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

Abstract

Interactions between bacterial hosts and their viruses (phages) lead to reciprocal genome evolution through a dynamic co-evolutionary process. Phage-mediated transfer of host genes--often located in genome islands--has had a major impact on microbial evolution. Furthermore, phage genomes have clearly been shaped by the acquisition of genes from their hosts. 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.

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…Of the first 13 transcripts that changed in abundance 6 h after heterotroph addition, 12 encoded members of the high light inducible (hli) family of stress-responsive proteins (the other is of unknown function; Supplementary Table S2). hlis were originally identified as genes that played a role in protecting cells from light shock (Funk and Vermaas, 1999;He et al, 2001;Bhaya et al, 2002), and are now known to respond to a variety of stresses in Prochlorococcus (Tolonen et al, 2006;Lindell et al, 2007;Thompson et al, 2011; Bagby and Chisholm, 2015). hlis are found in all Prochlorococcus genomes, but NATL2A is notable for having a much larger suite of hlis than many other Prochlorococcus (Coleman and Chisholm, 2007;Kettler et al, 2007;Berta-Thompson, 2015), which may be related to the ability of this clade of low-light adapted Prochlorococcus to withstand transient exposure to high light intensities (Malmstrom et al, 2010).…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…RNA isolation, stranded library construction and sequencing Total RNA was extracted from two biological replicates using the mirVana miRNA kit (Ambion, Austin, TX, USA) as described in Tolonen et al (2006) and Lindell et al (2007). DNA was removed using Turbo DNase (Ambion).…”

Four Central Points About Coevolution

“…Cyanobacteria in the genus Prochlorococcus are one of the major photosynthetic organisms in the open ocean, and by some estimates they are the most abundant photosynthetic organisms on earth. The genes for photosynthesis in these species show evidence of repeated transfer back and forth between the cyanobacterial genome and the genomes of the viruses with which they coevolve (Lindell et al 2004(Lindell et al , 2007. The result is a complex distribution of genes for photosynthesis among these coevolving, and ecologically important, hosts and viruses (Sharon et al 2009).…”