Elucidating the genetic basis of crystalline biofilm formation in Proteus mirabilis

Infection and Immunity

Volumn 82, Issue 4, 2014, Pages 1616-1626

  Holling, N ^a   Lednor, D ^b   Tsang, S ^b   Bissell, A ^b   Campbell, L ^b   Nzakizwanayo, J ^a   Dedi, C ^a   Hawthorne, J A ^a   Hanlon, G ^a   Ogilvie, L A ^a   Salvage, J P ^a   Patel, B A ^a   Barnes, L M ^a   Jones, B V ^a,c  

^a UNIVERSITY OF BRIGHTON   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c QUEEN VICTORIA HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; CEFALEXIN; CHLORAMPHENICOL; CIPROFLOXACIN; FOSFOMYCIN; GENTAMICIN; MECILLINAM; NALIDIXIC ACID; NITROFURANTOIN; NORFLOXACIN; PENICILLIN G; SILICONE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENETICS; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BIOFILM; BIOMASS; BLADDER CATHETERIZATION; CONTROLLED STUDY; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; MICTURITION; MUTAGENESIS; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEUS MIRABILIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSPOSON; URETHRAL CATHETER; URINE PH;

ANALYSIS OF VARIANCE; ANTI-BACTERIAL AGENTS; BIOFILMS; CALCIUM; CATHETERS, INDWELLING; CELL MOVEMENT; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION PROFILING; HUMANS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTROCHEMICAL, SCANNING; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEUS MIRABILIS; SEQUENCE ANALYSIS, DNA; UREASE; URINARY CATHETERIZATION;

EID: 84896470747     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01652-13     Document Type: Article

References (56)

1. Darouiche RO. 2001. Device-associated infections: a macroproblem that starts with microadherence. Clin. Infect. Dis. 33:1567-1572. http://dx.doi.org/10.1086/323130.
2. Saint S, Wiese J, Amory J, Bernstein ML, Patel UD, Zemencuk JK, Bernstein SJ, Lipsky BA, Hofer TP. 2000. Are physicians aware of which of their patients have indwelling urinary catheters? Am. J. Med. 109:476-480. http://dx.doi.org/10.1016/S0002-9343(00)00531-3.
3. Getliffe K, Newton T. 2006. Catheter-associated urinary tract infection in primary and community health care. Age Ageing 35:477-481. http://dx.doi.org/10.1093/ageing/afl052.
4. Stickler DJ, Zimakoff J. 1994. Complications of urinary-tract infections associated with devices used for long-term bladder management. J. Hosp. Infect. 28:177-194. http://dx.doi.org/10.1016/0195-6701(94)90101-5.
5. Jacobsen SM, Stickler DJ, Mobley HL, Shirtliff ME. 2008. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21:26-59. http://dx.doi.org/10.1128/CMR.00019-07.
6. McNulty C, Freeman E, Smith G, Gunn K, Foy C, Tompkins D, Brady A, Cartwright K. 2003. Prevalence of urinary tract catheterization in UK nursing homes. J. Hosp. Infect. 55:119-123. http://dx.doi.org/10.1016/S0195-6701(03)00224-X.
7. Nickel JC. 1991. Catheter-associated urinary tract infection: new perspectives on old problems. Can. J. Infect. Control 6:38-42.
8. Stickler DJ. 2008. Bacterial biofilms in patients with indwelling urinary catheters. Nat. Clin. Pract. Urol. 5:598-608. http://dx.doi.org/10.1038/ncpuro1231.
9. Tambyah PA. 2004. Catheter-associated urinary tract infections: diagnosis and prophylaxis. Int. J. Antimicrob. Agents 24(Suppl 1):S44-S48. http://dx.doi.org/10.1016/j.ijantimicag.2004.02.008.
10. Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, Saint S, Schaeffer AJ, Tambayh PA, Tenke P, Nicolle LE. 2010. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin. Infect. Dis. 50:625-663. http://dx.doi.org/10.1086/650482.
11. Trautner BW. 2010. Management of catheter-associated urinary tract infection. Curr. Opin. Infect. Dis. 23:76-82. http://dx.doi.org/10.1097/QCO.0b013e328334dda8.
12. Mobley HLT. 1996. Virulence of Proteus mirabilis, p 245-265. In Mobley HLT, Warren JW (ed), Urinary tract infections: molecular pathogenesis and clinical management. American Society for Microbiology, Washington, DC.
13. Warren JW. 1991. The catheter and urinary tract infection. Med. Clin. North Am. 75:481-493.
14. Macleod SM, Sticker DJ. 2007. Species interactions in mixed-community crystalline biofilms on urinary catheters. J. Med. Microbiol. 56:1549-1557. http://dx.doi.org/10.1099/jmm.0.47395-0.
15. Stickler DJ, Ganderton L, King J, Nettleton J, Winters C. 1993. Proteus mirabilis biofilms and the encrustation of urethral catheters. Urol. Res. 21:407-411. http://dx.doi.org/10.1007/BF00300077.
16. Stickler DJ, Morris N, Moreno MC, Sabbuba N. 1998. Studies on the formation of crystalline bacterial biofilms on urethral catheters. Eur. J. Clin. Microbiol. Infect. Dis. 17:649-652. http://dx.doi.org/10.1007/s100960050150.
17. Stickler DJ, Morgan SD. 2008. Observations on the development of the crystalline bacterial biofilms that encrust and block Foley catheters. J. Hosp. Infect. 69:350-360. http://dx.doi.org/10.1016/j.jhin.2008.04.031.
18. Griffith DP, Musher DM, Itin C. 1976. Urease: the preliminary cause of infection induced urinary stones. Invest. Urol. 13:346-350.
19. Jones BD, Mobley HL. 1987. Genetic and biochemical diversity of ureases of Proteus, Providencia, and Morganella species isolated from urinary tract infections. Infect. Immun. 55:2190-2203.
20. Clapham L, McLean RJC, Nickel JC, Downey J, Costerton JW. 1990. The influence of bacteria on struvite crystal habit and its importance in urinary stone formation. J. Crystal Growth 104:475-484. http://dx.doi.org/10.1016/0022-0248(90)90150-J.
21. Dumanski AJ, Hedelin H, Edinliljegren A, Beauchemin D, McLean RJC. 1994. Unique ability of the Proteus mirabilis capsule to enhance mineral growth in infectious urinary calculi. Infect. Immun. 62:2998-3003.
22. Cox AJ, Hukins DWL. 1989. Morphology of mineral-deposits on encrusted urinary catheters investigated by scanning electron-microscopy. J. Urol. 142:1347-1350.
23. Kunin CM. 1997. Urinary tract infections: detection, prevention and management, 5th ed, p 226-278. Williams & Wilkins, Baltimore, MD.
24. Sabbuba NA, Mahenthiralingam E, Stickler DJ. 2003. Molecular epidemiology of Proteus mirabilis infections of the catheterized urinary tract. J. Clin. Microbiol. 41:4961-4965. http://dx.doi.org/10.1128/JCM.41.11.4961-4965.2003.
25. Morris NS, Stickler DJ, Winters C. 1997. Which indwelling urethral catheters resist encrustation by Proteus mirabilis biofilms? Br. J. Urol. 80: 58-63. http://dx.doi.org/10.1046/j.1464-410X.1997.00185.x.
26. Jones BV, Young R, Mahenthiralingam E, Stickler DJ. 2004. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect. Immun. 72:3941-3950. http://dx.doi.org/10.1128/IAI.72.7.3941-3950.2004.
27. Stickler DJ, Morris NS, Winters C. 1999. Simple physical model to study formation and physiology of biofilms on urethral catheters. Methods Enzymol. 310:494-501. http://dx.doi.org/10.1016/S0076-6879(99)10037-5.
28. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for biofilm development. Mol. Microbiol. 30:295-304. http://dx.doi.org/10.1046/j.1365-2958.1998.01062.x.
29. Manoil C. 2000. Tagging exported proteins using Escherichia coli alkaline phosphatase gene fusions. Methods Enzymol. 326:35-47. http://dx.doi.org/10.1016/S0076-6879(00)26045-X.
30. Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, Luscombe NM, Abdellah Z, Arrosmith C, Atkin B, Chillingworth T, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Walker D, Whithead S, Thomson NR, Rather PN, Parkhill J, Mobley HL. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol. 190:4027-4037. http://dx.doi.org/10.1128/JB.01981-07.
31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
32. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40(Database issue):D109-D114. http://dx.doi.org/10.1093/nar/gkr988.
33. Creno RJ, Wenk RE, Bohlig P. 1970. Automated micromeasurement of urea using urease and the Berthelot reaction. Am. J. Clin. Pathol. 54:828-832.
34. Jones BV, Mahenthiralingam E, Sabbuba NA, Stickler DJ. 2005. Role of swarming in the formation of crystalline Proteus mirabilis biofilms on urinary catheters. J. Med. Microbiol. 54(Part 9):807-813. http://dx.doi.org/10.1099/jmm.0.46123-0.
35. British Society for Antimicrobial Chemotherapy. May 2013. BSAC methods for antimicrobial susceptibility testing, version 12. http://bsac.org.uk/wp-content/uploads/2012/02/Version-12-Apr-2013_final.pdf.
36. Kvist M, Hancock V, Klemm P. 2008. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl. Environ. Microbiol. 74:7376-7382. http://dx.doi.org/10.1128/AEM.01310-08.
37. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
38. Huson DH, Scornavacca C. 2012. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 61:1061-1067. http://dx.doi.org/10.1093/sysbio/sys062.
39. Armbruster CE, Mobley HL. 2012. Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat. Rev. Microbiol. 10:743-754. http://dx.doi.org/10.1038/nrmicro2890.
40. Pearson MM, Rasko DA, Smith SN, Mobley HLT. 2010. Transcriptome of swarming Proteus mirabilis. Infect. Immun. 78:2834-2845. http://dx.doi.org/10.1128/IAI.01222-09.
41. Glynn A, Ward V, Wilson J, Charlett A, Cookson B, Taylor L, Cole. 1997. Hospital-acquired infection: surveillance, policies and practice. Public Health Laboratory Service, London, United Kingdom.
42. Saint S, Chenworth CE. 2003. Biofilms and catheter-associated urinary tract infection. Infect. Dis. Clin. North Am. 17:411-432. http://dx.doi.org/10.1016/S0891-5520(03)00011-4.
43. Van Alst NE, Picardo KF, Iglewski BH, Haidaris CG. 2007. Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect. Immun. 75:3780-3790. http://dx.doi.org/10.1128/IAI.00201-07.
44. Wang H, Gunsalus RP. 2000. The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differently in response to nitrate than to nitrite. J. Bacteriol. 182:5813-5822. http://dx.doi.org/10.1128/JB.182.20.5813-5822.2000.
45. Franz M, Hörl WH. 1999. Common errors in diagnosis and management of urinary tract infection. I. Pathophysiology and diagnostic techniques. Nephrol. Dial. Transplant. 14:2746-2753. http://dx.doi.org/10.1093/ndt/14.11.2746.
46. Stickler DJ, Lear JC, Morris NS, Macleod SM, Downer A, Cadd DH, Feast WJ. 2006. Observations on the adherence of Proteus mirabilis onto polymer surfaces. J. Appl. Microbiol. 100:1028-1033. http://dx.doi.org/10.1111/j.1365-2672.2006.02840.x.
47. Page L, Griffiths L, Cole JA. 1990. Different physiological roles of two independent pathways for nitrite reduction to ammonia by enteric bacteria. Arch. Microbiol. 154:349-354.
48. Donlan R, Costerton WJ. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193. http://dx.doi.org/10.1128/CMR.15.2.167-193.2002.
49. Matsumura K, Furukawa S, Ogihara H, Morinaga Y. 2011. Roles of multidrug efflux pumps in the biofilm formation of Escherichia coli K12. Biocontrol Sci. 16:69-72. http://dx.doi.org/10.4265/bio.16.69.
50. Soto SM. 2013. Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence 4:223-229. http://dx.doi.org/10.4161/viru.23724.
51. Baugh S, Ekanayaka AS, Piddock LJV, Webber MA. 2012. Loss of or inhibition of all multidrug resistance efflux pumps in Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J. Antimicrob. Chemother. 67:2409-2417. http://dx.doi.org/10.1093/jac/dks228.
52. Zhang L, Mah T-F. 2008. Involvement of a novel efflux system in biofilmspecific resistance to antibiotics. J. Bacteriol. 190:4447-4452. http://dx.doi.org/10.1128/JB.01655-07.
53. Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285-293. http://dx.doi.org/10.1046/j.1365-2958.1998.01061.x.
54. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R. 2001. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39:223-235. http://dx.doi.org/10.1046/j.1365-2958.2001.02195.x.
55. Sulavik MC, Houseweart C, Cramer C, Jiwani N, Murgolo N, Greene J, DiDomenico B, Shaw KJ, Miller GH, Hare R, Shimer G. 2001. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45:1126-1136. http://dx.doi.org/10.1128/AAC.45.4.1126-1136.2001.
56. Turner RJ, Taylor DE, Weiner JH. 1997. Expression of Escherichia coli TehA gives resistance to antiseptics and disinfectants similar to that conferred by multidrug efflux pumps. Antimicrob. Agents Chemother. 41: 440-444.