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Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.

Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW - PLoS Biol. (2005)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Joint Program in Biological Oceanography, Woods Hole Oceanographic Institution and Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

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.

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Electron Micrograph of Negative-Stained Prochlorococcus Myoviruses P-SSM2 and P-SSM4Myovirus 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.
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pbio-0030144-g002: Electron Micrograph of Negative-Stained Prochlorococcus Myoviruses P-SSM2 and P-SSM4Myovirus 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.

Mentions: P-SSM2 and P-SSM4 are morphologically similar to the Myoviridae (tails are long and contractile; Figure 2). Both have an isometric head, contractile tail, baseplate, and tail fiber structures (Figure 2) that are most consistent (but see isometric head discussion later) with the morphological characteristics of the T4-like phages [39]. Their genomes also have general characteristics that are fully consistent with T4-like status within the Myoviridae (Table 3). Both genomes are relatively large: P-SSM2 has 252,401 bp (327 ORFs; 35.5% G+C content; Figure 3) and P-SSM4 has 178,249 bp (198 ORFs; 36.7% G+C content; Figure 4). An apparent strand bias is noteworthy because only 12 (of 327) and six (of 198) ORFs are predicted on the minus strand in the P-SSM2 and P-SSM4 genomes, respectively. Similar to the lytic T4-like phages, integrase genes were absent. Both genomes assembled and closed, suggesting the circularly permuted chromosome common among the T4-like phages (Table 3). A large portion of the nonhypothetical ORFs have best hits to phage proteins (14% and 21%, respectively) and bacterial proteins (26% and 21%, respectively; Figure 5). The phage hits were most similar to T4-like phage proteins, and about half of the bacterial ORFs were most similar to those from cyanobacteria. As with P-SSP7, most of the translated ORFs from P-SSM2 and P-SSM4 could not be assigned a function (60% and 58%, respectively). The majority of the differences between these two phages are due to the presence of two large clusters of genes (24 total) in P-SSM2 (see Figure 3) that are absent from P-SSM4. These clusters contain many sugar epimerase, transferase, and synthase genes that we hypothesize to be involved in lipopolysaccharide (LPS) biosynthesis. The large genome size, collective gene complement, and morphology suggest both P-SSM2 and P-SSM4 are most closely related to T4-like phages.


Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.

Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW - PLoS Biol. (2005)

Electron Micrograph of Negative-Stained Prochlorococcus Myoviruses P-SSM2 and P-SSM4Myovirus 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.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC1079782&req=5

pbio-0030144-g002: Electron Micrograph of Negative-Stained Prochlorococcus Myoviruses P-SSM2 and P-SSM4Myovirus 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.
Mentions: P-SSM2 and P-SSM4 are morphologically similar to the Myoviridae (tails are long and contractile; Figure 2). Both have an isometric head, contractile tail, baseplate, and tail fiber structures (Figure 2) that are most consistent (but see isometric head discussion later) with the morphological characteristics of the T4-like phages [39]. Their genomes also have general characteristics that are fully consistent with T4-like status within the Myoviridae (Table 3). Both genomes are relatively large: P-SSM2 has 252,401 bp (327 ORFs; 35.5% G+C content; Figure 3) and P-SSM4 has 178,249 bp (198 ORFs; 36.7% G+C content; Figure 4). An apparent strand bias is noteworthy because only 12 (of 327) and six (of 198) ORFs are predicted on the minus strand in the P-SSM2 and P-SSM4 genomes, respectively. Similar to the lytic T4-like phages, integrase genes were absent. Both genomes assembled and closed, suggesting the circularly permuted chromosome common among the T4-like phages (Table 3). A large portion of the nonhypothetical ORFs have best hits to phage proteins (14% and 21%, respectively) and bacterial proteins (26% and 21%, respectively; Figure 5). The phage hits were most similar to T4-like phage proteins, and about half of the bacterial ORFs were most similar to those from cyanobacteria. As with P-SSP7, most of the translated ORFs from P-SSM2 and P-SSM4 could not be assigned a function (60% and 58%, respectively). The majority of the differences between these two phages are due to the presence of two large clusters of genes (24 total) in P-SSM2 (see Figure 3) that are absent from P-SSM4. These clusters contain many sugar epimerase, transferase, and synthase genes that we hypothesize to be involved in lipopolysaccharide (LPS) biosynthesis. The large genome size, collective gene complement, and morphology suggest both P-SSM2 and P-SSM4 are most closely related to T4-like phages.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Joint Program in Biological Oceanography, Woods Hole Oceanographic Institution and Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

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.

Show MeSH
Related in: MedlinePlus