Role of the pre-neck appendage protein (Dpo7) from phage vB_SepiS-phiIPLA7 as an anti-biofilm agent in staphylococcal species

Frontiers in Microbiology

Volumn 6, Issue NOV, 2015, Pages

  Gutiérrez, Diana ^a   Briers, Yves ^b,c   Rodríguez Rubio, Lorena ^a,b   Martínez, Beatriz ^a   Rodríguez, Ana ^a   Lavigne, Rob ^b   García, Pilar ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Biofilm; Biofilm matrix; Exopolysaccharide depolymerase; S. aureus; S. epidermidis

Indexed keywords

EXOPOLYSACCHARIDE; EXOPOLYSACCHARIDE DEPOLYMERASE; POLYSTYRENE; PRE NECK APPENDAGE PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPHAGE; BIOFILM; CLONING; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENETIC ANALYSIS; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84949749871     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01315     Document Type: Article

References (64)

1. Alkawash, M. A., Soothill, J. S., and Schiller, N. L. (2006). Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114, 131-138. doi: 10.1111/j.1600-0463.2006.apm_356.x
2. Allen, R. C., Popat, R., Diggle, S. P., and Brown, S. P. (2014). Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. 12, 300-308. doi: 10.1038/nrmicro3232
3. Andres, D., Hanke, C., Baxa, U., Seul, A., Barbirz, S., and Seckler, R. (2010). Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J. Biol. Chem. 285, 36768-36775. doi: 10.1074/jbc. M110.169003
4. Becker, S. C., Dong, S., Baker, J. R., Foster-Frey, J., Pritchard, D. G., and Donovan, D. M. (2009). LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells. FEMS Microbiol. Lett. 294, 52-60. doi: 10.1111/j.1574-6968.2009.01541.x
5. Cerca, N., Oliveira, R., and Azeredo, J. (2007). Susceptibility of Staphylococcus epidermidis planktonic cells and biofilms to the lytic action of Staphylococcus bacteriophage K. Lett. Appl. Microbiol. 45, 313-317. doi: 10.1111/j.1472-765X.2007.02190.x
6. Chaignon, P., Sadovskaya, I., Ragunah, C., Ramasubbu, N., Kaplan, J. B., and Jabbouri, S. (2007). Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl. Microbiol. Biotechnol. 75, 125-132. doi: 10.1007/s00253-006-0790-y
7. Christner, M., Franke, G. C., Schommer, N. N., Wendt, U., Wegert, K., Pehle, P., et al. (2010). The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol. Microbiol. 75, 187-207. doi: 10.1111/j.1365-2958.2009.06981.x
8. Cornelissen, A., Ceyssens, P. J., Krylov, V. N., Noben, J. P., Volckaert, G., and Lavigne, R. (2012). Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology 434, 251-256. doi: 10.1016/j.virol.2012.09.030
9. Cornelissen, A., Ceyssens, P. J., T'Syen, J., Van Praet, H., Noben, J. P., Shaburova, O. V., et al. (2011). The T7-related Pseudomonas putida phage phi15 displays virion-associated biofilm degradation properties. PLoS ONE 6:e18597. doi: 10.1371/journal.pone.0018597
10. Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I., and Penadés, J. R. (2001). Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183, 2888-2896. doi: 10.1128/JB.183.9.2888-2896.2001
11. Daniel, A., Bonnen, P. E., and Fischetti, V. A. (2007). First complete genome sequence of two Staphylococcus epidermidis bacteriophages. J. Bacteriol. 189, 2086-2100. doi: 10.1128/JB.01637-06
12. Darouiche, R. O., Mansouri, M. D., Gawande, P. V., and Madhyastha, S. (2009). Antimicrobial and antibiofilm efficacy of triclosan and DispersinB combination. J. Antimicrob. Chemother. 64, 88-93. doi: 10.1093/jac/dkp158
13. David, M. Z., and Daum, R. S. (2010). Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 23, 616-687. doi: 10.1128/CMR.00081-09
14. Delgado, S., Arroyo, R., Jiménez, E., Maín, M. L., del Campo, R., Fernández, L., et al. (2009). Staphylococcus epidermidis strains isolated from breast milk of women suffering infectious mastitis: potential virulence traits and resistance to antibiotics. BMC Microbiol. 9:82. doi: 10.1186/1471-2180-9-82
15. Domenech, M., García, E., and Moscoso, M. (2011). In vitro destruction of Streptococcus pneumoniae biofilms with bacterial and phage peptidoglycan hydrolases. Antimicrob. Agents Chemother. 55, 4144-4148. doi: 10.1128/AAC.00492-11
16. Donelli, G., Francolini, I., Romoli, D., Guaglianone, E., Piozzi, A., Ragunath, C., et al. (2007). Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrob. Agents Chemother. 51, 2733-2740. doi: 10.1128/AAC.01249-06
17. Farber, B. F., Kaplan, M. H., and Clogston, A. G. (1990). Staphylococcus epidermidis extracted slime inhibits the antimicrobial action of glycopeptide antibiotics. J. Infect. Dis. 161, 37-40. doi: 10.1093/infdis/161.1.37
18. Fazekas, E., Kandra, L., and Gyemant, G. (2012). Model for beta-1,6-N-acetylglucosamine oligomer hydrolysis catalysed by DispersinB, a biofilm degrading enzyme. Carbohydr. Res. 363, 7-13. doi: 10.1016/j.carres.2012.09.016
19. García, P., Rodriguez, I., and Suárez, J. E. (2004). A-1 ribosomal frameshift in the transcript that encodes the major head protein of bacteriophage A2 mediates biosynthesis of a second essential component of the capsid. J. Bacteriol. 186, 1714-1719. doi: 10.1128/JB.186.6.1714-1719.2004
20. Gawande, P. V., Leung, K. P., and Madhyastha, S. (2014). Antibiofilm and antimicrobial efficacy of DispersinB(R)-KSL-W peptide-based wound gel against chronic wound infection associated bacteria. Curr. Microbiol. 68, 635-641. doi: 10.1007/s00284-014-0519-6
21. Glonti, T., Chanishvili, N., and Taylor, P. W. (2010). Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J. Appl. Microbiol. 108, 695-702. doi: 10.1111/j.1365-2672.2009.04469.x
22. Gutiérrez, D., Martínez, B., Rodríguez, A., and García, P. (2010). Isolation and characterization of bacteriophages infecting Staphylococcus epidermidis. Curr. Microbiol. 61, 601-608. doi: 10.1007/s00284-010-9659-5
23. Gutiérrez, D., Martínez, B., Rodríguez, A., and García, P. (2012). Genomic characterization of two Staphylococcus epidermidis bacteriophages with anti-biofilm potential. BMC Genomics 13:228. doi: 10.1186/1471-2164-13-228
24. Gutiérrez, D., Ruas-Madiedo, P., Martínez, B., Rodríguez, A., and García, P. (2014). Effective removal of staphylococcal biofilms by the endolysin LysH5. PLoS ONE 9:e107307. doi: 10.1371/journal.pone.0107307
25. Gutiérrez, D., Vandenheuvel, D., Martínez, B., Rodríguez, A., Lavigne, R., and García, P. (2015). Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono-and dual-species Staphylococcal biofilms. Appl. Environ. Microbiol. 81, 3336-3348. doi: 10.1128/AEM.03560-14
26. Hall-Stoodley, L., and Stoodley, P. (2009). Evolving concepts in biofilm infections. Cell Microbiol. 11, 1034-1043. doi: 10.1111/j.1462-5822.2009.01323.x
27. Holland, L. M., Conlon, B., and O'gara, J. P. (2011). Mutation of tagO reveals an essential role for wall teichoic acids in Staphylococcus epidermidis biofilm development. Microbiology 157, 408-418. doi: 10.1099/mic.0.042234-0
28. Hussain, M., Heilmann, C., Peters, G., and Herrmann, M. (2001). Teichoic acid enhances adhesion of Staphylococcus epidermidis to immobilized fibronectin. Microb. Pathog. 31, 261-270. doi: 10.1006/mpat.2001.0469
29. Hussain, M., Herrmann, M., von Eiff, C., Perdreau-Remington, F., and Peters, G. (1997). A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces. Infect. Immun. 65, 519-524.
30. Iorio, N. L., Caboclo, R. F., Azevedo, M. B., Barcellos, A. G., Neves, F. P., Domingues, R. M., et al. (2012). Characteristics related to antimicrobial resistance and biofilm formation of widespread methicillin-resistant Staphylococcus epidermidis ST2 and ST23 lineages in Rio de Janeiro hospitals, Brazil. Diagn. Microbiol. Infect. Dis. 72, 32-40. doi: 10.1016/j.diagmicrobio.2011.09.017
31. Itoh, Y., Wang, X., Hinnebusch, B. J., Preston, J. F. III, and Romeo, T. (2005). Depolymerization of beta-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J. Bacteriol. 187, 382-387. doi: 10.1128/JB.187.1.382-387.2005
32. Izano, E. A., Amarante, M. A., Kher, W. B., and Kaplan, J. B. (2008). Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl. Environ. Microbiol. 74, 470-476. doi: 10.1128/AEM.02073-07
33. Jakobsson, E., Jokilammi, A., Aalto, J., Ollikka, P., Lehtonen, J. V., Hirvonen, H., et al. (2007). Identification of amino acid residues at the active site of endosialidase that dissociate the polysialic acid binding and cleaving activities in Escherichia coli K1 bacteriophages. Biochem. J. 405, 465-472. doi: 10.1042/BJ20070177
34. Kaplan, J. B., Ragunath, C., Ramasubbu, N., and Fine, D. H. (2003). Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J. Bacteriol. 185, 4693-4698. doi: 10.1128/JB.185.4.1399-1404.2003
35. Kaplan, J. B., Ragunath, C., Velliyagounder, K., Fine, D. H., and Ramasubbu, N. (2004). Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 48, 2633-2636. doi: 10.1128/AAC.48.7.2633-2636.2004
36. Kim, W. S., Salm, H., and Geider, K. (2004). Expression of bacteriophage phiEa1h lysozyme in Escherichia coli and its activity in growth inhibition of Erwinia amylovora. Microbiology 150, 2707-2714. doi: 10.1099/mic.0.27224-0
37. Kropec, A., Maira-Litran, T., Jefferson, K. K., Grout, M., Cramton, S. E., Gotz, F., et al. (2005). Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect. Immun. 73, 6868-6876. doi: 10.1128/IAI.73.10.6868-6876.2005
38. Lowy, F. D. (1998). Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532. doi: 10.1056/NEJM199808203390806
39. Lu, T. K., and Collins, J. J. (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. U.S.A. 104, 11197-11202. doi: 10.1073/pnas.0704624104
40. Ma, Y., Chen, M., Jones, J. E., Ritts, A. C., Yu, Q., and Sun, H. (2012). Inhibition of Staphylococcus epidermidis biofilm by trimethylsilane plasma coating. Antimicrob. Agents Chemother. 56, 5923-5937. doi: 10.1128/AAC.01739-12
41. Mack, D., Fischer, W., Krokotsch, A., Leopold, K., Hartmann, R., Egge, H., et al. (1996). The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178, 175-183.
42. Mann, E. E., Rice, K. C., Boles, B. R., Endres, J. L., Ranjit, D., Chandramohan, L., et al. (2009). Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4:e5822. doi: 10.1371/journal.pone.0005822
43. Muller, J. J., Barbirz, S., Heinle, K., Freiberg, A., Seckler, R., and Heinemann, U. (2008). An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri Phage Sf6. Structure 16, 766-775. doi: 10.1016/j.str.2008.01.019
44. Mushtaq, N., Redpath, M. B., Luzio, J. P., and Taylor, P. W. (2005). Treatment of experimental Escherichia coli infection with recombinant bacteriophage-derived capsule depolymerase. J. Antimicrob Chemother. 56, 160-165. doi: 10.1093/jac/dki177
45. Nostro, A., Scaffaro, R., D'Arrigo, M., Botta, L., Filocamo, A., Marino, A., et al. (2013). Development and characterization of essential oil component-based polymer films: a potential approach to reduce bacterial biofilm. Appl. Microbiol. Biotechnol. 97, 9515-9523. doi: 10.1007/s00253-013-5196-z
46. Nostro, A., Scaffaro, R., Ginestra, G., D'Arrigo, M., Botta, L., Marino, A., et al. (2010). Control of biofilm formation by poly-ethylene-co-vinyl acetate films incorporating nisin. Appl. Microbiol. Biotechnol. 87, 729-737. doi: 10.1007/s00253-010-2598-z
47. Obeso, J. M., Martínez, B., Rodríguez, A., and García, P. (2008). Lytic activity of the recombinant staphylococcal bacteriophage PhiH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128, 212-218. doi: 10.1016/j.ijfoodmicro.2008.08.010
48. O'Neill, E., Pozzi, C., Houston, P., Humphreys, H., Robinson, D. A., Loughman, A., et al. (2008). A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol. 190, 3835-3850. doi: 10.1128/JB.00167-08
49. Otto, M. (2013). Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: Staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. Bioessays 35, 4-11. doi: 10.1002/bies.201200112
50. Patti, J. M., Allen, B. L., McGavin, M. J., and Hook, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617. doi: 10.1146/annurev.mi.48.100194.003101
51. Price, L. B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P. S., et al. (2012). Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 3:e00520-12. doi: 10.1128/mBio.00305-11
52. Rogers, K. L., Fey, P. D., and Rupp, M. E. (2009). Coagulase-negative staphylococcal infections. Infect. Dis. Clin. North Am. 23, 73-98. doi: 10.1016/j.idc.2008.10.001
53. Rupp, M. E. (2014). Clinical characteristics of infections in humans due to Staphylococcus epidermidis. Methods Mol. Biol. 1106, 1-16. doi: 10.1007/978-1-62703-736-5_1
54. Saising, J., Dube, L., Ziebandt, A. K., Voravuthikunchai, S. P., Nega, M., and Gotz, F. (2012). Activity of gallidermin on Staphylococcus aureus and Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 56, 5804-5810. doi: 10.1128/AAC.01296-12
55. Shen, Y., Koller, T., Kreikemeyer, B., and Nelson, D. C. (2013). Rapid degradation of Streptococcus pyogenes biofilms by PlyC, a bacteriophage-encoded endolysin. J. Antimicrob. Chemother. 68, 1818-1824. doi: 10.1093/jac/dkt104
56. Shiro, H., Muller, E., Gutiérrez, N., Boisot, S., Grout, M., Tosteson, T. D., et al. (1994). Transposon mutants of Staphylococcus epidermidis deficient in elaboration of capsular polysaccharide/adhesin and slime are avirulent in a rabbit model of endocarditis. J. Infect. Dis. 169, 1042-1049. doi: 10.1093/infdis/169.5.1042
57. Smith, N. L., Taylor, E. J., Lindsay, A. M., Charnock, S. J., Turkenburg, J. P., Dodson, E. J., et al. (2005). Structure of a group A streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded beta-helix. Proc. Natl. Acad. Sci. U.S.A. 102, 17652-17657. doi: 10.1073/pnas.0504782102
58. Sugimoto, S., Iwamoto, T., Takada, K., Okuda, K., Tajima, A., Iwase, T., et al. (2013). Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J. Bacteriol. 195, 1645-1655. doi: 10.1128/JB.01672-12
59. Tang, H., Cao, T., Liang, X., Wang, A., Salley, S. O., McAllister, J. II, et al. (2009). Influence of silicone surface roughness and hydrophobicity on adhesion and colonization of Staphylococcus epidermidis. J. Biomed. Mater. Res. A 88, 454-463. doi: 10.1002/jbm.a.31788
60. Turk, R., Singh, A., Rousseau, J., and Weese, J. S. (2013). In vitro evaluation of DispersinB on methicillin-resistant Staphylococcus pseudintermedius biofilm. Vet. Microbiol. 166, 576-579. doi: 10.1016/j.vetmic.2013.07.011
61. Valle, J., Toledo-Arana, A., Berasain, C., Ghigo, J. M., Amorena, B., Penadés, J. R., et al. (2003). SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48, 1075-1087. doi: 10.1046/j.1365-2958.2003.03493.x
62. Vergara-Irigaray, M., Maira-Litran, T., Merino, N., Pier, G. B., Penadés, J. R., and Lasa, I. (2008). Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology 154, 865-877. doi: 10.1099/mic.0.2007/013292-0
63. Yan, J., Mao, J., and Xie, J. (2014). Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 28, 265-274. doi: 10.1007/s40259-013-0081-y
64. Zhang, Y. Q., Ren, S. X., Li, H. L., Wang, Y. X., Fu, G., Yang, J., et al. (2003). Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49, 1577-1593. doi: 10.1046/j.1365-2958.2003.03671.x