title: Spontaneous Deletion of an "ORFanage" Region Facilitates Host Adaptation in a "Photosynthetic" Cyanophage.
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.
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: Richard J
authors.initials: RJ
authors.lastname: Puxty
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: Blanca
authors.initials: B
authors.lastname: Perez-Sepulveda
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: Branko
authors.initials: B
authors.lastname: Rihtman
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: David J
authors.initials: DJ
authors.lastname: Evans
authors.affiliation: Warwick Medical School, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: Andrew D
authors.initials: AD
authors.lastname: Millard
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, West Midlands, CV4 7AL, United Kingdom.
authors.forename: David J
authors.initials: DJ
authors.lastname: Scanlan
mesh_terms: D001435:Bacteriophages / Q000235:genetics*; D001483:Base Sequence; D017353:Gene Deletion; D056084:Genetic Fitness; D016679:Genome, Viral; D058507:Host Specificity; D016366:Open Reading Frames; D010802:Phylogeny; D046940:Synechococcus / Q000821:virology*; D026801:Synteny; D014871:Water Microbiology