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
    • "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.
    Biochimica et Biophysica Acta 09/2015; DOI:10.1016/j.bbabio.2015.08.011 · 4.66 Impact Factor
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    • "Lytic phages hijack their host's metabolic machinery to produce and release progeny (Young, 1992; Catalão et al., 2013), whereas temperate phages can either initiate a lytic infection or a lysogenic state in which the phage genome is either integrated into the host's chromosome or maintained extrachromosmally (Bertani and Bertani, 1971; Jiang and Paul, 1998). While lytic phages are ecologically important due to their influences on host abundance and nutrient cycling (Lindell et al., 2005; Shelford et al., 2012; Jover et al., 2014), the ecological impact of temperate phages is much less well studied. It is likely, however, that temperate phages have significant impact as they might improve host fitness by increasing growth rate (Edlin et al., 1975) or providing resistance to phage superinfection (Bossi et al., 2003) or other stressors (Wang et al., 2010). "
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    ABSTRACT: Bacterial viruses (phages) influence global biogeochemical cycles by modulating bacterial mortality, metabolic output and evolution. However, our understanding of phage infections is limited by few methods and environmentally-relevant model systems. Prior work showed that Cellulophaga baltica phage ϕ38:1 infects its original host lytically, and an alternative host either delayed lytically or lysogenically. Here we investigate these infections through traditional and marker-based approaches, and introduce geneELISA for high-throughput examination of phage-host interactions. All methods confirmed the lytic, original host infection (70-80 minute latent period; ∼8 phages produced per cell), but alternative host assays were more challenging. A 4.5-hour experiment detected no phage production by plaque assay, whereas phageFISH and geneELISA revealed phage genome replication and a latent period ≥150 minutes. Longer experiments (26 hours) suggested an 11-hour latent period and a burst size of 871 by plaque assay, whereas phageFISH identified cell lysis starting at <5 hours and lasting to 11 hours, but for only 7% to 21.5% of infected cells, respectively, and with ∼39 phages produced per cell. These findings help resolve the nature of the alternative host infection as delayed lytic and offer solutions to methodological challenges for studying inefficient phage-host interactions. This article is protected by copyright. All rights reserved.
    Environmental Microbiology 08/2015; DOI:10.1111/1462-2920.13009 · 6.20 Impact Factor
    • "Cyanobacteria play a key role in oceanic photosynthesis and contribute to the global carbon cycle and oxygen supply (Li et al., 1993; Liu et al., 1997; Partensky et al., 1999). Genes encoding for photosystem-II (PSII) reaction centers (the D1 and D2 proteins encoded by the psbA and psbD genes, respectively) are found in cultured and uncultured phages that infect marine cyanobacteria (Mann et al., 2003; Lindell et al., 2004; Millard et al., 2004; Lindell et al., 2005; Sullivan et al., 2005; Zeidner et al., 2005; Sullivan et al., 2006; Sharon et al., 2007), are expressed upon infection (Lindell et al., 2005; Clokie et al., 2006; Lindell et al., 2007), and it was suggested that this increases phage fitness (Bragg and Chisholm, 2008; Hellweger, 2009). See (Puxty et al., 2014) for a recent review on viral 'photosynthesis'. "
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    ABSTRACT: Marine photosynthesis is largely driven by cyanobacteria, namely Synechococcus and Prochlorococcus. Genes encoding for photosystem (PS) I and II reaction center proteins are found in cyanophages and are believed to increase their fitness. Two viral PSI gene arrangements are known, psaJF→C→A→B→K→E→D and psaD→C→A→B. The shared genes between these gene cassettes and their encoded proteins are distinguished by %G+C and protein sequence, respectively. The data on the psaD→C→A→B gene organization was reported from only two partial gene cassettes coming from Global Ocean Sampling (GOS) stations in the Pacific and Indian oceans. Now we have extended our search to 370 marine stations from six metagenomic projects. Genes corresponding to both PSI gene arrangements were detected in the Pacific, Indian, and Atlantic Oceans, confined to a strip along the equator (30°N and 30°S). In addition, we found that the predicted structure of the viral PsaA protein from the psaD→C→A→B organization contains a lumenal loop conserved in PsaA proteins from Synechococcus, but is completely absent in viral PsaA proteins from the psaJF→C→A→B→K→E→D gene organization and most Prochlorococcus strains. This may indicate a co-evolutionary scenario where cyanophages containing either of these gene organizations infect cyanobacterial ecotypes biogeographically restricted to the 30°N and 30°S equatorial strip. This article is protected by copyright. All rights reserved.
    Environmental Microbiology 08/2015; DOI:10.1111/1462-2920.13036 · 6.20 Impact Factor
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