Article

Photosynthesis genes in marine viruses yield proteins during host infection.

Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
Nature (Impact Factor: 42.35). 12/2005; 438(7064):86-9. DOI: 10.1038/nature04111
Source: PubMed

ABSTRACT 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.

2 Followers
 · 
147 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The discovery of abundant viruses in the oceans and on land has ushered in a quarter century of groundbreaking advancements in our understanding of viruses within ecosystems. Two types of observations from environmental samples - direct counts of viral particles and viral metagenomic sequences - have been critical to these discoveries. Accurate direct counts have established ecosystem-scale trends in the impacts of viral infection on microbial host populations and have shown that viral communities within aquatic and soil environments respond to both short term and seasonal environmental change. Direct counts have been critical for estimating viral production rate, a measurement essential to quantifying the implications of viral infection for the biogeochemical cycling of nutrients within ecosystems. While direct counts have defined the magnitude of viral processes; shotgun sequences of environmental viral DNA - virome sequences - have enabled researchers to estimate the diversity and composition of natural viral communities. Virome-enabled studies have found the virioplankton to contain thousands of viral genotypes in communities where the most dominant viral population accounts for a small fraction of total abundance followed by a long tail of diverse populations. Detailed examination of long virome sequences has led to new understanding of genotype-to-phenotype connections within marine viruses and revealed that viruses carry metabolic genes that are important to maintaining cellular energy during viral replication. Increased access to long virome sequences will undoubtedly reveal more genetic secrets of viruses and enable us to build a genomics rulebook for predicting key biological and ecological features of unknown viruses.
    The Journal of Microbiology 03/2015; 53(3):181-92. DOI:10.1007/s12275-015-5068-6 · 1.53 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The freshwater cyanobacterial virus (cyanophage) A-4L, a podovirus, can infect the model cyanobacterium Anabaena sp. strain PCC 7120 resulting in a high burst size and forming concentric plaques on its lawns. The complete genome sequence of A-4L was determined by the combination of high-throughput sequencing, terminal transferase-mediated polymerase chain reaction and restriction mapping. It contains 41750 bp with 810 bp direct terminal repeats and 38 potential open reading frames. As compared with other cyanobacterial podoviruses in diverse ecosystems, the A-4L has the longest terminal repeat and shares similar genome organizations with freshwater members. Furthermore, phylogenetic analysis based on concatenated sequences of 8 core proteins indicated that freshwater cyanobacterial podoviruses were clustered together and distinct from marine counterparts, suggesting a clear divergence in the cyanobacterial podovirus lineage between freshwater and marine ecosystems. Our findings uncover the unique genome structure of A-4L which contains long direct terminal repeats, and create the first model system to address knowledge gaps in understanding canobacterial virus-host interactions at the molecular level. Copyright © 2015. Published by Elsevier B.V.
    Virus Research 03/2015; 203. DOI:10.1016/j.virusres.2015.03.012 · 2.83 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: All viruses are obligate intracellular parasites and depend on certain host cell functions for multiplication. However, the extent of such dependence and the exact nature of the functions provided by the host cell remain poorly understood. Here, we investigated if non-essential Bacillus subtilis genes are necessary for multiplication of bacteriophage SPP1. Screening of a collection of 2514 single-gene knockouts of non-essential B. subtilis genes yielded only a handful of genes necessary for efficient SPP1 propagation. Among these were genes belonging to the yuk operon, which codes for the Esat-6-like secretion system including the SPP1 receptor protein YueB. In addition, we found that SPP1 multiplication is negatively affected by the absence of two other genes putB and efp. Gene efp encodes elongation factor P, which enhances ribosome activity by alleviating translational stalling during the synthesis of polyproline containing proteins. PutB is an enzyme involved in the proline degradation pathway that is required for infection at the post-exponential growth phase of B. subtilis when the bacterium undergoes a complex genetic re-programming. The putB knock-out shortens significantly the window of opportunity for SPP1 infection during the host cell life cycle. This window is a critical parameter for competitive phage multiplication in the soil environment where B. subtilis rarely meets conditions for exponential growth. Our results in combination with those reported for other virus-host systems suggest that bacterial viruses have evolved towards limited dependence on the non-essential host functions. A successful viral infection largely depends on the ability of the virus to highjack cellular machineries and to redirect the flow of building blocks and energy resources towards viral progeny production. However, the specific virus-host interactions underlying this fundamental transformation are poorly understood. Here, we report on the first systematic analysis of virus-host crosstalk during bacteriophage infection in Gram-positive bacteria. We show that lytic bacteriophage SPP1 is remarkably independent of non-essential genes of its host Bacillus subtilis, with only a handful of cellular genes being necessary for efficient phage propagation. We hypothesize that such limited dependence of the virus on its host results from a constant evolutionary arms-race and might be much more widespread than currently thought. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Journal of Virology 02/2015; 89(5):2875-2883. DOI:10.1128/JVI.03540-14 · 4.65 Impact Factor

Full-text (2 Sources)

Download
10 Downloads
Available from
Aug 26, 2014