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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250–14255 (2002)
Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)
Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M. L. & Brussow, H. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417–424 (2003)
Palenik, B. et al. The genome of a motile marine Synechococcus. Nature 424, 1037–1042 (2003)
Sullivan, M. B., Coleman, M. L., Weigele, P., Rohwer, F. & Chisholm, S. W. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biology 3, e144 (2005)
Mann, N. H. et al. The genome of S-PM2, a ‘photosynthetic’ T4-type bacteriophage that infects marine Synechococcus. J. Bacteriol. 187, 3188–3200 (2005)
Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004)
Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Bacterial photosynthesis genes in a virus. Nature 424, 741 (2003)
Millard, A., Clokie, M. R. J., Shub, D. A. & Mann, N. H. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc. Natl Acad. Sci. USA 101, 11007–11012 (2004)
Adir, N., Zer, H., Shochat, S. & Ohad, I. Photoinhibition—a historical perspective. Photosynth. Res. 76, 343–370 (2003)
Havaux, M., Guedeney, G., He, Q. & Grossman, A. R. Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim. Biophys. Acta 1557, 21–33 (2003)
Zeidner, G. et al. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7, 1505–1513 (2005)
Adolph, K. W. & Haskelkorn, R. Photosynthesis and the development of blue–green algal virus N-1. Virology 47, 370–374 (1972)
MacKenzie, J. J. & Haselkorn, R. Photosynthesis and the development of blue–green algal virus SM-1. Virology 49, 517–521 (1972)
Sherman, L. A. Infection of Synechococcus cedrorum by the cyanophage AS-1M. Virology 71, 199–206 (1976)
Suttle, C. A. & Chan, A. M. Marine cyanophages infecting oceanic and coastal strains of Synechococcus—abundance, morphology, cross-infectivity and growth-characteristics. Mar. Ecol. Prog. Ser. 92, 99–109 (1993)
Ginzburg, D., Padan, E. & Shilo, M. Effect of cyanophage infection on CO2 photoassimilation in Plectonema boryanum. J. Virol. 2, 695–701 (1968)
Rahoutei, J., Garcia-Luque, I. & Baron, M. Inhibitioin of photosynthesis by viral infection: effect on PSII structure and function. Physiol. Plant. 110, 286–292 (2000)
Arias, M. C., Lenardon, S. & Taleisnik, E. Carbon metabolism alterations in sunflower plants infected with the sunflower chlorotic mottle virus. J. Phytopath. 151, 267–273 (2003)
Xu, H., Vavilin, D., Funk, C. & Vermaas, W. Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803—consequences for pigment biosynthesis and accumulation. J. Biol. Chem. 279, 27971–27979 (2004)
Bruyant, F. et al. Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: combined effects of light and cell cycle. Limnol. Oceanogr. 50, 850–863 (2005)
Hendrix, R. W., Lawrence, J. G., Hatfull, G. F. & Casjens, S. The origins and ongoing evolution of viruses. Trends Microbiol. 8, 504–508 (2000)
Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127 (1999)
Sullivan, M. B., Waterbury, J. B. & Chisholm, S. W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047–1051 (2003)
Moore, L. R., Post, A. F., Rocap, G. & Chisholm, S. W. Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol. Oceanogr. 47, 989–996 (2002)
Zinser, E. R. et al. Prochlorococcus ecotype abundance in the North Atlantic Ocean revealed by an improved quantitative PCR method. Appl. Environ. Microbiol. (in the press)
Johnson, Z. I. Development and application of the background irradiance gradient–single turnover fluorometer (BIG-STf). Mar. Ecol. Prog. Ser. 283, 73–80 (2004)
Kolber, Z. S., Prasil, O. & Falkowski, P. G. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques—defining methodology and experimental protocols. Biochim. Biophys. Acta 1367, 88–106 (1998)
Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. & Gygi, S. P. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl Acad. Sci. USA 100, 6940–6945 (2003)
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.).
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
This table provides the nucleotide sequences of the primers used in RT and real-time PCR reactions. (DOC 40 kb)
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)
About this article
Cite this article
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
Nature Reviews Microbiology (2021)
The ISME Journal (2021)
Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions
The ISME Journal (2021)
A single-cell polony method reveals low levels of infected Prochlorococcus in oligotrophic waters despite high cyanophage abundances
The ISME Journal (2021)
Nature Communications (2021)