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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 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.

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Figure 1: Infection dynamics of Prochlorococcus MED4 by podovirus P-SSP7.
Figure 2: Temporal expression dynamics of P-SSP7 phage genes during infection of Prochlorococcus MED4.
Figure 3: Transcriptional profiles of Prochlorococcus MED4 genes with time after infection by P-SSP7.

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Acknowledgements

We thank C. Steglich, S. Bhattacharya, H. Keller, L. Thompson, P. Weigele, S. Choe, D. Endy, S. Kosuri, M. Shmoish and J. Aach for discussions, and J. Waldbauer and M. Osburne for comments on the manuscript, and the MIT Center for Environmental Health Sciences. This work was funded by the DOE Genomes to Life System Biology Center Grant (G.M.C. and S.W.C.), the Gordon and Betty Moore Foundation’s Marine Microbiology Program (S.W.C.), and the National Science Foundation (S.W.C).

The microarray data have been deposited in the GEO database under the accession number GSE8382.

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Correspondence to Sallie W. Chisholm.

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Supplementary information

Supplementary Information

This file contains Supplementary Methods with details of the experimental methodology and additional references; Supplementary Tables 1-8 and Supplementary Figures 1-10 with Legends showing proteomic and promoter results, list of upregulated host genes, phage gene expression cluster analysis and significance, hli gene expression table, RT-PCR verification of microarray results and normalization methods, comparison of phage quantification methods to quantitative PCR results and lists of primers used in this study (PDF 1691 kb)

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Lindell, D., Jaffe, J., Coleman, M. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86 (2007). https://doi.org/10.1038/nature06130

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