The elusive object of desire--interactions of bacteriophages and their hosts

Abstract

Bacteria and their viruses (phages) are locked in an evolutionary contest, with each side producing constantly changing mechanisms of attack and defense that are aimed to increase the odds of survival. As a result, phages play central roles in a great variety of genetic processes and increase the rate of evolutionary change of the bacterial host, which could ultimately work to the benefit of the host in a long run.

Figure 1. A model for the role of the host RNAP inhibitor gp2 during T7 infection (after [16*])

At the top, the linear genome of the T7 phage is shown. Arrows indicate three strong early promoters recognized by host RNAP (A1,2,3, red) and phage RNAP promoter ⎞OL (green). Other phage RNAP promoters are omitted for clarity. Below, the concatemeric intermediate of T7 genome replication is shown (open boxes labeled CJ are concatemeric junctions). During the wild-type T7 infection, gp2, the product of phage gene 2 binds to and inhibits host RNAP. T7 RNAP transcribes most of the T7 genome and pauses at CJ, recruiting the processing and packaging factors gp18 and gp19. In the absence of gp2 (bottom), host RNAP transcription proceeds throughout the infection. The transcription elongation rate of host RNAP is much lower than that of T7 RNAP, leading to T7 RNAP stalling behind transcribing host RNAP, and inducing aberrant pauses followed by recruitment of gp18/19 and incorrect processing at the left end of the genome.

Figure 2. Examples of genetic impact of phage on the host

The host bacteria are shown as rounded rectangles. M and N represent generation numbers for host and phage, respectively; their absolute values are arbitrary. M/N+1 indicate progeny generations. A. Co-evolution. A variant of a metabolism gene that specifies a beneficial trait to the host is shown as a green square. Left. Phage that carries the beneficial trait enables faster host metabolism during the course of infection, resulting in a more productive infection. Right. Host bacteria that survive the infection and acquire the beneficial trait have more efficient metabolism and thus have a growth advantage in competition with their predecessors. B. Arms race. An example of a contest between phage DNA protective modifications and host restriction system is shown (based on a situation encountered in T4 phage and its relatives). Each genetic interaction (infection) is shown in the same horizontal level, with the outcome of each interaction listed on the right. Host as the winner indicates that the restriction system has degraded the phage DNA; phage as the winner indicates that the phage DNA is resistant to the host’s restriction system. Evolutionary arms race steps undertaken by host or virus are indicated with bent vertical arrows, alongside the changing side. Adapted from [30]. C. CRISPR. Acquired immunity. Phage infection results in the demise of most cells, with an exception of rare survivors that incorporate portions of phage genome (shown as bar codes) into their CRISPR loci. The newly acquired CRISPR locus blocks propagation of the phage if there is a match between phage sequences and sequences of the CRISPR locus (the match is shown in red).