A 17th century illustration of the
Copernican model of a heliocentric
universe. Courtesy of Knowledge 2008
Of necessity, viruses rely on their host cells for both energy and molecular building blocks. Typically, lytic infection shuts down the synthesis of host proteins, and the cell's translation machinery is put to work in the service of viral replication. For marine cyanophage, this strategy runs into a troublesome wrinkle.
Let's first digress for a moment and look at the problem faced by all photosynthesizers, cyanobacteria included. Capturing sunlight for cellular work is a risky business. Both UV and visible light can damage the proteins that make up the core of the cell's photosystems. Too much sunlight, and photosynthesis doesn't just level off, it slows down—a phenomenon dubbed photoinhibition. Photoinhibition results when the cell's mechanisms for photosystem repair can't keep up with the damage caused by excess light energy. In cyanobacteria, photosystem II—which catalyzes the light-dependent production of oxygen from water—is particularly vulnerable. At its core sits a dimer of two related proteins, D1 and D2. To keep up with the light-induced damage, D1 turns over very rapidly, and D2 more slowly. De novo synthesis of D1 is required for sustained photosynthesis.
There is a Catch-22 here.
If the infecting cyanophage shuts down the synthesis of host proteins, D1 synthesis stops and photosynthesis declines. Continued photosynthesis is required for maximal phage replication. So what's a cyanophage to do?
Bring a gene for D1 along—that’s the answer! In a broad survey of the cyanophages, Chisholm and colleagues found that 88% of them carry a gene for D1. It is thought that the phages acquired this gene from their hosts on at least four separate occasions. These genes are not accidental baggage, as they are transcribed during infection. About half of the surveyed cyanophages also carry a gene for D2, the other protein in the dimer. This gene could be investigated further and was found to be translated, as well as transcribed. Apparently, a D2 gene is not needed by all cyanophage, but is useful for some. Since D1 and D2 must associate to form a functional dimer, a phage that carries a matched pair would avoid possible incompatibility with the D2 protein of the host. With this in mind, it is not surprising that cyanophage that carry genes for both D1 and D2 infect a broader range of hosts. Phages are great transporters of bacterial genes, but seldom, to our knowledge, have phage taken on board essential metabolic genes from their hosts and employed them for their own purposes.
If photosynthesis is needed for a successful infection, what do these phages do at night? Here’s the beginning of an answer. Light is required for adsorption of at least one Synechococcus phage strain. Infective virions present at night simply must wait around until dawn. A burst of light-induced adsorption after dawn leads to release of progeny virions around dusk, which is not a bad thing to do on several counts. For one, viral replication would benefit from the hours of maximum photosynthesis. For another, being inside a host during the day affords protection from sunlight-induced inactivation, a major cause of phage mortality in surface waters. Lastly, being extracellular at night gets one out of the way of the nocturnal predators that graze on cyanobacteria. Pretty smart.
For cyanophages as well as their cyanobacterial hosts, it is truly a heliocentric world.