Comparative physiological study of the wild type and the small colony variant of Pseudomonas aeruginosa 20265 under controlled growth conditions

World Journal of Microbiology and Biotechnology

Volumn 30, Issue 3, 2014, Pages 1027-1036

  Sabra, W ^a,b,c   Haddad, A M ^b,d   Zeng, A P ^a,b  

^a HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c ALEXANDRIA UNIVERSITY   (Egypt)

^d GENETIC ENGINEERING AND BIOTECHNOLOGY RESEARCH INSTITUTE   (Egypt)

Author keywords

Controlled bioreactor; Iron limitation; Oxygen transfer; pO2 control; Pseudomonas aeruginosa; SCV; Virulence factor

Indexed keywords

IRON-LIMITATION; OXYGEN TRANSFER; PSEUDOMONAS AERUGINOSA; SCV; VIRULENCE FACTORS;

BACTERIA; CULTIVATION; PLANTS (BOTANY);

IRON;

IRON; OXYGEN;

AEROBIC METABOLISM; ARTICLE; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PSEUDOMONAS AERUGINOSA;

AEROBIOSIS; HUMANS; IRON; OXYGEN; PSEUDOMONAS AERUGINOSA;

EID: 84893555990     PISSN: 09593993     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11274-013-1521-z     Document Type: Article

References (43)

1. Amiel E, Lovewell RR, O'Toole GA, Hogan DA, Berwin B (2010) Pseudomonas aeruginosa evasion of phagocytosis is mediated by loss of swimming motility and is independent of flagellum expression. Infect Immun 78: 2937-2945.
2. Besier S, Smaczny C, Von MC, Krahl A, Ackermann H, Brade V, Wichelhaus TA (2007) Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J Clin Microbiol 45: 168-172.
3. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, Smith EE, Nguyen H, Ernst RK, Larson Freeman TJ, Spencer DH, Brittnacher M, Hayden HS, Selgrade S, Klausen M, Goodlett DR, Burns JL, Ramsey BW, Miller SI (2007) Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533.
4. Davies JA, Harrison JJ, Marques LL, Foglia GR, Stremick CA, Storey DG, Turner RJ, Olson ME, Ceri H (2007) The GacS sensor kinase controls phenotypic reversion of small colony variants isolated from biofilms of Pseudomonas aeruginosa PA14. FEMS Microbiol Ecol 59: 32-46.
5. Deretic V, Martin DW, Schurr MJ, Mudd MH, Hibler NS, Curcic R, Boucher JC (1993) Conversion to mucoidy in Pseudomonasaeruginosa. Biotechnology 11(10): 1133-1136.
6. Deretic V, Schurr MJ, Boucher JC, Martin DW (1994) Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors. J Bacteriol 176: 2773-2780.
7. Deziel E, Comeau Y, Villemur R (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204.
8. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539-574.
9. Haussler S (2004) Biofilm formation by the small colony variant phenotype of Pseudomonasaeruginosa. Environ Microbiol 6: 546-551.
10. Haussler S, Rohde M, Steinmetz I (1999a) Highly resistant Burkholderia pseudomallei small colony variants isolated in vitro and in experimental melioidosis. Med Microbiol Immunol 188: 91-97.
11. Haussler S, Tummler B, Weissbrodt H, Rohde M, Steinmetz I (1999b) Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29: 621-625.
12. Haussler S, Ziegler I, Lottel A, Von GF, Rohde M, Wehmhohner D, Saravanamuthu S, Tummler B, Steinmetz I (2003) Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52: 295-301.
13. Hawdon NA, Aval PS, Barnes RJ, Gravelle SK, Rosengren J, Khan S, Ciofu O, Johansen HK, Hoiby N, Ulanova M (2010) Cellular responses of A549 alveolar epithelial cells to serially collected Pseudomonas aeruginosa from cystic fibrosis patients at different stages of pulmonary infection. FEMS Immunol Med Microbiol 59: 207-220.
14. Kessler E, Safrin M, Olson JC, Ohman DE (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268: 7503-7508.
15. Kim EJ, Sabra W, Zeng A-P (2003) Iron deficiency leads to inhibition of oxygen transfer and enhanced formation of virulence factors in cultures of Pseudomonas aeruginosa PAO1. Microbiology 149: 2627-2634.
16. Kim EJ, Wang W, Deckwer WD, Zeng A-P (2005) Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density. Microbiology 151: 1127-1138.
17. Kirisits MJ, Prost L, Starkey M, Parsek MR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71: 4809-4821.
18. Kobayashi H (2005) Airway biofilms: implications for pathogenesis and therapy of respiratory tract infections. Treat Respir Med 4: 241-253.
19. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
20. Malone JG, Jaeger T, Spangler C, Ritz D, Spang A, Arrieumerlou C, Kaever V, Landmann R, Jenal U (2010) YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog 6: e1000804.
21. Moreau-Marquis S, Bomberger JM, Anderson GG, Swiatecka-Urban A, Ye S, O'Toole GA, Stanton BA (2008) The DeltaF508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am J Physiol Lung Cell Mol Physiol 295: L25-L37.
22. Mulcahy LR, Burns JL, Lory S, Lewis K (2010) Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol 192: 6191-6199.
23. Nelson LK, Stanton MM, Elphinstone RE, Helwerda J, Turner RJ, Ceri H (2010) Phenotypic diversification in vivo: Pseudomonas aeruginosa gacS- strains generate small colony variants in vivo that are distinct from in vitro variants. Microbiology 156(12): 3699-3709.
24. Neut D, van der Mei HC, Bulstra SK, Busscher HJ (2007) The role of small-colony variants in failure to diagnose and treat biofilm infections in orthopedics. Acta Orthop 78: 299-308.
25. Oliver A (2010) Mutators in cystic fibrosis chronic lung infection: prevalence, mechanisms, and consequences for antimicrobial therapy. Int J Med Microbiol 300: 563-572.
26. Oliver A, Mena A (2010) Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 16: 798-808.
27. Proctor RA, Balwit JM, Vesga O (1994) Variant subpopulations of Staphylococcus aureus as cause of persistent and recurrent infections. Infect Agents Dis 3: 302-312.
28. Proctor RA, van LP, Kristjansson M, Maslow JN, Arbeit RD (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20: 95-102.
29. Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, Tay M, Hauser A, McDougald D, Webb JS, Kjelleberg S (2009) The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J 3: 271-282.
30. Rolli J, Loukili N, Levrand S, Rosenblatt-Velin N, Rignault-Clerc S, Waeber B, Feihl F, Pacher P, Liaudet L (2010a) Bacterial flagellin elicits widespread innate immune defense mechanisms, apoptotic signaling, and a sepsis-like systemic inflammatory response in mice. Crit Care 14: R160.
31. Rolli J, Rosenblatt-Velin N, Li J, Loukili N, Levrand S, Pacher P, Waeber B, Feihl F, Ruchat P, Liaudet L (2010b) Bacterial flagellin triggers cardiac innate immune responses and acute contractile dysfunction. PLoS ONE 5: e12687.
32. Sabra W, Zeng A-P, Lunsdorf H, Deckwer W-D (2000) Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role in protecting nitrogenase. Appl Environ Microbiol 66: 4037-4044.
33. Sabra W, Kim EJ, Zeng A-P (2002) Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures. Microbiology 148: 3195-3202.
34. Sabra W, Lunsdorf H, Zeng A-P (2003) Alterations in the formation of lipopolysaccharide and membrane vesicles on the surface of Pseudomonas aeruginosa PAO1 under oxygen stress conditions. Microbiology 149: 2789-2795.
35. Schneider M, Muhlemann K, Droz S, Couzinet S, Casaulta C, Zimmerli S (2008) Clinical characteristics associated with isolation of small-colony variants of Staphylococcus aureus and Pseudomonas aeruginosa from respiratory secretions of patients with cystic fibrosis. J Clin Microbiol 46: 1832-1834.
36. Soberon-Chavez G, Lepine F, Deziel E (2005) Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol 68: 718-725.
37. Starkey M, Hickman JH, Ma L, Zhang N, De LS, Hinz A, Palacios S, Manoil C, Kirisits MJ, Starner TD, Wozniak DJ, Harwood CS, Parsek MR (2009) Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191: 3492-3503.
38. von Eiff C, Peters G, Becker K (2006) The small colony variant (SCV) concept-the role of staphylococcal SCVs in persistent infections. Injury 37(2): S26-S33.
39. von Gotz F, Haussler S, Jordan D, Saravanamuthu SS, Wehmhoner D, Strussmann A, Lauber J, Attree I, Buer J, Tummler B, Steinmetz I (2004) Expression analysis of a highly adherent and cytotoxic small colony variant of Pseudomonas aeruginosa isolated from a lung of a patient with cystic fibrosis. J Bacteriol 186: 3837-3847.
40. Webb JS, Lau M, Kjelleberg S (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186: 8066-8073.
41. Wei Q, Tarighi S, Dotsch A, Haussler S, Musken M, Wright VJ, Camara M, Williams P, Haenen S, Boerjan B, Bogaerts A, Vierstraete E, Verleyen P, Schoofs L, Willaert R, De Groote VN, Michiels J, Vercammen K, Crabbe A, Cornelis P (2011) Phenotypic and genome-wide analysis of an antibiotic-resistant small colony variant (SCV) of Pseudomonas aeruginosa. PLoS ONE 6: e29276.
42. Werth N, Beerlage C, Rosenberger C, Yazdi AS, Edelmann M, Amr A, Bernhardt W, Von EC, Becker K, Schafer A, Peschel A, Kempf VA (2010) Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS ONE 5: e11576.
43. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, Botzenhart K, Yankaskas JR, Randell S, Boucher RC, Doring G (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109: 317-325.