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. 2005 May;3(5):e144.
doi: 10.1371/journal.pbio.0030144. Epub 2005 Apr 19.

Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations

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Free PMC article

Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations

Matthew B Sullivan et al. PLoS Biol. .
Free PMC article

Abstract

The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish "core" genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of "cyanobacterial" genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent "signature" cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages-T7 and T4-but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.

Figures

Figure 1
Figure 1. Features of the Prochlorococcus Podovirus P-SSP7
(A) Electron micrograph of negative-stained podovirus P-SSP7. Note the distinct T7-like capsid and tail structure. Scale bar indicates 100 nm. (B) Genome arrangement of Prochlorococcus podovirus P-SSP7. The ORFs are sequentially numbered within the boxes, and gene names are designated above the boxes. Gene designations use T7 nomenclature for T7-like genes [24] or microbial nomenclature for non-phage genes. Class I, II, and III genes refer to those in T7 [66] that belong to gene regions primarily involved in host transcription of phage genes (class I), DNA replication (class II), and the formation of the virion structure (class III). The ORFs are designated by boxes, and in this genome, all ORFs are oriented in the same direction. Although the phage genome is one molecule of DNA, the representation is broken to fit on a single page. Note that the P-SSP7 genome is most similar to genomes of the T7-like phages. (C) Taxonomy of best BLASTp hits for P-SSP7. Each predicted coding sequence from the phage genomes was used as a query against the nonredundant database to identify the taxon of the best hit (details in Materials and Methods). Blue slices indicate phage hits, while yellow slices indicate cellular hits. (D) Diagrammatic representation of the genomic regions surrounding a putative phage and host integration site. This site consists of a 42-bp exact match between the podovirus P-SSP7 and its host Prochlorococcus MED4 located directly downstream of the phage integrase gene and the noncoding strand of a host tRNA gene.
Figure 2
Figure 2. Electron Micrograph of Negative-Stained Prochlorococcus Myoviruses P-SSM2 and P-SSM4
Myovirus P-SSM2 with (A) non-contracted tail and (B) contracted tail, and myovirus P-SSM4 with (C) contracted tail and (D) non-contracted tail. Note the T4-like capsid, baseplate, and tail structure in both myoviruses. Scale bars indicate 100 nm.
Figure 3
Figure 3. Genome Arrangement of the Prochlorococcus Myovirus P-SSM2
Gene names are designated above the box representing the ORF where genes were identified; descriptions of genes are in Table 4. The ORFs located above the centering line are on the forward DNA strand, whereas those below the line are on the reverse strand. Although the genome is one molecule, the representation is broken to fit the page. Colors indicate the putative role for the identified genes as inferred from T4 phage. Gene designations use T4 nomenclature for T4-like genes [104] or microbial nomenclature for non-phage genes.
Figure 4
Figure 4. Genome Arrangement of the ProchlorococcusMyovirus P-SSM4
Gene nomenclature is as in Figure 3.
Figure 5
Figure 5. Taxonomy of Best BLASTp Hits for P-SSM2 and P-SSM4
Each predicted coding sequence from both phage genomes was used as a query against the nonredundant database to identify the taxon of the best hit (details in Materials and Methods). Blue slices indicate phage hits, while yellow slices indicate cellular hits.
Figure 6
Figure 6. Bioinformatically Identified Tail Fiber Genes from Prochlorococcus Myoviruses
Red bars indicate P-SSM2 ORFs (labeled as M2); blue bars indicate P-SSM4 ORFs (labeled as M4). Due to space constraints, P-SSM2 orf67 and P-SSM4 orf10 are broken as indicated.

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