High Diversity and Novel Species of Pseudomonas aeruginosa Bacteriophages

Sepúlveda-Robles, Omar Alejandro; Kameyama, Luis; Guarneros, Gabriel

doi:10.1128/aem.00065-12

Cited by 55 publications

(59 citation statements)

References 40 publications

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“…Unlike phages of other species (Nolan et al, 2006;Dorscht et al, 2009;Sepúlveda-Robles et al, 2012), P. acnes phages show a high genetic similarity. The phages may have evolved recently under limited selection, as no clear lineages can be found among the phages studied, suggesting that these phages may be relatively new to their hosts .…”

Section: Phage Strainsmentioning

confidence: 99%

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

et al. 2015

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The viral population, including bacteriophages, is an important component of the human microbiota, yet is poorly understood. We aim to determine whether bacteriophages modulate the composition of the bacterial populations, thus potentially playing a role in health or disease. We investigated the diversity and host interactions of the bacteriophages of Propionibacterium acnes, a major human skin commensal implicated in acne pathogenesis. By sequencing 48 P. acnes phages isolated from acne patients and healthy individuals and by analyzing the P. acnes phage populations in healthy skin metagenomes, we revealed that P. acnes phage populations in the skin microbial community are often dominated by one strain. We also found phage strains shared among both related and unrelated individuals, suggesting that a pool of common phages exists in the human population and that transmission of phages may occur between individuals. To better understand the bacterium-phage interactions in the skin microbiota, we determined the outcomes of 74 genetically defined Propionibacterium strains challenged by 15 sequenced phages. Depending on the Propionibacterium lineage, phage infection can result in lysis, pseudolysogeny, or resistance. In type II P. acnes strains, we found that encoding matching clustered regularly interspaced short palindromic repeat spacers is insufficient to confer phage resistance. Overall, our findings suggest that the prey-predator relationship between bacteria and phages may have a role in modulating the composition of the microbiota. Our study also suggests that the microbiome structure of an individual may be an important factor in the design of phage-based therapy.

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Section: Phage Strainsmentioning

confidence: 99%

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

et al. 2015

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“…An electron microscopy examination of R. etli phages showed that they belong to the class Caudovirales (Myoviridae and Podoviridae), which has commonly been isolated from other Rhizobium species and many other bacterial species (9,49). It is known that phage morphology is not indicative of genetic relatedness; therefore, we distinguished phages in our collection on the basis of the genome sequence, categorizing them into four types.…”

Section: Discussionmentioning

confidence: 99%

“…Several authors have classified bacteriophages into species on the basis of genome sequence and structural relatedness (49,51). Although the number of phages analyzed in the current study was low, we propose that the genomic types of R. etli might correspond to phage species.…”

Section: Discussionmentioning

confidence: 99%

Narrow-Host-Range Bacteriophages That Infect Rhizobium etli Associate with Distinct Genomic Types

Santamaría¹,

Bustos²,

Sepúlveda-Robles

et al. 2014

Appl Environ Microbiol

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bIn this work, we isolated and characterized 14 bacteriophages that infect Rhizobium etli. They were obtained from rhizosphere soil of bean plants from agricultural lands in Mexico using an enrichment method. The host range of these phages was narrow but variable within a collection of 48 R. etli strains. We obtained the complete genome sequence of nine phages. Four phages were resistant to several restriction enzymes and in vivo cloning, probably due to nucleotide modifications. The genome size of the sequenced phages varied from 43 kb to 115 kb, with a median size of ϳ45 to 50 kb. A large proportion of open reading frames of these phage genomes (65 to 70%) consisted of hypothetical and orphan genes. The remainder encoded proteins needed for phage morphogenesis and DNA synthesis and processing, among other functions, and a minor percentage represented genes of bacterial origin. We classified these phages into four genomic types on the basis of their genomic similarity, gene content, and host range. Since there are no reports of similar sequences, we propose that these bacteriophages correspond to novel species. Bacteriophages have an enormous impact on the ecology and evolution of bacteria (1-3). It is well-known that bacteriophages are agents of gene mobilization across bacterial populations and that the majority of bacterial genomes harbor prophages as well as individual genes of phage origin (4-6). Conversely, temperate phages often carry bacterial genes as a result of prophage induction and recombination (7,8). Some reports indicate that phages exist for almost every known bacterial species (9). In the case of symbiotic nitrogen-fixing bacteria, such as Sinorhizobium meliloti (10, 11), Rhizobium leguminosarum (12-14), Mesorhizobium spp. (15), and Bradyrhizobium spp. (16), phages have been isolated and characterized, but no genome sequences have been reported. As a consequence, genomic comparisons have not been made. To date, only the complete genome sequence of phage 16-3 of S. meliloti has been determined (17).Lytic and temperate phages that infect rhizobial species have been isolated from soils and from lysogens induced after UV light treatment or mitomycin C exposure (11). The presence of phageresistant and -sensitive strains of Rhizobium suggests that phages play a substantial role in the selection or elimination of certain genotypes (11,(18)(19)(20). For instance, bacteriophages reduce the population density of susceptible strains of Rhizobium trifolii on the root surface, allowing resistant strains to form nodules (21,22). In field experiments, the persistence of genetically modified rhizobia has been explained in part by their resistance to phages (19).In the completely sequenced genomes of Rhizobium etli strains CFN42 and CIAT652 (23, 24), there are some open reading frames (ORFs) with relatively high degrees of identity to bacteriophage genes, such as DNA integrases, DNA transferases, lysozymes, and the small and large subunits of DNA terminase. In this work, we obtained a collection of 14 R. etli ...

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“…Comparative genomic analysis (14) shows that 119X is similar to PaP2, a phage that was isolated in China (15). In addition, in a previous study, Sepulveda-Robles et al (16) reported the isolation of 68 virulent P. aeruginosa phages in Mexico. Only 13 of those phages were assigned to the Podoviridae family using electron microscopy.…”

mentioning

confidence: 99%

“…Only 13 of those phages were assigned to the Podoviridae family using electron microscopy. Based on infection, restriction, and DNA hybridization patterns, all of these phages were clustered in a single group, and a partial sequence of one of these phages (PaMx32) suggested that these organisms are similar to 119X (16). Interestingly, these podophages showed the broadest host range among Mexican strains, productively infecting 30% to 60% of the more than 100 clinical isolates tested (16); however, these isolates were unable to infect the type strains PAO1 and PA14.…”

mentioning

confidence: 99%

Genomic and Transcriptional Mapping of PaMx41, Archetype of a New Lineage of Bacteriophages Infecting Pseudomonas aeruginosa

Cruz-Plancarte

Cazares

Guarneros

2016

Appl Environ Microbiol

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Previously, a collection of virulent phages infecting Pseudomonas aeruginosa was isolated from open water reservoirs and residual waters. Here, we described the comparative genomics of a set of five related phages from the collection, the physical structure of the genome, the structural proteomics of the virion, and the transcriptional program of archetypal phage PaMx41. The phage genomes were closely associated with each other and with those of two other P. aeruginosa phages, 119X and PaP2, which were previously filed in the databases. Overall, the genomes were approximately 43 kb, harboring 53 conserved open reading frames (ORFs) and three short ORFs in indel regions and containing 45% GC content. The genome of PaMx41 was further characterized as a linear, terminally redundant DNA molecule. A total of 16 ORFs were associated with putative functions, including nucleic acid metabolism, morphogenesis, and lysis, and eight virion proteins were identified through mass spectrometry. However, the coding sequences without assigned functions represent 70% of the ORFs. The PaMx41 transcription program was organized in early, middle, and late expressed genomic modules, which correlated with regions containing functionally related genes. The high genomic conservation among these distantly isolated phages suggests that these viruses undergo selective pressure to remain unchanged. The 119X lineage represents a unique set of phages that corresponds to a novel phage group. The features recognized in the genomes and the broad host range of clinical strains suggest that these phages are candidates for therapy applications. IMPORTANCEPseudomonas aeruginosa is an opportunistic pathogen that causes stubborn nosocomial infections that are frequently resistant to multiple antibiotics. Bacterial viruses (bacteriophages or phages) represent a natural mechanism for pathogenic bacterial control. Here, a group of virulent phages, previously shown to infect a broad range of clinical P. aeruginosa strains, was characterized at the genomic and molecular levels. These phages belong to a unique and tightly related group. In addition, we conducted a transcriptional study of an archetypal phage of this group to characterize the role of many unknown coding sequences based on expression temporalities. These results contribute to our knowledge of 119X-like phages and, in general, provide information concerning P. aeruginosa podophage diversity and lytic cycles. The renewed interest in the study of genetic diversity in phage populations has been prompted by the accessibility of massive DNA sequencing platforms, which has radically increased the number of phage genome sequences reported in the data banks (1). Presently, genome sequencing is an invaluable tool in phage characterization, which is fundamental at the first stages of the functional annotation of new coding sequences (2). Homologous sequences or structures in data banks provide accurate clues concerning the potential function of coding sequences. In addition, the genome sequence i...

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High Diversity and Novel Species of Pseudomonas aeruginosa Bacteriophages

Cited by 55 publications

References 40 publications

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

Narrow-Host-Range Bacteriophages That Infect Rhizobium etli Associate with Distinct Genomic Types

Genomic and Transcriptional Mapping of PaMx41, Archetype of a New Lineage of Bacteriophages Infecting Pseudomonas aeruginosa

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