemostat experiment, Synechococcus sp. WH7803 and the virus (RIM8) underwent multiple coevolutionary cycles, leading to the rapid diversification of both host and virus. Over the course of the experiment, we detected between 4 and 13 newly evolved viral phenotypes (differing in host range) and between 4 and 11 newly evolved Synechococcus phenotypes (differing in viral resistance) in each chemostat. Genomic analysis of isolates identified several candidate genes in both the host and virus that might influence their interactions. Notably, none of the viral candidates were tail fiber genes, thought to be the primary determinants of host range in tailed bacteriophages, highlighting the difficulty in generalizing results from bacteriophage infecting γ-Proteobacteria. Finally, we show that pairwise virus-host coevolution may have broader community consequences; coevolution in the chemostat altered the sensitivity of Synechoccocus to a diverse suite of viruses, as well as the virus' ability to infect additional Synechococcus strains. Our results indicate that rapid coevolution may contribute to the generation and maintenance of Synechococcus and virus diversity and thereby influence viral-mediated mortality of these key marine bacteria.

Fig. 1.

Synechococcus sp. WH7803 and virus (RIM8) dynamics in the four replicate chemostats A–D. The top third of each panel plots the abundance of Synechococcus cells (red solid line) and infectious viral particles (blue dashed line) over time. For reference, the gray line is cell abundance in the control (no virus) chemostat. The middle of the panel indicates the host phenotypes detected at six time points, and the bottom of the panel, the viral phenotypes detected at the same six time points. Each chemostat was inoculated with ancestral virus (φ₀) on day 0. Host range mutants are numbered in their order of infectivity (e.g., φ₁–φ₁₂), with higher numbers indicating the ability to infect a greater number of host phenotypes. Host phenotypes are labeled by their ability to resist infection by each host range mutant from the same chemostat. For example, S (sensitive to RIM8) is the ancestral host, and R_0–2 is resistant to φ₀, φ₁, and φ₂. We cannot determine whether a particular phenotype evolved directly from another phenotype, because some of the same phenotypes might have evolved more than once. Therefore, the dashed lines connecting the phenotypes are for ease of reading and make only the most parsimonious assumptions. The fully sequenced host and viral isolates are circled in A.

Fig. 2.

Dendrogram of the phenotype of the chemostat Synechococcus populations, where phenotype is defined as the sensitivity or resistance to 31 virus strains from Rhode Island waters (Table S5). The populations are indicated by chemostat (A, B, C, D, and X for the no-virus control) and sampling day. The number of virus strains to which the populations are resistant is noted. Of note, the Synechococcus population from the control chemostat at the end of the experiment (X-167) was similar to populations from day 0 of the experiment, indicating that resistance did not increase in the absence of virus.