Burkholderia cenocepacia Prophages—Prevalence, Chromosome Location and Major Genes Involved

Roszniowski, Bartosz; McClean, Siobhán; Drulis-Kawa, Zuzanna

doi:10.3390/v10060297

Cited by 18 publications

(24 citation statements)

References 69 publications

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“…These data corroborate our findings, whereby 35 % of the prophages under study were integrated close to host tRNA, specifically tRNA-ARG, which coincides with the findings of Roszniowski et al . for a Burkholderia cenocepacia prophage sequence [ 58 ]. Additionally, the subsequent integration sites that we identified are also consistent with those most frequently observed by these researchers (ABC transporter genes and transcriptional regulators) [ 58 ].…”

Section: Discussionmentioning

confidence: 99%

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Genomic analysis of 40 prophages located in the genomes of 16 carbapenemase-producing clinical strains of Klebsiella pneumoniae

et al. 2020

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Klebsiella pneumoniae is the clinically most important species within the genus Klebsiella and, as a result of the continuous emergence of multi-drug resistant (MDR) strains, the cause of severe nosocomial infections. The decline in the effectiveness of antibiotic treatments for infections caused by MDR bacteria has generated particular interest in the study of bacteriophages. In this study, we characterized a total of 40 temperate bacteriophages (prophages) with a genome range of 11.454–84.199 kb, predicted from 16 carbapenemase-producing clinical strains of K. pneumoniae belonging to different sequence types, previously identified by multilocus sequence typing. These prophages were grouped into the three families in the order Caudovirales (27 prophages belonging to the family Myoviridae , 10 prophages belonging to the family Siphoviridae and 3 prophages belonging to the family Podoviridae ). Genomic comparison of the 40 prophage genomes led to the identification of four prophages isolated from different strains and of genome sizes of around 33.3, 36.1, 39.6 and 42.6 kb. These prophages showed sequence similarities (query cover >90 %, identity >99.9 %) with international Microbe Versus Phage (MVP) ( http://mvp.medgenius.info/home ) clusters 4762, 4901, 3499 and 4280, respectively. Phylogenetic analysis revealed the evolutionary proximity among the members of the four groups of the most frequently identified prophages in the bacterial genomes studied (33.3, 36.1, 39.6 and 42.6 kb), with bootstrap values of 100 %. This allowed the prophages to be classified into three clusters: A, B and C. Interestingly, these temperate bacteriophages did not infect the highest number of strains as indicated by a host-range assay, these results could be explained by the development of superinfection exclusion mechanisms. In addition, bioinformatic analysis of the 40 identified prophages revealed the presence of 2363 proteins. In total, 59.7 % of the proteins identified had a predicted function, mainly involving viral structure, transcription, replication and regulation (lysogenic/lysis). Interestingly, some proteins had putative functions associated with bacterial virulence (toxin expression and efflux pump regulators), phage defence profiles such as toxin–antitoxin modules, an anti-CRISPR/Cas9 protein, TerB protein (from ter ZABCDE operon) and methyltransferase proteins.

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Section: Discussionmentioning

confidence: 99%

“…for a Burkholderia cenocepacia prophage sequence [ 58 ]. Additionally, the subsequent integration sites that we identified are also consistent with those most frequently observed by these researchers (ABC transporter genes and transcriptional regulators) [ 58 ].…”

Section: Discussionmentioning

confidence: 99%

Genomic analysis of 40 prophages located in the genomes of 16 carbapenemase-producing clinical strains of Klebsiella pneumoniae

et al. 2020

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“…Prophage detection in bacterial genomes remains challenging and the limitations of using only PHASTER for prophage identification are acknowledged [76]. However, PHASTER is an excellent screening tool for examining large numbers of genomes and was applied herein to putatively predict prophage carriage across 81 B. vietnamiensis strains, the largest collection of a Burkholderia species investigated to date for prophages.…”

Section: Discussionmentioning

confidence: 99%

“…This is lower than the percentages found in other bacterial genera (Escherichia, Streptococcus, Borrelia; 10%-20%) [3,83], but close to others (Salmonella; 4.9%) [83], and similar to other Burkholderia and closely related Paraburkholderia. Prophage material was found to comprise up to 3.67% of B. cenocepacia genomes (16 strains) [76], up to 2.34% in B. pseudomallei (6 strains), 2.00% in B. thailandensis (1 strain), 0.55% in Paraburkholderia xenovorans (1 strain), up to 4.98% in B. multivorans (3 strains) [61] and up to 4% in Paraburkholderia genomes (36 strains) [79], although certain Paraburkholderia strains can carry up to >10% of their genome as prophage material [67].…”

Section: Discussionmentioning

confidence: 99%

“…A recent publication actually identified a similarity between a 13 kb portion of Ralstonia phage RS138 and B. vietnamiensis G4 chromosome 1 [ 74 ] which is likely to be related to G4P1, and the gene content and organisation of G4P1 is highly similar to Mannheima and Haemophilus Mu-like phages [ 60 ]. Whilst the phages of B. cenocepacia have been found to encode putative virulence factors, and transduction of antibiotic resistance genes by Burkholderia phages has been observed, the overall contributions of phages to virulence and fitness of Burkholderia remains largely unknown [ 28 , 75 , 76 ]. Similarly, the G4P1 prophage does not appear to encode any virulence or antibiotic resistance determinants but has a large number of hypothetical proteins ( n = 21) of unknown function.…”

Section: Discussionmentioning

confidence: 99%

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A Novel Inducible Prophage from Burkholderia vietnamiensis G4 Is Widely Distributed across the Species and Has Lytic Activity against Pathogenic Burkholderia

Weiser

Yap

Otter

et al. 2020

Viruses

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Burkholderia species have environmental, industrial and medical significance, and are important opportunistic pathogens in individuals with cystic fibrosis (CF). Using a combination of existing and newly determined genome sequences, this study investigated prophage carriage across the species B. vietnamiensis, and also isolated spontaneously inducible prophages from a reference strain, G4. Eighty-one B. vietnamiensis genomes were bioinformatically screened for prophages using PHASTER (Phage Search Tool Enhanced Release) and prophage regions were found to comprise up to 3.4% of total genetic material. Overall, 115 intact prophages were identified and there was evidence of polylysogeny in 32 strains. A novel, inducible Mu-like phage (vB_BvM-G4P1) was isolated from B. vietnamiensis G4 that had lytic activity against strains of five Burkholderia species prevalent in CF infections, including the Boston epidemic B. dolosa strain SLC6. The cognate prophage to vB_BvM-G4P1 was identified in the lysogen genome and was almost identical (>93.5% tblastx identity) to prophages found in 13 other B. vietnamiensis strains (17% of the strain collection). Phylogenomic analysis determined that the G4P1-like prophages were widely distributed across the population structure of B. vietnamiensis. This study highlights how genomic characterization of Burkholderia prophages can lead to the discovery of novel bacteriophages with potential therapeutic or biotechnological applications.

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Protein with negative surface charge distribution, Bnr1, shows characteristics of a DNA‐mimic protein and may be involved in the adaptation of Burkholderia cenocepacia

Dennehy¹,

Duggan

Dignam³

et al. 2022

MicrobiologyOpen

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Adaptation of opportunistic pathogens to their host environment requires reprogramming of a vast array of genes to facilitate survival in the host. Burkholderia cenocepacia, a Gram‐negative bacterium with a large genome of ∼8 Mb that colonizes environmental niches, is exquisitely adaptable to the hypoxic environment of the cystic fibrosis lung and survives in macrophages. We previously identified an immunoreactive acidic protein encoded on replicon 3, BCAS0292. Deletion of the BCAS0292 gene significantly altered the abundance of 979 proteins by 1.5‐fold or more; 19 proteins became undetectable while 545 proteins showed ≥1.5‐fold reduced abundance, suggesting the BCAS0292 protein is a global regulator. Moreover, the ∆BCAS0292 mutant showed a range of pleiotropic effects: virulence and host‐cell attachment were reduced, antibiotic susceptibility was altered, and biofilm formation enhanced. Its growth and survival were impaired in 6% oxygen. In silico prediction of its three‐dimensional structure revealed BCAS0292 presents a dimeric β‐structure with a negative surface charge. The ΔBCAS0292 mutant displayed altered DNA supercoiling, implicated in global regulation of gene expression. Three proteins were identified in pull‐downs with FLAG‐tagged BCAS0292, including the Histone H1‐like protein, HctB, which is recognized as a global transcriptional regulator. We propose that BCAS0292 protein, which we have named Burkholderia negatively surface‐charged regulatory protein 1 (Bnr1), acts as a DNA‐mimic and binds to DNA‐binding proteins, altering DNA topology and regulating the expression of multiple genes, thereby enabling the adaptation of B. cenocepacia to highly diverse environments.

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Burkholderia cenocepacia Prophages—Prevalence, Chromosome Location and Major Genes Involved

Cited by 18 publications

References 69 publications

Genomic analysis of 40 prophages located in the genomes of 16 carbapenemase-producing clinical strains of Klebsiella pneumoniae

Genomic analysis of 40 prophages located in the genomes of 16 carbapenemase-producing clinical strains of Klebsiella pneumoniae

A Novel Inducible Prophage from Burkholderia vietnamiensis G4 Is Widely Distributed across the Species and Has Lytic Activity against Pathogenic Burkholderia

Protein with negative surface charge distribution, Bnr1, shows characteristics of a DNA‐mimic protein and may be involved in the adaptation of Burkholderia cenocepacia

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