Generic placeholder image

Current Pharmaceutical Biotechnology

Author(s): Nur S. Ismail, Suresh K. Subbiah and Niazlin M. Taib*

DOI: 10.2174/1389201021666200629145217

DownloadDownload PDF Flyer Cite As
Application of Phenotype Microarray for Profiling Carbon Sources Utilization between Biofilm and Non-Biofilm of Pseudomonas aeruginosa from Clinical Isolates

Page: [1539 - 1550] Pages: 12

  • * (Excluding Mailing and Handling)

Explore Articles
About Journal
For Authors
For Editors
For Reviewers

Abstract

Background: This is the fastest work in obtaining the metabolic profiles of Pseudomonas aeruginosa in order to combat the infection diseases which leads to high morbidity and mortality rates. Pseudomonas aeruginosa is a high versatility of gram-negative bacteria that can undergo aerobic and anaerobic respiration. Capabilities in deploying different carbon sources, energy metabolism and regulatory system, ensure the survival of this microorganism in the diverse environment condition. Determination of differences in carbon sources utilization among biofilm and non-biofilm of Pseudomonas aeruginosa provides a platform in understanding the metabolic activity of the microorganism.

Methods: The study was carried out from September 2017 to February 2019. Four archive isolates forming strong and intermediate biofilm and non-biofilms producer were subcultured from archive isolates. ATCC 27853 P. aeruginosa was used as a negative control or non-biofilm producing microorganism. Biofilm formation was confirmed by Crystal Violet Assay (CVA) and Congo Red Agar (CRA). Metabolic profiles of the biofilm and non-biofilms isolates were determined by phenotype microarrays (Biolog Omnilog).

Results and Discussion: In this study, Pseudomonas aeruginosa biofilm isolates utilized uridine, L-threonine and L-serine while non-biofilm utilized adenosine, inosine, monomethyl, sorbic acid and succinamic acid.

Conclusion: The outcome of this result will be used for future studies to improve detection or inhibit the growth of P. aeruginosa biofilm and non-biofilm respectively.

Keywords: Pseudomonas, CVA, CRA, phenotype, microarrays, M.I.C, biofilm.

Graphical Abstract

[1]
Schmidt, K.D.; Tümmler, B.; Römling, U. Comparative genome mapping of Pseudomonas aeruginosa PAO with P. aeruginosa C, which belongs to a major clone in cystic fibrosis patients and aquatic habitats. J. Bacteriol., 1996, 178(1), 85-93.
[http://dx.doi.org/10.1128/JB.178.1.85-93.1996] [PMID: 8550447]
[2]
Ramos, J.L. Genomics, Life Style and Molecular Architecture; Kluwer Academic: Boston, Massachusetts, USA, 2004.
[3]
Frimmersdorf, E.; Horatzek, S.; Pelnikevich, A.; Wiehlmann, L.; Schomburg, D. How Pseudomonas aeruginosa adapts to various environments: A metabolomic approach.Environ. Microbiol, 2010, 12(6), 1734-1747.
[http://dx.doi.org/10.1111/j.1462-2920.2010.02253.x] [PMID: 20553553]
[4]
Bodey, G.P.; Jadeja, L.; Elting, L. Pseudomonas bacteremia. Retrospective analysis of 410 episodes. Arch. Intern. Med., 1985, 145(9), 1621-1629..
[http://dx.doi.org/10.1001/archinte.1985.00360090089015] [PMID: 3927867]
[5]
Chatzinikolaou, I.; Abi-Said, D.; Bodey, G.P.; Rolston, K.V.; Tarrand, J.J.; Samonis, G. Recent experience with Pseudomonas aeruginosa bacteremia in patients with cancer: Retrospective analysis of 245 episodes. Arch. Intern. Med., 2000, 160(4), 501-509.
[http://dx.doi.org/10.1001/archinte.160.4.501] [PMID: 10695690]
[6]
Williams, H.D.; Zlosnik, J.E.; Ryall, B. Oxygen, cyanide, and energy generation in the cystic fibrosis pathogen Pseudomonas aeruginosa. Adv. Microb. Physiol., 2006, 1-71.
[http://dx.doi.org/10.1016/S0065-2911(06)52001-6]
[7]
Singh, V.; Haque, S.; Niwas, R.; Srivastava, A.; Pasupuleti, M.; Tripathi, C.K.M. Strategies for fermentation medium optimization: An in-depth review. Front. Microbiol., 2017, 7, 2087.
[http://dx.doi.org/10.3389/fmicb.2016.02087] [PMID: 28111566]
[8]
Harmsen, M.; Yang, L.; Pamp, S.J.; Tolker-Nielsen, T. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol.,, 2010, 59(3), 253, 268.
[http://dx.doi.org/10.1111/j.1574-695X.2010.00690.x] [PMID: 20497222]
[9]
Hoyle, B.D.; Wong, C.K.; Costerton, J.W. Disparate efficacy of tobramycin on Ca2+-, Mg2+-, and HEPES-treated Pseudomonas aeruginosa biofilms. Can. J. Microbiol., 1992, 38(11), 1214-1218.
[http://dx.doi.org/10.1139/m92-201] [PMID: 1477794]
[10]
Shigeta, M.; Tanaka, G.; Komatsuzawa, H.; Sugai, M.; Suginaka, H.; Usui, T. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: A simple method. Chemotherapy, 1997, 43(5), 340-345.
[http://dx.doi.org/10.1159/000239587] [PMID: 9309367]
[11]
Alipour, M.; Suntres, Z.E.; Omri, A. Importance of DNase and alginate lyase for enhancing free and liposome encapsulated aminoglycoside activity against Pseudomonas aeruginosa. J. Antimicrob. Chemother., 2009, 64(2), 317-325.
[http://dx.doi.org/10.1093/jac/dkp165] [PMID: 19465435]
[12]
Banin, E.; Brady, K.M.; Greenberg, E.P. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm.Appl. Environ. Microbiol , 2006, 72(3), 2064-2069.
[http://dx.doi.org/10.1128/AEM.72.3.2064-2069.2006] [PMID: 16517655]
[13]
Pamp, S.J.; Gjermansen, M.; Johansen, H.K.; Tolker-Nielsen, T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes.Mol. Microbiol.,, 2008, 68(1), 223-240.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06152.x] [PMID: 18312276]
[14]
Anderson, G.G.; Kenney, T.F.; Macleod, D.L.; Henig, N.R.; O’Toole, G.A. Eradication of Pseudomonas aeruginosa biofilms on cultured airway cells by a fosfomycin/tobramycin antibiotic combination. Pathog. Dis., 2013, 67(1), 39-45.
[http://dx.doi.org/10.1111/2049-632X.12015] [PMID: 23620118]
[15]
Wagenlehner, F.M.; Naber, K.G. Treatment of bacterial urinary tract infections: Presence and future. Eur. Urol., 2006, 49(2), 235-244.
[http://dx.doi.org/10.1016/j.eururo.2005.12.017] [PMID: 16413668]
[16]
Tielen, P.; Kuhn, H.; Rosenau, F.; Jaeger, K.E.; Flemming, H.C.; Wingender, J. Interaction between extracellular lipase LipA and the polysaccharide alginate of Pseudomonas aeruginosa. BMC Microbiol., 2013, 13(1), 159.
[http://dx.doi.org/10.1186/1471-2180-13-159] [PMID: 23848942]
[17]
Bochner, B.R. Sleuthing out bacterial identities. Nature, 1989, 339(6220), 157-158.
[http://dx.doi.org/10.1038/339157a0] [PMID: 2654644]
[18]
Johnson, D.A.; Tetu, S.G.; Phillippy, K.; Chen, J.; Ren, Q.; Paulsen, I.T. High-throughput phenotypic characterization of Pseudomonas aeruginosa membrane transport genes. PLoS Genet., 2008, 4(10)e1000211
[http://dx.doi.org/10.1371/journal.pgen.1000211] [PMID: 18833300]
[19]
O’Toole, G.A. Microtiter dish biofilm formation assay. J. Vis. Exp., 2011, 47(47), 10-11.
[http://dx.doi.org/10.3791/2437] [PMID: 21307833]
[20]
Freeman, D.J.; Falkiner, F.R.K.C. Slime, new method for detecting negative, production by coagulase. J. Clin. Pathol., 1989, 42(8), 872-874.
[http://dx.doi.org/10.1136/jcp.42.8.872] [PMID: 2475530]
[21]
Martin, A.; Camacho, M.; Portaels, F.; Palomino, J.C. Resazurin microtiter assay plate testing of Mycobacterium tuberculosis susceptibilities to second-line drugs: Rapid, simple, and inexpensive method. Antimicrob. Agents Chemother, 2003, 47(11), 3616-3619.
[http://dx.doi.org/10.1128/AAC.47.11.3616-3619.2003] [PMID: 14576129]
[22]
Collier, D.N.; Hager, P.W.; Phibbs, P.V., Jr Catabolite repression control in the Pseudomonads. Res. Microbiol., 1996, 147(6-7), 551-561.
[http://dx.doi.org/10.1016/0923-2508(96)84011-3] [PMID: 9084769]
[23]
Rojo, F. Carbon catabolite repression in Pseudomonas: Optimizing metabolic versatility and interactions with the environment. FEMS Microbiol. Rev.,, 2010, 34(6), 658-584.
[http://dx.doi.org/10.1111/j.1574-6976.2010.00218.x] [PMID: 20412307]
[24]
Dimroth, P.; Hilbi, H. Enzymic and genetic basis for bacterial growth on malonate.Mol. Microbiol.,, 1997, 25(1), 3-10.
[http://dx.doi.org/10.1046/j.1365-2958.1997.4611824.x] [PMID: 11902724]
[25]
Yuste, L.; Canosa, I.; Rojo, F. Carbon-source-dependent expression of the PalkB promoter from the Pseudomonas oleovorans alkane degradation pathway J. Bacteriol, 1998, 180(19), 5218-5226..
[http://dx.doi.org/10.1128/JB.180.19.5218-5226.1998] [PMID: 9748457]
[26]
Staijen, I.E.; Marcionelli, R.; Witholt, B. The PalkBFGHJKL promoter is under carbon catabolite repression control in Pseudomonas oleovorans but not in Escherichia coli alk+ recombinants. J. Bacteriol., 1999, 181(5), 1610-1616.
[http://dx.doi.org/10.1128/JB.181.5.1610-1616.1999] [PMID: 10049394]
[27]
Müller, C.; Petruschka, L.; Cuypers, H.; Burchhardt, G.; Herrmann, H. Carbon catabolite repression of phenol degradation in Pseudomonas putida is mediated by the inhibition of the activator protein PhlR. J. Bacteriol , 1996,, 178(7), 2030-2036..
[http://dx.doi.org/10.1128/JB.178.7.2030-2036.1996] [PMID: 8606180]
[28]
Berg, J.M.; Tymoczko, J.L.; Stryer, L. Glycolysis is an energyconversion pathway in many organisms. Biochemistry, 5th ed; WH Freeman: New York,; , 2002.
[29]
Pizzorno, G.; Cao, D.; Leffert, J.J.; Russell, R.L.; Zhang, D.; Handschumacher, R.E. Homeostatic control of uridine and the role of uridine phosphorylase: A biological and clinical update.Biochim. Biophys. Acta , 2002, 1587(2-3), 133-144.
[http://dx.doi.org/10.1016/S0925-4439(02)00076-5] [PMID: 12084455]
[30]
Renck, D.; Machado, P.; Souto, A.A.; Rosado, L.A.; Erig, T.; Campos, M.M.; Farias, C.B.; Roesler, R.; Timmers, L.F.; de Souza, O.N.; Santos, D.S.; Basso, L.A. Design of novel potent inhibitors of human uridine phosphorylase-1: Synthesis, inhibition studies, thermodynamics, and in vitro influence on 5-fluorouracil cytotoxicity. J. Med. Chem., 2013, 56(21), 8892-8902.
[http://dx.doi.org/10.1021/jm401389u] [PMID: 24131420]
[31]
Bajaj, A.; Kumar, A.; Yadav, S.; Kaur, G.; Bala, M.; Singh, N.K.; Mathan Kumar, R.; Manickam, N.; Mayilraj, S. Isolation and characterization of a novel Gram-negative bacterium Chromobacterium alkanivorans sp. nov., strain IITR-71T degrading halogenated alkanes. Int. J. Syst. Evol. Microbiol., 2016, 66(12), 5228-5235.
[http://dx.doi.org/10.1099/ijsem.0.001500] [PMID: 27619232]
[32]
Matsumoto, H.; Ohta, S.; Kobayashi, R.; Terawaki, Y. Chromosomal location of genes participating in the degradation of purines in Pseudomonas aeruginosa. Mol. Gen. Genet., 1978, 167(2), 165-176.
[http://dx.doi.org/10.1007/BF00266910] [PMID: 104142]
[33]
Bongaerts, G.P.; Sin, I.L.; Peters, A.L.; Vogels, G.D. Purine degradation in Pseudomonas aeruginosa and Pseudomonas testosteroni. Biochim. Biophys. Acta, 1977, 499(1), 111-118.
[http://dx.doi.org/10.1016/0304-4165(77)90233-1] [PMID: 407941]
[34]
Toussaint, J.P.; Farrell-Sherman, A.; Feldman, T.P.; Smalley, N.E.; Schaefer, A.L.; Greenberg, E.P.; Dandekar, A.A. Gene duplication in Pseudomonas Aeruginosa improves growth on adenosine. J. Bacteriol., 2017, 199(21), e00261-e17.
[http://dx.doi.org/10.1128/JB.00261-17] [PMID: 28808129]
[35]
Costerton, J.W.; Stewart, P.S.; Greenberg, E.P. Bacterial biofilms: A common cause of persistent infections. Science, 1999, 284(5418), 1318-1322.
[http://dx.doi.org/10.1126/science.284.5418.1318] [PMID: 10334980]
[36]
Sheng, L.; Pu, M.; Hegde, M.; Zhang, Y.; Jayaraman, A.; Wood, T.K. Interkingdom adenosine signal reduces Pseudomonas aeruginosa pathogenicity. Microb. Biotechnol, 2012, 5(4), 560-572.
[http://dx.doi.org/10.1111/j.1751-7915.2012.00338.x] [PMID: 22414222]
[37]
Prub, B.M.; Nelms, J.M.; Park, C.; Wolfe, A.J. Mutations in NADH: Ubiquinone oxidoreductase. J. Bacteriol., 1994, 176(8), 2143-2150.
[38]
Zinser, E.R.; Kolter, R. Prolonged stationary-phase incubation selects for Lrp mutations in Escherichia coli prolonged stationary-phase incubation selects for Lrp mutations in Escherichia coli K-12. J. Bacteriol., 2000, 182(15), 4361-4365.
[39]
Mathee, K.; Leal, S.M.; Newman, E. Characterization of L-serine deaminases, SdaA (PA2448) and SdaB (PA5379), and their potential role in Pseudomonas aeruginosa pathogenesis; BioRxivorg, 2018, p. 394957.
[40]
Wong, H.C.; Lessie, T.G. Hydroxy amino acid metabolism in Pseudomonas cepacia: Role of L-serine deaminase in dissimilation of serine, glycine, and threonine. J. Bacteriol., 1979, 140(1), 240-245.
[http://dx.doi.org/10.1128/JB.140.1.240-245.1979] [PMID: 500557]
[41]
Keune, H.; Sahm, H.; Wagner, F. Production of L-serine by the methano utilizing bacterium, Pseudomonas 3ab. Eur. J. Appl. Microbiol. Biotechnol., 1976, 2(3), 175-184.
[http://dx.doi.org/10.1007/BF00930878]
[42]
Heptinstall, J.; Quayle, J.R. Pathways leading to and from serine during growth of Pseudomonas AM1 on C1 compounds or succinate. Biochem. J., 1970, 117(3), 563-572.
[http://dx.doi.org/10.1042/bj1170563] [PMID: 4315933]
[43]
Goodwin, G.W.; Rougraff, P.M.; Davis, E.J.; Harris, R.A. Purification and characterization of methylmalonate-semialdehyde dehydrogenase from rat liver. Identity to malonate-semialdehyde dehydrogenase. J. Biol. Chem., 1989, 264(25), 14965-14971.
[PMID: 2768248]
[44]
Tchigvintsev, A.; Singer, A.; Brown, G.; Flick, R.; Evdokimova, E.; Tan, K.; Gonzalez, C.F.; Savchenko, A.; Yakunin, A.F. Biochemical and structural studies of uncharacterized protein PA0743 from Pseudomonas aeruginosa revealed NAD+-dependent L-serine dehydrogenase. J. Biol. Chem., 2012, 287(3), 1874-1883.
[http://dx.doi.org/10.1074/jbc.M111.294561] [PMID: 22128181]
[45]
Yasuda, M.; Nagata, S.; Yamane, S.; Kunikata, C.; Kida, Y.; Kuwano, K.; Suezawa, C.; Okuda, J. Pseudomonas aeruginosa serA gene is required for bacterial translocation through Caco-2 cell monolayers. PLoS One, 2017, 12(1)e0169367
[http://dx.doi.org/10.1371/journal.pone.0169367] [PMID: 28046014]
[46]
Stanier, R.Y.; Palleroni, N.J.; Doudoroff, M. The aerobic pseudomonads a taxonomic study. Microbiology, 1966, 43(2), 159-271.
[47]
Castric, P.A. Glycine metabolism by Pseudomonas aeruginosa: Hydrogen cyanide biosynthesis. J. Bacteriol., 1977, 130(2), 826-831.
[http://dx.doi.org/10.1128/JB.130.2.826-831.1977] [PMID: 233722]
[48]
Bowyer, A.; Mikolajek, H.; Wright, J.N.; Coker, A.; Erskine, P.T.; Cooper, J.B.; Bashir, Q.; Rashid, N.; Jamil, F.; Akhtar, M. Crystallization and preliminary X-ray diffraction analysis of L-Threonine Dehydrogenase (TDH) from the Hyperthermophilic archae on Thermococcus kodakaraensis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2008, 64(Pt 9), 828-830.
[http://dx.doi.org/10.1107/S1744309108025384] [PMID: 18765916]
[49]
Koodie, L.; Dhople, A.M. Acid tolerance of Escherichia coli O157: H7 and its survival in apple juice. Microbios, 2001, 104(409), 167-175.
[PMID: 11327111]
[50]
Salmond, C.V.; Kroll, R.G.; Booth, I.R. The effect of food preservatives on pH homeostasis in Escherichia coli. J. Gen. Microbiol.,, 1984, 130(11), 2845-2850.
[http://dx.doi.org/10.1099/00221287-130-11-2845] [PMID: 6396375]
[51]
Stratford, M.; Plumridge, A.; Archer, D.B. Decarboxylation of sorbic acid by spoilage yeasts is associated with the PAD1 gene. Appl. Environ. Microbiol., 2007, 73(20), 6534-6542.
[http://dx.doi.org/10.1128/AEM.01246-07] [PMID: 17766451]
[52]
Lu, H.J.; Breidt, F., Jr; Pérez-Díaz, I.M.; Osborne, J.A. Antimicrobial effects of weak acids on the survival of Escherichia coli O157:H7 under anaerobic conditions J. Food Prot, 2011, 74(6), 893-898.
[http://dx.doi.org/10.4315/0362-028X.JFP-10-404] [PMID: 21669064]
[53]
Brandenburg, K.S.; Rodriguez, K.J.; McAnulty, J.F.; Murphy, C.J.; Abbott, N.L.; Schurr, M.J.; Czuprynski, C.J. Tryptophan inhibits biofilm formation by Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 2013, 57(4), 1921-1925.
[http://dx.doi.org/10.1128/AAC.00007-13] [PMID: 23318791]
[54]
Kolodkin-gal, I.; Romero, D.; Cao, S.; Clardy, J.; Kolter, R.; Losick, R. Introduction 2 the virtual vehicle system. Math. Model., 2010, 328(5978), 627-629.
[http://dx.doi.org/10.1126/science.1188628.D-Amino]
[55]
Gordon, G.L.; Doelle, H.W. Production of racemic lactic acid in Pediococcus cerevisiae cultures by two lactate dehydrogenases. J. Bacteriol., 1975, 121(2), 600-607.
[http://dx.doi.org/10.1128/JB.121.2.600-607.1975] [PMID: 234418]
[56]
Vogels, G.D.; Van der Drift, C. Degradation of purines and pyrimidines by microorganisms Bacteriol. Rev., 1976, 40(2), 403-468.
[http://dx.doi.org/10.1128/MMBR.40.2.403-468.1976] [PMID: 786256]
[57]
Chohnan, S.; Takamura, Y. Malonate decarboxylase in bacteria and its application for determination of intracellular Acyl-CoA thioesters. Microbes Environ., 2004, 19(3), 179-189.
[http://dx.doi.org/10.1264/jsme2.19.179]
[58]
Wolfe, J.B.; Ivler, D.; Rittenberg, S.C. Malonate oxidation by dry cells and cell-free extracts. J. Bacteriol., 1955, 69(3), 240-243.
[59]
Chen, H.Y.; Yuan, M.; Livermore, D.M. Mechanisms of resistance to β-lactam antibiotics amongst Pseudomonas aeruginosa isolates collected in the UK in 1993. J. Med. Microbiol., 1995, 43(4), 300-309.
[http://dx.doi.org/10.1099/00222615-43-4-300] [PMID: 7562993]
[60]
Orrett, F.A. Antimicrobial susceptibility survey of Pseudomonas aeruginosa strains isolated from clinical sources. J. Natl. Med. Assoc., 2004, 96(8), 1065-1069.
[PMID: 15303411]
[61]
Anil, C.; Shahid, R.M. Antimirobial susceptibility patterns of Pseudomonas aeruginosa clinical isolates at a tertiary care hospital in Kathmandu, Nepal. Asian J. Pharmaceut. Clin. Res., 2013, 6(3), 235-238.
[62]
Govan, J.R.; Harris, G.S. Pseudomonas aeruginosa and cystic fibrosis: Unusual bacterial adaptation and pathogenesis. Microbiol. Sci., 1986, 3(10), 302-308.
[PMID: 3155268]
[63]
Owlia, P.; Nosrati, R.; Alaghehbandan, R.; Lari, A.R. Antimicrobial susceptibility differences among mucoid and non-mucoid Pseudomonas aeruginosa isolates. GMS Hyg. Infect. Control, 2014, 9(2), Doc13.
[PMID: 25152858]
[64]
Lima, J.L.D.C.; Alves, L.R.; Jacomé, P.R.L.A.; Bezerra Neto, J.P.; Maciel, M.A.V.; Morais, M.M.C. Biofilm production by clinical isolates of Pseudomonas aeruginosa and structural changes in LasR protein of isolates non biofilm-producing. Braz. J. Infect. Dis., 2018, 22(2), 129-136.
[http://dx.doi.org/10.1016/j.bjid.2018.03.003] [PMID: 29601791]
[65]
Finlayson, E.A.; Brown, P.D. Comparison of antibiotic resistance and virulence factors in pigmented and non-pigmented Pseudomonas aeruginosa comparación de la resistencia antibiótica y los factores de virulencia En Las Pseudomonas aeruginosa. Pigmentadas y No Pigmentadas,, 2011, 60(876)
[66]
Nasimuddin, S.; Malaiyan, J.; Kandaswamy, M. A Study on antibiotic sensitivity pattern in biofilm positive and negative isolates of Pseudomonas aeruginosa isolated from clinical samples. J. Medical Sci. Clin. Res., 2016, 04(03), 9798-9801.
[http://dx.doi.org/10.18535/jmscr/v4i3.38]
[67]
Rodríguez-Baño, J.; Martí, S.; Soto, S.; Fernández-Cuenca, F.; Cisneros, J.M.; Pachón, J.; Pascual, A.; Martínez-Martínez, L.; McQueary, C.; Actis, L.A.; Vila, J. Spanish Group for the Study of Nosocomial Infections (GEIH). Biofilm formation in Acinetobacter baumannii: Associated features and clinical implications Clin. Microbiol. Infect.,, 2008, 14(3), 276-278.
[http://dx.doi.org/10.1111/j.1469-0691.2007.01916.x] [PMID: 18190568]
[68]
O’Neill, E.; Pozzi, C.; Houston, P.; Humphreys, H.; Robinson, D.A.; Loughman, A.; Foster, T.J.; O’Gara, J.P. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol., 2008, 190(11), 3835-3850.
[http://dx.doi.org/10.1128/JB.00167-08] [PMID: 18375547]
[69]
Whiteley, M.; Bangera, M.G.; Bumgarner, R.E.; Parsek, M.R.; Teitzel, G.M.; Lory, S.; Greenberg, E.P. Gene expression in Pseudomonas aeruginosa biofilms. Nature, 2001, 413(6858), 860-864.
[http://dx.doi.org/10.1038/35101627] [PMID: 11677611]
[70]
Mah, T.F. Biofilm-specific antibiotic resistance. Future Microbiol., 2012, 7(9), 1061-1072.
[http://dx.doi.org/10.2217/fmb.12.76] [PMID: 22953707]