Pseudomonas aeruginosa exoproducts determine antibiotic efficacy against Staphylococcus aureus

PLoS Biology

Volumn 15, Issue 11, 2017, Pages

  Radlinski, Lauren ^a   Rowe, Sarah E ^a   Kartchner, Laurel B ^a,b   Maile, Robert ^a,b   Cairns, Bruce A ^a,b   Vitko, Nicholas P ^a   Gode, Cindy J ^a   Lachiewicz, Anne M ^a,b   Wolfgang, Matthew C ^a   Conlon, Brian P ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HEPTYL 4 HYDROXYQUINOLINE 1 OXIDE; ADENOSINE TRIPHOSPHATE; CIPROFLOXACIN; LASA PROTEIN; PROTEINASE; RHAMNOLIPID; TOBRAMYCIN; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT; GLYCOLIPID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIOLYSIS; BURN; BURN INFECTION; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG TOLERANCE; MOUSE; NONHUMAN; ORGANISMAL INTERACTION; PROTON MOTIVE FORCE; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; ANIMAL; ANTIBIOTIC RESISTANCE; C57BL MOUSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MICROBIOLOGY; MIXED INFECTION; OXYGEN CONSUMPTION; PATHOLOGY; PHYSIOLOGY; PSEUDOMONAS INFECTION; STAPHYLOCOCCUS INFECTION; WOUND INFECTION;

ANIMALS; ANTI-BACTERIAL AGENTS; BURNS; COINFECTION; DRUG RESISTANCE, BACTERIAL; GLYCOLIPIDS; MICE; MICE, INBRED C57BL; MICROBIAL INTERACTIONS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; OXYGEN CONSUMPTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VANCOMYCIN; WOUND INFECTION;

EID: 85036495200     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.2003981     Document Type: Article

References (65)

1. Conlon BP, Staphylococcus aureus chronic and relapsing infections: Evidence of a role for persister cells: An investigation of persister cells, their formation and their role in S. aureus disease. Bioessays. 2014;36(10):991–6. Epub 2014/08/08. doi: 10.1002/bies.201400080 25100240
2. Levin BR, Rozen DE, Non-inherited antibiotic resistance. Nat Rev Microbiol. 2006;4(7):556–62. doi: 10.1038/nrmicro1445 16778840
3. Kubicek-Sutherland JZ, Lofton H, Vestergaard M, Hjort K, Ingmer H, Andersson DI, Antimicrobial peptide exposure selects for Staphylococcus aureus resistance to human defence peptides. J Antimicrob Chemother. 2017;72(1):115–27. doi: 10.1093/jac/dkw381 27650186
4. Kong EF, Tsui C, Kucharikova S, Andes D, Van Dijck P, Jabra-Rizk MA, Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix. MBio. 2016;7(5). doi: 10.1128/mBio.01365-16 27729510
5. Hoffman LR, Deziel E, D’Argenio DA, Lepine F, Emerson J, McNamara S, et al. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2006;103(52):19890–5. doi: 10.1073/pnas.0606756104 17172450
6. Radlinski L, Conlon BP, Antibiotic efficacy in the complex infection environment. Curr Opin Microbiol. 2017;42:19–24. doi: 10.1016/j.mib.2017.09.007 28988156
7. Sorg RA, Lin L, van Doorn GS, Sorg M, Olson J, Nizet V, et al. Collective Resistance in Microbial Communities by Intracellular Antibiotic Deactivation. PLoS Biol. 2016;14(12):e2000631. doi: 10.1371/journal.pbio.2000631 28027306
8. Weimer KE, Juneau RA, Murrah KA, Pang B, Armbruster CE, Richardson SH, et al. Divergent mechanisms for passive pneumococcal resistance to beta-lactam antibiotics in the presence of Haemophilus influenzae. J Infect Dis. 2011;203(4):549–55. doi: 10.1093/infdis/jiq087 21220774
9. Brook I, The role of beta-lactamase-producing-bacteria in mixed infections. BMC Infect Dis. 2009;9:202. doi: 10.1186/1471-2334-9-202 20003454
10. Nicoloff H, Andersson DI, Indirect resistance to several classes of antibiotics in cocultures with resistant bacteria expressing antibiotic-modifying or -degrading enzymes. J Antimicrob Chemother. 2016;71(1):100–10. doi: 10.1093/jac/dkv312 26467993
11. Gjodsbol K, Christensen JJ, Karlsmark T, Jorgensen B, Klein BM, Krogfelt KA, Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J. 2006;3(3):225–31. doi: 10.1111/j.1742-481X.2006.00159.x 16984578
12. Pastar I, Nusbaum AG, Gil J, Patel SB, Chen J, Valdes J, et al. Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection. PLoS ONE. 2013;8(2):e56846. doi: 10.1371/journal.pone.0056846 23451098
13. Hendricks KJ, Burd TA, Anglen JO, Simpson AW, Christensen GD, Gainor BJ, Synergy between Staphylococcus aureus and Pseudomonas aeruginosa in a rat model of complex orthopaedic wounds. J Bone Joint Surg Am. 2001;83-A(6):855–61. 11407793
14. Duan K, Dammel C, Stein J, Rabin H, Surette MG, Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol. 2003;50(5):1477–91. 14651632
15. Nguyen AT, Jones JW, Camara M, Williams P, Kane MA, Oglesby-Sherrouse AG, Cystic Fibrosis Isolates of Pseudomonas aeruginosa Retain Iron-Regulated Antimicrobial Activity against Staphylococcus aureus through the Action of Multiple Alkylquinolones. Front Microbiol. 2016;7:1171. doi: 10.3389/fmicb.2016.01171 27512392
16. Filkins LM, Graber JA, Olson DG, Dolben EL, Lynd LR, Bhuju S, et al. Coculture of Staphylococcus aureus with Pseudomonas aeruginosa Drives S. aureus towards Fermentative Metabolism and Reduced Viability in a Cystic Fibrosis Model. J Bacteriol. 2015;197(14):2252–64. doi: 10.1128/JB.00059-15 25917910
17. Machan ZA, Taylor GW, Pitt TL, Cole PJ, Wilson R, 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa. J Antimicrob Chemother. 1992;30(5):615–23. 1493979
18. Kessler E, Safrin M, Olson JC, Ohman DE, Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem. 1993;268(10):7503–8. 8463280
19. Bharali P, Saikia JP, Ray A, Konwar BK, Rhamnolipid (RL) from Pseudomonas aeruginosa OBP1: a novel chemotaxis and antibacterial agent. Colloids Surf B Biointerfaces. 2013;103:502–9. doi: 10.1016/j.colsurfb.2012.10.064 23261573
20. Haba E, Pinazo A, Jauregui O, Espuny MJ, Infante MR, Manresa A, Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng. 2003;81(3):316–22. doi: 10.1002/bit.10474 12474254
21. Baldan R, Cigana C, Testa F, Bianconi I, De Simone M, Pellin D, et al. Adaptation of Pseudomonas aeruginosa in Cystic Fibrosis airways influences virulence of Staphylococcus aureus in vitro and murine models of co-infection. PLoS ONE. 2014;9(3):e89614. doi: 10.1371/journal.pone.0089614 24603807
22. Wakeman CA, Moore JL, Noto MJ, Zhang Y, Singleton MD, Prentice BM, et al. The innate immune protein calprotectin promotes Pseudomonas aeruginosa and Staphylococcus aureus interaction. Nat Commun. 2016;7:11951. doi: 10.1038/ncomms11951 27301800
23. Smith AC, Rice A, Sutton B, Gabrilska R, Wessel AK, Whiteley M, et al. Albumin Inhibits Pseudomonas aeruginosa Quorum Sensing and Alters Polymicrobial Interactions. Infection and immunity. 2017;85(9). doi: 10.1128/IAI.00116-17 28630071
24. Read RC, Roberts P, Munro N, Rutman A, Hastie A, Shryock T, et al. Effect of Pseudomonas aeruginosa rhamnolipids on mucociliary transport and ciliary beating. J Appl Physiol (1985). 1992;72(6):2271–7.
25. Kownatzki R, Tummler B, Doring G, Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet. 1987;1(8540):1026–7.
26. Hunter RC, Klepac-Ceraj V, Lorenzi MM, Grotzinger H, Martin TR, Newman DK, Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. American journal of respiratory cell and molecular biology. 2012;47(6):738–45. doi: 10.1165/rcmb.2012-0088OC 22865623
27. Barr HL, Halliday N, Camara M, Barrett DA, Williams P, Forrester DL, et al. Pseudomonas aeruginosa quorum sensing molecules correlate with clinical status in cystic fibrosis. The European respiratory journal: official journal of the European Society for Clinical Respiratory Physiology. 2015;46(4):1046–54. doi: 10.1183/09031936.00225214 26022946
28. O’Brien S, Williams D, Fothergill JL, Paterson S, Winstanley C, Brockhurst MA, High virulence sub-populations in Pseudomonas aeruginosa long-term cystic fibrosis airway infections. BMC Microbiol. 2017;17(1):30. doi: 10.1186/s12866-017-0941-6 28158967
29. Mates SM, Eisenberg ES, Mandel LJ, Patel L, Kaback HR, Miller MH, Membrane potential and gentamicin uptake in Staphylococcus aureus. Proc Natl Acad Sci U S A. 1982;79(21):6693–7. 6959147
30. Sotirova AV, Spasova DI, Galabova DN, Karpenko E, Shulga A, Rhamnolipid-biosurfactant permeabilizing effects on gram-positive and gram-negative bacterial strains. Curr Microbiol. 2008;56(6):639–44. doi: 10.1007/s00284-008-9139-3 18330632
31. Bjarnsholt T, Jensen PO, Jakobsen TH, Phipps R, Nielsen AK, Rybtke MT, et al. Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS ONE. 2010;5(4):e10115. doi: 10.1371/journal.pone.0010115 20404933
32. Lepine F, Milot S, Deziel E, He J, Rahme LG, Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom. 2004;15(6):862–9. doi: 10.1016/j.jasms.2004.02.012 15144975
33. Jain DK, Collinsthompson DL, Lee H, Trevors JT, A Drop-Collapsing Test for Screening Surfactant-Producing Microorganisms. J Microbiol Meth. 1991;13(4):271–9. doi: 10.1016/0167-7012(91)90064-W
34. Shan Y, Brown Gandt A, Rowe SE, Deisinger JP, Conlon BP, Lewis K, ATP-Dependent Persister Formation in Escherichia coli. mBio. 2017;8(1). doi: 10.1128/mBio.02267-16 28174313
35. Conlon BP, Rowe SE, Gandt AB, Nuxoll AS, Donegan NP, Zalis EA, et al. Persister formation in Staphylococcus aureus is associated with ATP depletion. Nat Microbiol. 2016;1:16051. doi: 10.1038/nmicrobiol.2016.51 27398229
36. Fuchs S, Pane-Farre J, Kohler C, Hecker M, Engelmann S, Anaerobic gene expression in Staphylococcus aureus. J Bacteriol. 2007;189(11):4275–89. doi: 10.1128/JB.00081-07 17384184
37. Ryall B, Davies JC, Wilson R, Shoemark A, Williams HD, Pseudomonas aeruginosa, cyanide accumulation and lung function in CF and non-CF bronchiectasis patients. The European respiratory journal: official journal of the European Society for Clinical Respiratory Physiology. 2008;32(3):740–7. doi: 10.1183/09031936.00159607 18480102
38. Thierbach S, Birmes FS, Letzel MC, Hennecke U, Fetzner S, Chemical Modification and Detoxification of the Pseudomonas aeruginosa Toxin 2-Heptyl-4-hydroxyquinoline N-Oxide by Environmental and Pathogenic Bacteria. ACS Chem Biol. 2017;12(9):2305–12. doi: 10.1021/acschembio.7b00345 28708374
39. Grande KK, Gustin JK, Kessler E, Ohman DE, Identification of critical residues in the propeptide of LasA protease of Pseudomonas aeruginosa involved in the formation of a stable mature protease. J Bacteriol. 2007;189(11):3960–8. doi: 10.1128/JB.01828-06 17351039
40. Orazi G, O’Toole GA, Pseudomonas aeruginosa Alters Staphylococcus aureus Sensitivity to Vancomycin in a Biofilm Model of Cystic Fibrosis Infection. MBio. 2017;8(4). doi: 10.1128/mBio.00873-17 28720732
41. Neely CJ, Kartchner LB, Mendoza AE, Linz BM, Frelinger JA, Wolfgang MC, et al. Flagellin treatment prevents increased susceptibility to systemic bacterial infection after injury by inhibiting anti-inflammatory IL-10+ IL-12- neutrophil polarization. PLoS ONE. 2014;9(1):e85623. doi: 10.1371/journal.pone.0085623 24454904
42. Cowell BA, Twining SS, Hobden JA, Kwong MS, Fleiszig SM, Mutation of lasA and lasB reduces Pseudomonas aeruginosa invasion of epithelial cells. Microbiology. 2003;149(Pt 8):2291–9. doi: 10.1099/mic.0.26280-0 12904569
43. White CD, Alionte LG, Cannon BM, Caballero AR, O’Callaghan RJ, Hobden JA, Corneal virulence of LasA protease—deficient Pseudomonas aeruginosa PAO1. Cornea. 2001;20(6):643–6. 11473168
44. Limoli DH, Yang J, Khansaheb MK, Helfman B, Peng L, Stecenko AA, et al. Staphylococcus aureus and Pseudomonas aeruginosa co-infection is associated with cystic fibrosis-related diabetes and poor clinical outcomes. European Journal of Clinical Microbiology & Infectious Diseases. 2016;35(6):947–53. doi: 10.1007/s10096-016-2621-0 26993289
45. Hendricks KJ, Burd TA, Anglen JO, Simpson AW, Christensen GD, Gainor BJ, Synergy between Staphylococcus aureus and Pseudomonas aeruginosa in a rat model of complex orthopaedic wounds. Journal of Bone and Joint Surgery-American Volume. 2001;83a(6):855–61.
46. Armbruster CE, Hong W, Pang B, Weimer KED, Juneau RA, Turner J, et al. Indirect Pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling. MBio. 2010;1(3). ARTN e00102–10doi: 10.1128/mBio.00102-10 20802829
47. Burmolle M, Webb JS, Rao D, Hansen LH, Sorensen SJ, Kjelleberg S, Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microb. 2006;72(6):3916–23. doi: 10.1128/Aem.03022-05 16751497
48. Taber HW, Mueller JP, Miller PF, Arrow AS, Bacterial uptake of aminoglycoside antibiotics. Microbiol Rev. 1987;51(4):439–57. 3325794
49. Allison KR, Brynildsen MP, Collins JJ, Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature. 2011;473(7346):216–20. Epub 2011/05/13. doi: 10.1038/nature10069 21562562
50. Beaudoin T, Yau YCW, Stapleton PJ, Gong Y, Wang PW, Guttman DS, et al. Staphylococcus aureus interaction with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. NPJ Biofilms Microbiomes. 2017;3:25. doi: 10.1038/s41522-017-0035-0 29062489
51. Reynolds PE, Structure, biochemistry and mechanism of action of glycopeptide antibiotics. Eur J Clin Microbiol Infect Dis. 1989;8(11):943–50. 2532132
52. Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, Ramsey BW, et al. Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros. 2009;8(1):66–70. doi: 10.1016/j.jcf.2008.09.006 18974024
53. Limoli DH, Whitfield GB, Kitao T, Ivey ML, Davis MR, Jr.Grahl N, et al. Pseudomonas aeruginosa Alginate Overproduction Promotes Coexistence with Staphylococcus aureus in a Model of Cystic Fibrosis Respiratory Infection. MBio. 2017;8(2). doi: 10.1128/mBio.00186-17 28325763
54. Lipuma JJ, The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev. 2010;23(2):299–323. doi: 10.1128/CMR.00068-09 20375354
55. Held K, Ramage E, Jacobs M, Gallagher L, Manoil C, Sequence-verified two-allele transposon mutant library for Pseudomonas aeruginosa PAO1. J Bacteriol. 2012;194(23):6387–9. doi: 10.1128/JB.01479-12 22984262
56. Hoang T, Karkhoff-Schweizer R, Kutchma A, Schweizer H, A broad-host-range FLP-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene. 1998;212:77–86. 9661666
57. Cheung AL, Nast CC, Bayer AS, Selective activation of sar promoters with the use of green fluorescent protein transcriptional fusions as the detection system in the rabbit endocarditis model. Infection and immunity. 1998;66(12):5988–93. 9826382
58. Szalek E, Kaminska A, Gozdzik-Spychalska J, Grzeskowiak E, Batura-Gabryel H, The PK/PD index (CMAX/MIC) for ciprofloxacin in patients with cystic fibrosis. Acta Pol Pharm. 2011;68(5):777–83. 21928725
59. Burkhardt O, Lehmann C, Madabushi R, Kumar V, Derendorf H, Welte T, Once-daily tobramycin in cystic fibrosis: better for clinical outcome than thrice-daily tobramycin but more resistance development?J Antimicrob Chemother. 2006;58(4):822–9. doi: 10.1093/jac/dkl328 16885180
60. Barcia-Macay M, Lemaire S, Mingeot-Leclercq MP, Tulkens PM, Van Bambeke F, Evaluation of the extracellular and intracellular activities (human THP-1 macrophages) of telavancin versus vancomycin against methicillin-susceptible, methicillin-resistant, vancomycin-intermediate and vancomycin-resistant Staphylococcus aureus. J Antimicrob Chemother. 2006;58(6):1177–84. doi: 10.1093/jac/dkl424 17062609
61. Ruddy J, Emerson J, Moss R, Genatossio A, McNamara S, Burns JL, et al. Sputum tobramycin concentrations in cystic fibrosis patients with repeated administration of inhaled tobramycin. J Aerosol Med Pulm Drug Deliv. 2013;26(2):69–75. doi: 10.1089/jamp.2011.0942 22620494
62. Rohwedder R, Bergan T, Caruso E, Thorsteinsson SB, Dellatorre H, Scholl H, Penetration of Ciprofloxacin and Metabolites into Human Lung, Bronchial and Pleural Tissue after 250 and 500 Mg Oral Ciprofloxacin. Chemotherapy. 1991;37(4):229–38. 1790720
63. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K, Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett. 2004;230(1):13–8. 14734160
64. Shen Y, G A, Rowe SE, Deisinger J, Conlon BP, Lewis K, ATP dependent persister formation in Escherichia coli. MBio. 2017;8(1):e02267–16. doi: 10.1128/mBio.02267-16 28174313
65. Sundin DP, Meyer C, Dahl R, Geerdes A, Sandoval R, Molitoris BA, Cellular mechanism of aminoglycoside tolerance in long-term gentamicin treatment. Am J Physiol. 1997;272(4 Pt 1):C1309–18. 9142857