Cyanophages and Their Role in the Ecology of Cyanobacteria

Summary

Cyanophages belong to three recognized families of double-stranded DNA viruses; Myoviridae (contractile tails); Styloviridae (long non-contractile tails); and Podoviridae (short tails). They have a complex pattern of host ranges, are widely distributed, and can be readily isolated from marine and fresh waters. Although cyanophages are related to other bacteriophages, it is likely that they evolved more than 3 billion years ago when cyanobacteria diverged from other prokaryotes. In marine waters, genetically-diverse Myoviridae which infect Synechococcus spp. are the most abundant cyanophages; Styloviridae and Podoviridae are most commonly isolated from fresh waters. Morphological evidence also suggests that freshwater and marine myoviruses are more closely related to each other than they are to other bacteriophages. Cyanophages that infect phycoerythrin-rich Synechococcus spp. can be extremely abundant in coastal marine environments where they can occur at titers in excess of 10⁶ mL^-1 and 10⁵ g^-1 of sediment. In surface waters abundance varies over orders of magnitude on a seasonal basis. Abundance follows that of Synechococcus, with evidence for a threshold in Synechococcus of ca. 10³ to 10⁴ mL^-1 beyond which cyanophage abundance increases greatly. In nearshore waters the high concentrations of cyanophages and Synechococcus result in high encounter frequencies and selection for Synechococcus communities that are largely resistant to infection. Encounters are much less frequent offshore and this leads to the appearance of a community that appears to have low resistance to infection. In freshwaters, viruses which infect filamentous cyanobacteria appear to be most abundant and also show strong seasonal dynamics however; even in the most eutrophic environments titers are orders of magnitude less than in productive coastal waters. Little effort was made to screen freshwaters for cyanophages that infect phycoerythrin-rich Synechococcus. In marine surface waters turnover times for cyanophage populations range from hours to days. Solar radiation has a major affect on cyanophage infectivity and results in the selection of cyanophage communities that are more resistant to destruction by sunlight during summer. In contrast to surface waters, infectious cyanophages can persist in sediments for at least 100 years. Although the effect of cyanophages on the mortality of cyanobacterial communities is likely to be variable, current estimates suggest that cyanophages are responsible for the removal of approximately 3% of marine Synechococcus on a daily basis. In addition to lytic infection, lysogenic associations were clearly demonstrated in filamentous and unicellular cyanobacteria, but the ecological implications of lysogeny remain unexplored. Environmental factors and the physiological state of cyanobacteria clearly affect cyanophage-cyanobacterial interactions but remain poorly understood.