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.cyanophage | bacterial diversity | arms race

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

“…First, resistant strains with clear growth rate costs and those with no observable growth rate costs are often found (14,25,27,66,67). Second, a mutation that confers resistance to one phage or antibiotic can lead to hypersensitivity to other phages or antibiotics (14,15,27,28,68). Third, just as a different mutation in the same locus can lead to different rates of infection (this study), different mutations can lead to variable levels of resistance to the same antibiotic (69).…”

“…This cost is frequently, but not always, manifested as a reduction in growth rate (24)(25)(26)(27). Recently, an additional type of cost of resistance was identified, that of enhanced infection whereby resistance to one phage leads to greater susceptibility to other phages (14,15,28).…”

“…Although studied only rarely in marine organisms (12)(13)(14)(15)(16), this coexistence is likely to be the result of millions of years of coevolution between these antagonistic interacting partners, as has been well documented for other systems (17)(18)(19)(20). From the perspective of the bacteria, survival entails the selection of cells that are resistant to infection, preventing viral production and enabling the continuation of the cell lineage.…”

Within-host competitive interactions as a mechanism for the maintenance of parasite diversity

“…The patchy structure inherent in the parasite lifestyle sets the stage for heterogeneity across hosts to favour coexistence and for competition to act as a continual selective force on parasite traits. The interplay between ecological and evolutionary forces in maintaining parasite diversity is already well recognized with respect to host genetic diversity [58][59][60]. Analogously, competitive interactions within the host can shape the evolution of parasite phenotypes and can even facilitate the coexistence of multiple parasite types.…”

Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification

“…Smillie et al 2011) and marine picoplankton, mostly of the genera Synechococcus and Prochlorococcus (e.g. Marston et al 2012). In terms of cyanobacteria, it has been further suggested that most HGT are mediated by phages (cyanophages) (e.g.…”