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Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis.

ABSTRACT: We characterized two newly isolated myoviruses, Bp8p-C and Bp8p-T, infecting the ginger rhizome rot disease pathogen Bacillus pumilus GR8. The plaque of Bp8p-T exhibited a clear center with a turbid rim, suggesting that Bp8p-T could transform into latent phage. Lysogeny assays showed that both the two phages could form latent states, while Bp8p-T could form latent phage at a higher frequency and stability than Bp8p-C. The genomes of Bp8p-C and Bp8p-T were 151,417 and 151,419 bp, respectively; both encoded 212 putative proteins, and only differed by three nucleotides. Moreover, owing to this difference, Bp8p-C encoded a truncated, putative actin-like plasmid segregation protein Gp27-C. Functional analysis of protein Gp27 showed that Gp27-T encoded by Bp8p-T exhibited higher ATPase activity and assembly ability than Gp27-C. The results indicate that the difference in Gp27 affected the phage lysogenic ability. Structural proteome analysis of Bp8p-C virion resulted in the identification of 14 structural proteins, among which a pectin lyase-like protein, a putative poly-gamma-glutamate hydrolase, and three proteins with unknown function, were firstly identified as components of the phage virion. Both phages exhibited specific lytic ability to the host strain GR8. Bp8p-C showed better control effect on the pathogen in ginger rhizome slices than Bp8p-T, suggesting that Bp8p-C has a potential application in bio-control of ginger rhizome rot disease.

SUBMITTER: Yuan Y

PROVIDER: S-EPMC4272706 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis.

Yuan Yihui Y Peng Qin Q Wu Dandan D Kou Zheng Z Wu Yan Y Liu Pengming P Gao Meiying M

Applied and environmental microbiology 20141024 1

We characterized two newly isolated myoviruses, Bp8p-C and Bp8p-T, infecting the ginger rhizome rot disease pathogen Bacillus pumilus GR8. The plaque of Bp8p-T exhibited a clear center with a turbid rim, suggesting that Bp8p-T could transform into latent phage. Lysogeny assays showed that both the two phages could form latent states, while Bp8p-T could form latent phage at a higher frequency and stability than Bp8p-C. The genomes of Bp8p-C and Bp8p-T were 151,417 and 151,419 bp, respectively; bo ...[more]

PMID: 25344242

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Project description:Bacteriophages are large and diverse components of the biosphere, and many phages are temperate. Upon infection, temperate phages can establish lysogeny in which a prophage is typically integrated into the bacterial chromosome. Here, we describe the phenomenon of tRNA-dependent lysogeny, a previously unrecognized behavior of some temperate phages. tRNA-dependent lysogeny is characterized by two unusual features. First, a phage-encoded tyrosine family integrase mediates site-specific recombination between a phage attP site and a bacterial attB site overlapping a host tRNA gene. However, attP and attB share only a short (~10 bp) common core such that a functional tRNA is not reconstructed upon integration. Second, the phage encodes a tRNA of the same isotype as the disrupted but essential host tRNA, complementing its loss, and consequently is required for the survival of lysogenic progeny. As expected, an integrase-defective phage mutant forms turbid plaques, and bacterial progeny are immune to superinfection, but they lack stability, and the prophage is rapidly lost. In contrast, a tRNA-defective phage mutant forms clear plaques and more closely resembles a repressor mutant, and lysogens are recovered only at very low frequency through the use of secondary attachment sites elsewhere in the host genome. Integration-proficient plasmids derived from these phages must also carry a cognate phage tRNA gene for efficient integration, and these may be useful tools for mycobacterial genetics. We show that tRNA-dependent lysogeny is used by phages within multiple different groups of related viruses and may be prevalent elsewhere in the broader phage community.IMPORTANCEBacteriophages are the most numerous biological entities in the biosphere, and a substantial proportion of phages are temperate, forming stable lysogens in which a prophage copy of the genome integrates into the bacterial chromosome. Many phages encode a variety of tRNA genes whose roles are poorly understood, although it has been proposed that they enhance translational efficiencies in lytic growth or that they counteract host defenses that degrade host tRNAs. Here, we show that phage-encoded tRNAs play key roles in the establishment of lysogeny of some temperate phages. They do so by compensating for the loss of tRNA function when phages integrate at an attB site overlapping a tRNA gene but fail to reconstruct the tRNA at the attachment junction. In this system of tRNA-dependent lysogeny, the phage-encoded tRNA is required for lysogeny, and deletion of the phage tRNA gives rise to a clear plaque phenotype and obligate lytic growth.

Project description:Bacillus pumilus plays an important role in industrial application and biocontrol activities, as well as causing humans and plants disease, leading to economic losses and biosafety concerns. However, until now, the pathogenesis and underlying mechanisms of B. pumilus strains remain unclear. In our previous study, one representative isolate of B. pumilus named HM-7 has been recovered and proved to be the causal agent of fruit rot on muskmelon (Cucumis melo). Herein, we present a complete and annotated genome sequence of HM-7 that contains 4,111 coding genes in a single 3,951,520 bp chromosome with 41.04% GC content. A total of 3,481 genes were functionally annotated with the GO, COG, and KEGG databases. Pan-core genome analysis of HM-7 and 20 representative B. pumilus strains, as well as six closely related Bacillus species, discovered 740 core genes and 15,205 genes in the pan-genome of 21 B. pumilus strains, in which 485 specific-genes were identified in HM-7 genome. The average nucleotide identity (ANI), and whole-genome-based phylogenetic analysis revealed that HM-7 was most closely related to the C4, GR8, MTCC-B6033, TUAT1 and SH-B11 strains, but evolutionarily distinct from other strains in B. pumilus. Collinearity analysis of the six similar B. pumilus strains showed high levels of synteny but also several divergent regions for each strains. In the HM-7 genome, we identified 484 genes in the carbohydrate-active enzymes (CAZyme) class, 650 genes encoding virulence factors, and 1,115 genes associated with pathogen-host interactions. Moreover, three HM-7-specific regions were determined, which contained 424 protein-coding genes. Further investigation of these genes showed that 19 pathogenesis-related genes were mainly associated with flagella formation and secretion of toxic products, which might be involved in the virulence of strain HM-7. Our results provided detailed genomic and taxonomic information for the HM-7 strain, and discovered its potential pathogenic mechanism, which lay a foundation for developing effective prevention and control strategies against this pathogen in the future.

Dataset Information

Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis.

Publications

Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis.

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