Contribution of phage‐derived genomic islands to the virulence of facultative bacterial pathogens

Busby, Ben; Kristensen, David M.; Koonin, Eugene V.

doi:10.1111/j.1462-2920.2012.02886.x

Cited by 65 publications

(61 citation statements)

References 50 publications

(55 reference statements)

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“…Apparently, these are bacterial genes that have been acquired by and transferred between viruses on a relatively small scale. It is well known that gene exchange also occurs in the reverse direction, from phages to hosts: for instance, many virulence factors in pathogenic bacteria come from integrated prophages (40,41). However, due to the discounting of matches in the prophage regions for the calculation of VQ, most such genes are recognized as viral with a medium to high VQ; for example, Shiga toxins that are never observed in bacteria outside detected prophages have a VQ of 1.0.…”

Section: Resultsmentioning

confidence: 99%

Orthologous Gene Clusters and Taxon Signature Genes for Viruses of Prokaryotes

et al. 2013

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Viruses are the most abundant biological entities on earth and encompass a vast amount of genetic diversity. The recent rapid increase in the number of sequenced viral genomes has created unprecedented opportunities for gaining new insight into the structure and evolution of the virosphere. Here, we present an update of the phage orthologous groups (POGs), a collection of 4,542 clusters of orthologous genes from bacteriophages that now also includes viruses infecting archaea and encompasses more than 1,000 distinct virus genomes. Analysis of this expanded data set shows that the number of POGs keeps growing without saturation and that a substantial majority of the POGs remain specific to viruses, lacking homologues in prokaryotic cells, outside known proviruses. Thus, the great majority of virus genes apparently remains to be discovered. A complementary observation is that numerous viral genomes remain poorly, if at all, covered by POGs. The genome coverage by POGs is expected to increase as more genomes are sequenced. Taxon-specific, single-copy signature genes that are not observed in prokaryotic genomes outside detected proviruses were identified for two-thirds of the 57 taxa (those with genomes available from at least 3 distinct viruses), with half of these present in all members of the respective taxon. These signatures can be used to specifically identify the presence and quantify the abundance of viruses from particular taxa in metagenomic samples and thus gain new insights into the ecology and evolution of viruses in relation to their hosts.

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Section: Resultsmentioning

confidence: 99%

Orthologous Gene Clusters and Taxon Signature Genes for Viruses of Prokaryotes

et al. 2013

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“…Analogous to the COG database, each viral COG (VOG) represents all of the descendants of a single ancestral gene (orthologs) within the analyzed set of genomes. The pVOGs can be used for gene prediction and functional annotation in new virus genomes (11–13), metagenomic data (14–21) and host genomes containing proviruses (22,23). In addition to gene prediction and protein function, the pVOGs provide a third form of annotation, namely the distribution (presence or absence) of the constituent genes across viruses and cellular organisms, i.e.…”

Section: Introductionmentioning

confidence: 99%

Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation

2016

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Viruses are the most abundant and diverse biological entities on earth, and while most of this diversity remains completely unexplored, advances in genome sequencing have provided unprecedented glimpses into the virosphere. The Prokaryotic Virus Orthologous Groups (pVOGs, formerly called Phage Orthologous Groups, POGs) resource has aided in this task over the past decade by using automated methods to keep pace with the rapid increase in genomic data. The uses of pVOGs include functional annotation of viral proteins, identification of genes and viruses in uncharacterized DNA samples, phylogenetic analysis, large-scale comparative genomics projects, and more. The pVOGs database represents a comprehensive set of orthologous gene families shared across multiple complete genomes of viruses that infect bacterial or archaeal hosts (viruses of eukaryotes will be added at a future date). The pVOGs are constructed within the Clusters of Orthologous Groups (COGs) framework that is widely used for orthology identification in prokaryotes. Since the previous release of the POGs, the size has tripled to nearly 3000 genomes and 300 000 proteins, and the number of conserved orthologous groups doubled to 9518. User-friendly webpages are available, including multiple sequence alignments and HMM profiles for each VOG. These changes provide major improvements to the pVOGs database, at a time of rapid advances in virus genomics. The pVOGs database is hosted jointly at the University of Iowa at http://dmk-brain.ecn.uiowa.edu/pVOGs and the NCBI at ftp://ftp.ncbi.nlm.nih.gov/pub/kristensen/pVOGs/home.html.

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“…Bacterial genomes often contain a range of intact and remnant prophage elements (1)(2)(3), and ecologically important bacterial traits are believed to be phage-derived (e.g., phage-derived bacteriocins) (4). Phage-related sequences are observed more frequently in pathogenic than nonpathogenic strains (5), and prophage acquisition can be associated with changes in pathogen virulence (6,7). Prophages can directly contribute accessory gene functions (1,8) or disrupt bacterial genes by insertional inactivation.…”

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Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

Davies

James

Williams

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Temperate phages drive genomic diversification in bacterial pathogens. Phage-derived sequences are more common in pathogenic than nonpathogenic taxa and are associated with changes in pathogen virulence. High abundance and mobilization of temperate phages within hosts suggests that temperate phages could promote withinhost evolution of bacterial pathogens. However, their role in pathogen evolution has not been experimentally tested. We experimentally evolved replicate populations of Pseudomonas aeruginosa with or without a community of three temperate phages active in cystic fibrosis (CF) lung infections, including the transposable phage, ɸ4, which is closely related to phage D3112. Populations grew as freefloating biofilms in artificial sputum medium, mimicking sputum of CF lungs where P. aeruginosa is an important pathogen and undergoes evolutionary adaptation and diversification during chronic infection. Although bacterial populations adapted to the biofilm environment in both treatments, population genomic analysis revealed that phages altered both the trajectory and mode of evolution. Populations evolving with phages exhibited a greater degree of parallel evolution and faster selective sweeps than populations without phages. Phage ɸ4 integrated randomly into the bacterial chromosome, but integrations into motility-associated genes and regulators of quorum sensing systems essential for virulence were selected in parallel, strongly suggesting that these insertional inactivation mutations were adaptive. Temperate phages, and in particular transposable phages, are therefore likely to facilitate adaptive evolution of bacterial pathogens within hosts.Pseudomonas aeruginosa | cystic fibrosis | mobile genetic element | experimental evolution | bacteriophage C omparative genomics suggests that temperate phages play an important role in the evolution and genomic diversification of bacterial pathogens (1). Bacterial genomes often contain a range of intact and remnant prophage elements (1-3), and ecologically important bacterial traits are believed to be phage-derived (e.g., phage-derived bacteriocins) (4). Phage-related sequences are observed more frequently in pathogenic than nonpathogenic strains (5), and prophage acquisition can be associated with changes in pathogen virulence (6, 7). Prophages can directly contribute accessory gene functions (1, 8) or disrupt bacterial genes by insertional inactivation. Of particular note are the transposable class of temperate phages (also known as mutator phages), including D3112 of Pseudomonas aeruginosa (9, 10), which integrate throughout the chromosome disrupting existing genes and increasing the supply of mutations available to selection. Recent reports of high rates of phage mobilization within hosts (11) and high temperate phage abundance in humans (12), including at sites of chronic infection where phage particles have been observed to exceed bacterial host densities by 10-to 100-fold (13), suggests that temperate phages could play an important role in driving within-host...

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Contribution of phage‐derived genomic islands to the virulence of facultative bacterial pathogens

Cited by 65 publications

References 50 publications

Orthologous Gene Clusters and Taxon Signature Genes for Viruses of Prokaryotes

Orthologous Gene Clusters and Taxon Signature Genes for Viruses of Prokaryotes

Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation

Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

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