Photosynthesis genes in marine viruses yield proteins during host infection. Nature

Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
Nature (Impact Factor: 41.46). 12/2005; 438(7064):86-9. DOI: 10.1038/nature04111
Source: PubMed


Cyanobacteria, and the viruses (phages) that infect them, are significant contributors to the oceanic 'gene pool'. This pool is dynamic, and the transfer of genetic material between hosts and their phages probably influences the genetic and functional diversity of both. For example, photosynthesis genes of cyanobacterial origin have been found in phages that infect Prochlorococcus and Synechococcus, 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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Available from: Debbie Lindell, Aug 26, 2014
    • "These include the photosystem II core reaction center genes, psbA and psbD, two photosynthesis-related hli stress-response genes, and the phycoerythrin biosynthesis gene, cpeT. Two of these genes (psbA and hli) are known to be transcribed with DNA replication and metabolism genes in other cyanophages (Lindell et al., 2005; Lindell et al., 2007) and are thought to be important for continued photosynthetic activity and the production of ATP and reducing equivalents needed for phage DNA replication and nucleotide biosynthesis (Mann et al., 2003; Lindell et al., 2005; Lindell et al., 2007). In addition, two photosynthetic electron transfer genes (petE and PTOX) clustered with the late genes, with maximal transcript levels detected at 2 h after infection (see Supplementary Text). "
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    ABSTRACT: Cyanobacteria are highly abundant in the oceans and are constantly exposed to lytic viruses. The T4-like cyanomyoviruses are abundant in the marine environment and have broad host-ranges relative to other cyanophages. It is currently unknown whether broad host-range phages specifically tailor their infection program for each host, or employ the same program irrespective of the host infected. Also unknown is how different hosts respond to infection by the same phage. Here we used microarray and RNA-seq analyses to investigate the interaction between the Syn9 T4-like cyanophage and three phylogenetically, ecologically and genomically distinct marine Synechococcus strains: WH7803, WH8102 and WH8109. Strikingly, Syn9 led a nearly identical infection and transcriptional program in all three hosts. Different to previous assumptions for T4-like cyanophages, three temporally regulated gene expression classes were observed. Furthermore, a novel regulatory element controlled early-gene transcription, and host-like promoters drove middle gene transcription, different to the regulatory paradigm for T4. Similar results were found for the P-TIM40 phage during infection of Prochlorococcus NATL2A. Moreover, genomic and metagenomic analyses indicate that these regulatory elements are abundant and conserved among T4-like cyanophages. In contrast to the near-identical transcriptional program employed by Syn9, host responses to infection involved host-specific genes primarily located in hypervariable genomic islands, substantiating islands as a major axis of phage-cyanobacteria interactions. Our findings suggest that the ability of broad host-range phages to infect multiple hosts is more likely dependent on the effectiveness of host defense strategies than on differential tailoring of the infection process by the phage.The ISME Journal advance online publication, 1 December 2015; doi:10.1038/ismej.2015.210.
    No preview · Article · Dec 2015 · The ISME Journal
    • "After Prochlorococcus MED4 was infected by cyanopodovirus P-SSP7, the host psbA transcripts declined to 50–60% of the maximal level, while the phage psbA transcripts increased to ∼50% of the total psbA transcripts (host plus phage) (Lindell et al., 2005). During infection, photosystem II efficiency of the host cells only decreased very slightly, suggesting that the phage psbA transcripts might supplement host photosynthesis (Lindell et al., 2005). The high-affinity phosphate-binding protein PstS and its associated ABC transporter (encoded by genes pstA, pstB and pstC) is the predominant P acquisition system in bacteria (Hsieh and Wanner, 2010), including Prochlorococcus (Moore et al., 2005). "
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    ABSTRACT: The transcriptomic responses of bacteria to environmental stresses have been studied extensively, yet we know little about how the stressed cells respond to bacteriophage infection. Here we conducted the first RNA-Seq study of stressed bacteria to phage infection by infecting the marine picocyanobacterium Prochlorococcus NATL2A with cyanomyovirus P-SSM2 under P limitation, a strong selective force in the oceans. Transcripts of the P-acquisition genes in the uninfected cells were enriched after P limitation, including the high-affinity phosphate-binding protein gene pstS. They were still enriched in the infected cells under P-limited conditions. In contrast, transcripts of ATP synthase and ribosomal protein genes were depleted in the uninfected cells after P limitation, but were enriched during phage infection of P-starved cells. Cyanophage P-SSM2 contains pstS, and pstS and its adjacent gene g247 of unknown function were the only phage genes that were enriched under P-limited conditions. We further found that the host pstS transcript number per cell decreased after infection, however, it was still much higher in the P-limited infected cells than that in the nutrient-replete cells. Moreover, phage pstS transcript number per cell was ∼20 times higher than the host copy, which may help maintain the host phosphate uptake rate during infection.
    No preview · Article · Nov 2015 · Environmental Microbiology
    • "Association of Hlips with the PSII complexes and the related Hlip-mediated photoprotection of PSII is most probably related to the presence of hli genes in genomes of some marine cyanophages [51]. These organisms also contain psbA and psbD genes coding for the D1 and D2 subunits of PSII [52] and expression of these genes and synthesis of the viral D1 and D2 proteins in the host cyanobacterial cells have been demonstrated [53]. It is probable that synthesis A C C E P T E D M A N U S C R I P T "
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    ABSTRACT: Cyanobacteria contain a family of genes encoding one-helix high-light-inducible proteins (Hlips) that are homologous to light harvesting chlorophyll a/b-binding proteins of plants and algae. Based on various experimental approaches, a spectrum of functions that includes regulation of chlorophyll biosynthesis, transient chlorophyll binding, quenching of singlet oxygen and non-photochemical quenching of absorbed energy is ascribed to these proteins. However, these functions had not been supported by conclusive experimental evidence until recently when it became clear that Hlips are able to quench absorbed light energy and assist during terminal step(s) of the chlorophyll biosynthesis and early stages of Photosystem II assembly. In this review we summarize and discuss the present knowledge about Hlips and provide a model of how individual members of the Hlip family operate during the biogenesis of chlorophyll-proteins, namely Photosystem II. Copyright © 2015. Published by Elsevier B.V.
    No preview · Article · Sep 2015 · Biochimica et Biophysica Acta
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