Comparative Analysis of Two Phenotypically-similar but Genomically-distinct Burkholderia Cenocepacia-specific Bacteriophages

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2012 Jun 9

PMID 22676492

Citations 27

Authors

Karlene H Lynch

Paul Stothard

Jonathan J Dennis

Affiliations

Soon will be listed here.

Abstract

Background: Genomic analysis of bacteriophages infecting the Burkholderia cepacia complex (BCC) is an important preliminary step in the development of a phage therapy protocol for these opportunistic pathogens. The objective of this study was to characterize KL1 (vB_BceS_KL1) and AH2 (vB_BceS_AH2), two novel Burkholderia cenocepacia-specific siphoviruses isolated from environmental samples.

Results: KL1 and AH2 exhibit several unique phenotypic similarities: they infect the same B. cenocepacia strains, they require prolonged incubation at 30°C for the formation of plaques at low titres, and they do not form plaques at similar titres following incubation at 37°C. However, despite these similarities, we have determined using whole-genome pyrosequencing that these phages show minimal relatedness to one another. The KL1 genome is 42,832 base pairs (bp) in length and is most closely related to Pseudomonas phage 73 (PA73). In contrast, the AH2 genome is 58,065 bp in length and is most closely related to Burkholderia phage BcepNazgul. Using both BLASTP and HHpred analysis, we have identified and analyzed the putative virion morphogenesis, lysis, DNA binding, and MazG proteins of these two phages. Notably, MazG homologs identified in cyanophages have been predicted to facilitate infection of stationary phase cells and may contribute to the unique plaque phenotype of KL1 and AH2.

Conclusions: The nearly indistinguishable phenotypes but distinct genomes of KL1 and AH2 provide further evidence of both vast diversity and convergent evolution in the BCC-specific phage population.

Citing Articles

Phage therapy to treat cystic fibrosis complex lung infections: perspectives and challenges.

Canning J, Laucirica D, Ling K, Nicol M, Stick S, Kicic A Front Microbiol. 2024; 15:1476041.

PMID: 39493847 PMC: 11527634. DOI: 10.3389/fmicb.2024.1476041.

Prophylactic phage biocontrol prevents infection in a quantitative model of bacterial virulence.

Lauman P, Dennis J Appl Environ Microbiol. 2024; 90(10):e0131724.

PMID: 39240081 PMC: 11497830. DOI: 10.1128/aem.01317-24.

The dataset on the draft whole-genome sequences of two strains isolated from urine samples of patients with urinary tract diseases.

Valeeva L, Pudova D, Khabipova N, Shigapova L, Shagimardanova E, Rogov A Data Brief. 2023; 51:109704.

PMID: 37965601 PMC: 10641123. DOI: 10.1016/j.dib.2023.109704.

Metagenomic comparisons reveal a highly diverse and unique viral community in a seasonally fluctuating hypersaline microbial mat.

Cisneros-Martinez A, Eguiarte L, Souza V Microb Genom. 2023; 9(7).

PMID: 37459167 PMC: 10438804. DOI: 10.1099/mgen.0.001063.

Synergistic Interactions among Complex-Targeting Phages Reveal a Novel Therapeutic Role for Lysogenization-Capable Phages.

Lauman P, Dennis J Microbiol Spectr. 2023; 11(3):e0443022.

PMID: 37195168 PMC: 10269493. DOI: 10.1128/spectrum.04430-22.

References

Weigele P, Pope W, Pedulla M, Houtz J, Smith A, Conway J . Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol. 2007; 9(7):1675-95. DOI: 10.1111/j.1462-2920.2007.01285.x. View

Young I, Wang I, Roof W . Phages will out: strategies of host cell lysis. Trends Microbiol. 2000; 8(3):120-8. DOI: 10.1016/s0966-842x(00)01705-4. View

Sullivan M, Huang K, Ignacio-Espinoza J, Berlin A, Kelly L, Weigele P . Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol. 2010; 12(11):3035-56. PMC: 3037559. DOI: 10.1111/j.1462-2920.2010.02280.x. View

Delcher A, Phillippy A, Carlton J, Salzberg S . Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 2002; 30(11):2478-83. PMC: 117189. DOI: 10.1093/nar/30.11.2478. View

Langley R, Kenna D, Vandamme P, Ure R, Govan J . Lysogeny and bacteriophage host range within the Burkholderia cepacia complex. J Med Microbiol. 2003; 52(Pt 6):483-490. DOI: 10.1099/jmm.0.05099-0. View

Bull J, Badgett M, Wichman H, Huelsenbeck J, Hillis D, Gulati A . Exceptional convergent evolution in a virus. Genetics. 1997; 147(4):1497-507. PMC: 1208326. DOI: 10.1093/genetics/147.4.1497. View

Juncker A, Willenbrock H, von Heijne G, Brunak S, Nielsen H, Krogh A . Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003; 12(8):1652-62. PMC: 2323952. DOI: 10.1110/ps.0303703. View

Summer E, Gonzalez C, Bomer M, Carlile T, Embry A, Kucherka A . Divergence and mosaicism among virulent soil phages of the Burkholderia cepacia complex. J Bacteriol. 2005; 188(1):255-68. PMC: 1317576. DOI: 10.1128/JB.188.1.255-268.2006. View

Silva A, Benitez J . A Vibrio cholerae relaxed (relA) mutant expresses major virulence factors, exhibits biofilm formation and motility, and colonizes the suckling mouse intestine. J Bacteriol. 2005; 188(2):794-800. PMC: 1347285. DOI: 10.1128/JB.188.2.794-800.2006. View

10.

Taylor C, Beresford M, Epton H, Sigee D, Shama G, Andrew P . Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol. 2002; 184(3):621-8. PMC: 139534. DOI: 10.1128/JB.184.3.621-628.2002. View

11.

Moon S, Byun Y, Kim H, Jeong S, Han K . Predicting genes expressed via -1 and +1 frameshifts. Nucleic Acids Res. 2004; 32(16):4884-92. PMC: 519117. DOI: 10.1093/nar/gkh829. View

12.

Haralalka S, Nandi S, Bhadra R . Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J Bacteriol. 2003; 185(16):4672-82. PMC: 166452. DOI: 10.1128/JB.185.16.4672-4682.2003. View

13.

Hennecke F, Kolmar H, Brundl K, Fritz H . The vsr gene product of E. coli K-12 is a strand- and sequence-specific DNA mismatch endonuclease. Nature. 1991; 353(6346):776-8. DOI: 10.1038/353776a0. View

14.

Carvalho C, Gannon B, Halfhide D, Santos S, Hayes C, Roe J . The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol. 2010; 10:232. PMC: 2940857. DOI: 10.1186/1471-2180-10-232. View

15.

Hammer B, Swanson M . Co-ordination of legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol. 1999; 33(4):721-31. DOI: 10.1046/j.1365-2958.1999.01519.x. View

16.

Golshahi L, Lynch K, Dennis J, Finlay W . In vitro lung delivery of bacteriophages KS4-M and ΦKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J Appl Microbiol. 2010; 110(1):106-17. DOI: 10.1111/j.1365-2672.2010.04863.x. View

17.

Soding J, Biegert A, Lupas A . The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005; 33(Web Server issue):W244-8. PMC: 1160169. DOI: 10.1093/nar/gki408. View

18.

Oliveira A, Sereno R, Azeredo J . In vivo efficiency evaluation of a phage cocktail in controlling severe colibacillosis in confined conditions and experimental poultry houses. Vet Microbiol. 2010; 146(3-4):303-8. DOI: 10.1016/j.vetmic.2010.05.015. View

19.

Marchler-Bauer A, Bryant S . CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004; 32(Web Server issue):W327-31. PMC: 441592. DOI: 10.1093/nar/gkh454. View

20.

Xu J, Hendrix R, Duda R . Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell. 2004; 16(1):11-21. DOI: 10.1016/j.molcel.2004.09.006. View