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Spontaneous Deletion of an "ORFanage" Region Facilitates Host Adaptation in a "Photosynthetic" Cyanophage.

Puxty RJ, Perez-Sepulveda B, Rihtman B, Evans DJ, Millard AD, Scanlan DJ - PLoS ONE (2015)

Bottom Line: These ORFs are found at one loci and are not homologous to any proteins in any other sequenced organism (ORFans).We demonstrate a fitness cost to S-PM2WT associated with possession of these ORFs under standard laboratory growth.We posit that these ORFs contribute to the flexible gene content of cyanophages and offer a distinct fitness advantage in freshwater and hypersaline environments.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.

ABSTRACT
Viruses have been suggested to be the largest source of genetic diversity on Earth. Genome sequencing and metagenomic surveys reveal that novel genes with unknown functions are abundant in viral genomes. Yet few observations exist for the processes and frequency by which these genes are gained and lost. The surface waters of marine environments are dominated by marine picocyanobacteria and their co-existing viruses (cyanophages). Recent genome sequencing of cyanophages has revealed a vast array of genes that have been acquired from their cyanobacterial hosts. Here, we re-sequenced the cyanophage S-PM2 genome after 10 years of near continuous passage through its marine Synechococcus host. During this time a spontaneous mutant (S-PM2d) lacking 13% of the S-PM2 ORFs became dominant in the cyanophage population. These ORFs are found at one loci and are not homologous to any proteins in any other sequenced organism (ORFans). We demonstrate a fitness cost to S-PM2WT associated with possession of these ORFs under standard laboratory growth. Metagenomic surveys reveal these ORFs are present in various aquatic environments, are likely of cyanophage origin and appear to be enriched in environments from the extremes of salinity (freshwater and hypersaline). We posit that these ORFs contribute to the flexible gene content of cyanophages and offer a distinct fitness advantage in freshwater and hypersaline environments.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic analysis, isolation sites and ORFan presence in S-PM2.(a) Phylogenetic reconstruction of the sequenced T4-like cyanophages showing the sub-cluster containing S-PM2, Syn1 and S-CAM1. Phylogenetic reconstruction is based on the amino acid alignment of gp20 sequences. (b) Map showing the year and site of isolation of cyanophages S-PM2, Syn1 and S-CAM1. (c) Genetic map of S-PM2 and closely related cyanophages Syn1 and S-CAM1. Orthologous ORFs are linked by grey lines. Locations of tRNAs are shown by purple triangles. Blue filled ORFs in the S-PM2 panel show the locations of the ORFans. Top panel shows reads mapped to S-PM2 from high-throughput sequencing.
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pone.0132642.g001: Phylogenetic analysis, isolation sites and ORFan presence in S-PM2.(a) Phylogenetic reconstruction of the sequenced T4-like cyanophages showing the sub-cluster containing S-PM2, Syn1 and S-CAM1. Phylogenetic reconstruction is based on the amino acid alignment of gp20 sequences. (b) Map showing the year and site of isolation of cyanophages S-PM2, Syn1 and S-CAM1. (c) Genetic map of S-PM2 and closely related cyanophages Syn1 and S-CAM1. Orthologous ORFs are linked by grey lines. Locations of tRNAs are shown by purple triangles. Blue filled ORFs in the S-PM2 panel show the locations of the ORFans. Top panel shows reads mapped to S-PM2 from high-throughput sequencing.

Mentions: S-PM2 is an obligately lytic myovirus with a genome ~196 kb in size, encoding 244 ORFs [23]. Comparative genomics with other sequenced marine cyanomyoviruses suggests that S-PM2 is an “outlier” [15]. This is due to the fact that S-PM2 lacks many of the marine cyanophage “nearly-core” genes identified in [15]. Of particular interest is the paucity of so called “auxiliary metabolic genes” (AMGs sensu [24]) in S-PM2, in comparison with other marine cyanophages [15]. Despite this, S-PM2 still possesses a relatively large genome, containing genes that are unique amongst other cyanophages. Indeed, a contiguous region of the genome from ORF 017 to 050 contains 33 ORFans and as such has been called an “ORFanage” region [25]. This ORFanage region can be clearly distinguished when compared with the closely related cyanophages Syn1 and S-CAM1 (Fig 1A and 1C), which were isolated from disparate locations over an 18 year period (Fig 1B).


Spontaneous Deletion of an "ORFanage" Region Facilitates Host Adaptation in a "Photosynthetic" Cyanophage.

Puxty RJ, Perez-Sepulveda B, Rihtman B, Evans DJ, Millard AD, Scanlan DJ - PLoS ONE (2015)

Phylogenetic analysis, isolation sites and ORFan presence in S-PM2.(a) Phylogenetic reconstruction of the sequenced T4-like cyanophages showing the sub-cluster containing S-PM2, Syn1 and S-CAM1. Phylogenetic reconstruction is based on the amino acid alignment of gp20 sequences. (b) Map showing the year and site of isolation of cyanophages S-PM2, Syn1 and S-CAM1. (c) Genetic map of S-PM2 and closely related cyanophages Syn1 and S-CAM1. Orthologous ORFs are linked by grey lines. Locations of tRNAs are shown by purple triangles. Blue filled ORFs in the S-PM2 panel show the locations of the ORFans. Top panel shows reads mapped to S-PM2 from high-throughput sequencing.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4503421&req=5

pone.0132642.g001: Phylogenetic analysis, isolation sites and ORFan presence in S-PM2.(a) Phylogenetic reconstruction of the sequenced T4-like cyanophages showing the sub-cluster containing S-PM2, Syn1 and S-CAM1. Phylogenetic reconstruction is based on the amino acid alignment of gp20 sequences. (b) Map showing the year and site of isolation of cyanophages S-PM2, Syn1 and S-CAM1. (c) Genetic map of S-PM2 and closely related cyanophages Syn1 and S-CAM1. Orthologous ORFs are linked by grey lines. Locations of tRNAs are shown by purple triangles. Blue filled ORFs in the S-PM2 panel show the locations of the ORFans. Top panel shows reads mapped to S-PM2 from high-throughput sequencing.
Mentions: S-PM2 is an obligately lytic myovirus with a genome ~196 kb in size, encoding 244 ORFs [23]. Comparative genomics with other sequenced marine cyanomyoviruses suggests that S-PM2 is an “outlier” [15]. This is due to the fact that S-PM2 lacks many of the marine cyanophage “nearly-core” genes identified in [15]. Of particular interest is the paucity of so called “auxiliary metabolic genes” (AMGs sensu [24]) in S-PM2, in comparison with other marine cyanophages [15]. Despite this, S-PM2 still possesses a relatively large genome, containing genes that are unique amongst other cyanophages. Indeed, a contiguous region of the genome from ORF 017 to 050 contains 33 ORFans and as such has been called an “ORFanage” region [25]. This ORFanage region can be clearly distinguished when compared with the closely related cyanophages Syn1 and S-CAM1 (Fig 1A and 1C), which were isolated from disparate locations over an 18 year period (Fig 1B).

Bottom Line: These ORFs are found at one loci and are not homologous to any proteins in any other sequenced organism (ORFans).We demonstrate a fitness cost to S-PM2WT associated with possession of these ORFs under standard laboratory growth.We posit that these ORFs contribute to the flexible gene content of cyanophages and offer a distinct fitness advantage in freshwater and hypersaline environments.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.

ABSTRACT
Viruses have been suggested to be the largest source of genetic diversity on Earth. Genome sequencing and metagenomic surveys reveal that novel genes with unknown functions are abundant in viral genomes. Yet few observations exist for the processes and frequency by which these genes are gained and lost. The surface waters of marine environments are dominated by marine picocyanobacteria and their co-existing viruses (cyanophages). Recent genome sequencing of cyanophages has revealed a vast array of genes that have been acquired from their cyanobacterial hosts. Here, we re-sequenced the cyanophage S-PM2 genome after 10 years of near continuous passage through its marine Synechococcus host. During this time a spontaneous mutant (S-PM2d) lacking 13% of the S-PM2 ORFs became dominant in the cyanophage population. These ORFs are found at one loci and are not homologous to any proteins in any other sequenced organism (ORFans). We demonstrate a fitness cost to S-PM2WT associated with possession of these ORFs under standard laboratory growth. Metagenomic surveys reveal these ORFs are present in various aquatic environments, are likely of cyanophage origin and appear to be enriched in environments from the extremes of salinity (freshwater and hypersaline). We posit that these ORFs contribute to the flexible gene content of cyanophages and offer a distinct fitness advantage in freshwater and hypersaline environments.

No MeSH data available.


Related in: MedlinePlus