Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution

TLDR: It is hypothesized that phage have evolved to use upregulated host genes, leading to their stable incorporation into phage genomes and their subsequent transfer back to hosts in genome islands, and activation of host genes during infection may be directing the co-evolution of gene content in both host and phages genomes.

Abstract: It's known that interactions between bacteria and their viruses (or phages) can result in a degree of co-evolution of host and phage. A picture of just how close that relationship can become is given by whole-genome expression profiling of the marine cyanobacterium Prochlorococcus and its T7-like cyanophage during infection. A number of host genes are expressed in a coordinated fashion during phage infection, and the phage seem to have evolved to make good use of the gene products. These cyanobacteria are ubiquitous in the oceans and dominant in their particular niche. It seems likely that evolutionary cooperation between host and phage contributes to the success of both partners. Phages have a major impact on the evolution of their bacterial hosts. Providing the first whole genome expression profiling of the marine cyanobacterium Prochlorococcus and its T7-like cyanophage during lytic infection reveals potential mechanistic features of this co-evolutionary process. Interactions between bacterial hosts and their viruses (phages) lead to reciprocal genome evolution through a dynamic co-evolutionary process1,2,3,4,5. Phage-mediated transfer of host genes—often located in genome islands—has had a major impact on microbial evolution1,4,6. Furthermore, phage genomes have clearly been shaped by the acquisition of genes from their hosts2,3,5. Here we investigate whole-genome expression of a host and phage, the marine cyanobacterium Prochlorococcus MED4 and the T7-like cyanophage P-SSP7, during lytic infection, to gain insight into these co-evolutionary processes. Although most of the phage genome was linearly transcribed over the course of infection, four phage-encoded bacterial metabolism genes formed part of the same expression cluster, even though they are physically separated on the genome. These genes—encoding photosystem II D1 (psbA), high-light inducible protein (hli), transaldolase (talC) and ribonucleotide reductase (nrd)—are transcribed together with phage DNA replication genes and seem to make up a functional unit involved in energy and deoxynucleotide production for phage replication in resource-poor oceans. Also unique to this system was the upregulation of numerous genes in the host during infection. These may be host stress response genes and/or genes induced by the phage. Many of these host genes are located in genome islands and have homologues in cyanophage genomes. We hypothesize that phage have evolved to use upregulated host genes, leading to their stable incorporation into phage genomes and their subsequent transfer back to hosts in genome islands. Thus activation of host genes during infection may be directing the co-evolution of gene content in both host and phage genomes.