Photosynthesis genes in marine viruses yield proteins during host infection

Abstract

Cyanobacteria, and the viruses (phages) that infect them, are significant contributors to the oceanic ‘gene pool’1,2. This pool is dynamic, and the transfer of genetic material between hosts and their phages3,4,5,6 probably influences the genetic and functional diversity of both. For example, photosynthesis genes of cyanobacterial origin have been found in phages that infect Prochlorococcus5,7 and Synechococcus8,9, the numerically dominant phototrophs in ocean ecosystems. These genes include psbA, which encodes the photosystem II core reaction centre protein D1, and high-light-inducible (hli) genes. Here we show that phage psbA and hli genes are expressed during infection of Prochlorococcus and are co-transcribed with essential phage capsid genes, and that the amount of phage D1 protein increases steadily over the infective period. We also show that the expression of host photosynthesis genes declines over the course of infection and that replication of the phage genome is a function of photosynthesis. We thus propose that the phage genes are functional in photosynthesis and that they may be increasing phage fitness by supplementing the host production of these proteins.

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Figure 1: Photosynthesis and phage infection.
Figure 2: Expression of phage and host photosynthesis genes.
Figure 3: Analysis of host and phage peptides.
Figure 4: Co-transcription of phage photosynthesis and capsid genes.

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Acknowledgements

We thank T. Rector and R. Steen for doing the Affymetrix GeneChip experiments; C. Steglich, M. Sullivan, M. Coleman, and E. Zinser for discussions; and M. Sullivan for comments on the manuscript. This research was supported by grants from the National Science Foundation (to S.W.C.), the Gordon and Betty Moore Foundation's Program in Marine Microbiology (to S.W.C), and the Department of Energy Genomes to Life Program (to S.W.C and G.M.C.).

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Correspondence to Sallie W. Chisholm.

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Supplementary information

Supplementary Table S1

This table provides the nucleotide sequences of the primers used in RT and real-time PCR reactions. (DOC 40 kb)

Supplementary Figure S1

This figure shows transcript levels of the phage and host psbA genes during infection as determined by RT-PCR. These results show that the expression of the phage psbA gene increases with time during infection while host psbA expression declines. These results confirm those from microarray analysis presented in Fig. 2a. (DOC 43 kb)

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Lindell, D., Jaffe, J., Johnson, Z. et al. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005). https://doi.org/10.1038/nature04111

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