Dataset Information

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.

SUBMITTER: Puxty RJ

PROVIDER: S-EPMC4503421 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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

Puxty Richard J RJ Perez-Sepulveda Blanca B Rihtman Branko B Evans David J DJ Millard Andrew D AD Scanlan David J DJ

PloS one 20150715 7

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 ...[more]

PMID: 26177354

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Project description:Host-pathogen co-evolutionary dynamics force microbial plant pathogens to constantly develop and adjust specific adaptations to thrive in their plant host, and therefore also act as strong drivers of divergence and speciation in pathogens. Factors that confer host specialization and determine host specificity are very diverse and range from molecular and morphological strategies to metabolic and reproductive adaptations. Identification of these key factors is a major goal in the study of pathogen evolution and may aid the development of sustainable crops and crop protection strategies. We here took a novel experimental approach and conducted comparative microscopy and transcriptome analyses of the closely related, recently diverged fungal pathogens Zymoseptoria tritici, Z. pseudotritici, and Z. ardabiliae that establish compatible and incompatible interactions with wheat. Although infections of the incompatible species induce plant defense response during invasion of stomatal openings, we found a highly conserved early-infection program among the three species. The transcriptional programs of the three pathogens are conserved to a large extent, as only 9.2% of the 8,885 orthologous genes are significantly differentially expressed during initial infection of wheat. The genes up-regulated in the compatible pathogen reflect adaptation to growth in wheat tissue e.g., by re-programming of fungal metabolism. In contrast, genes primarily involved in counteracting cell stress and damage are strongly induced in the incompatible species. Based on the species-specific gene expression profiles, we further identified nine candidate genes encoding putative effectors and host-specificity determinants in Z. tritici. These effectors are strongly induced in the compatible species and may interfere with host immune suppression. We also identify putative necrotrophic effectors which are induced at the onset of necrotrophic growth. Together, the results presented here indicate that host specialization has involved transcriptional adaptation of a relatively small number of genes. Our findings demonstrate the potential comparative analyses of compatible and incompatible infections present for identifying traits involved in pathogen evolution and host specialization.

Dataset Information

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

Publications

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

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