Response of sessile cells to stress: from changes in gene expression to phenotypic adaptation
Tom Coenye
Laboratory of Pharmaceutical Microbiology, Ghent University, Gent, Belgium
Search for more papers by this authorTom Coenye
Laboratory of Pharmaceutical Microbiology, Ghent University, Gent, Belgium
Search for more papers by this authorEditor: Mark Shirtliff
Abstract
A better understanding of the genotypic and phenotypic adaptation of sessile (biofilm-associated) microorganisms to various forms of stress is required in order to develop more effective antibiofilm strategies. This review presents an overview of what high-throughput transcriptomic analyses have taught us concerning the response of various clinically relevant microorganisms (including Pseudomonas aeruginosa, Burkholderia cenocepacia and Candida albicans) to treatment with antibiotics or disinfectants. In addition, several problems associated with identifying gene expression patterns in biofilms in general and their implications for identifying the response to stress are discussed (with a focus on heterogeneity in microbial biofilms and the role of small RNAs in microbial group behavior).
References
- Agladze K, Jackson D & Romeo T (2003) Periodicity of cell attachment patterns during Escherichia coli biofilm development. J Bacteriol 185: 5632–5638.
- Anderson GA, Moreau-Marquis S, Stanton BA & O'Toole GA (2008) In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect Immun 76: 1423–1433.
- Andes D, Nett J, Oschel P, Albrecht R, Marchillo K & Pitula A (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72: 6023–6031.
- Bagge N, Schuster M, Hentzer M, Ciofu O, Givskov M, Greenberg EP & Hoiby N (2004) Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob Agents Ch 48: 1175–1187.
- Beggs WH (1994) Physicochemical cell damage in relation to lethal amphotericin B action. Antimicrob Agents Ch 38: 363–364.
- Beloin C & Ghigo JM (2005) Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 13: 16–19.
- Beloin C, Valle J, Latour-Lambert P et al. (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659–674.
- Boles BR, Thoendel M & Singh PK (2004) Self-generated diversity produces ‘insurance effects’ in biofilm communities. P Natl Acad Sci USA 101: 16630–16635.
- Brajtburg J, Powderly WG, Kobayashi GS & Medoff G (1990) Amphotericin B: current understanding of mechanisms of action. Antimicrob Agents Ch 34: 183–188.
- Bryan LE, Nicas T, Holloway BW & Crowther C (1980) Aminoglycoside-resistant mutation of Pseudomonas aeruginosa defective in cytochrome c552 and nitrate reductase. Antimicrob Agents Ch 17: 71–79.
- Calderone RA & Fonzi WA (2001) Virulence factors of Candida albicans. Trends Microbiol 9: 327–335.
- Coenye T & Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5: 719–729.
- Coenye T, Drevinek P, Mahenthiralingam E, Shah SA, Gill RT, Vandamme P & Ussery DW (2007) Identification of putative noncoding RNA genes in the Burkholderia cenocepacia J2315 genome. FEMS Microbiol Lett 276: 83–92.
- De Kievit TR, Parkins MD, Gillis RJ, Srikumar R, Ceri H, Poole K, Iglewski B & Storey DG (2001) Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Ch 45: 1761–1770.
- De Lay N & Gottesman S (2009) The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191: 461–476.
- Domka J, Lee J, Bansal T & Wood TK (2007) Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol 9: 332–346.
-
Donlan RM &
Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms.
Clin Microbiol Rev
15: 167–193.
10.1001/archinte.162.13.1483 Google Scholar
- Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11: 30–36.
- Drevinek P, Holden MT, Ge Z, Jones AM, Ketchell I, Gill RT & Mahenthiralingam E (2008) Gene expression changes linked to antimicrobial resistance, oxidative stress, iron depletion and retained motility are observed when Burkholderia cenocepacia grows in cystic fibrosis sputum. BMC Infect Dis 8: 121.
- Franz R, Kelly SL, Lamb DC, Kelly DE, Ruhnke M & Morschhäuser J (1998) Multiple molecular mechanisms contribute to a stepwise development of fluconazole resistance in clinical Candida albicans strains. Antimicrob Agents Ch 42: 3065–3072.
- Fux CA, Costerton JW, Stewart PS & Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13: 34–40.
- Gale EF (1986) Nature and development of phenotypic resistance to amphotericin B in Candida albicans. Adv Microb Physiol 27: 277–320.
- Garcia-Sanchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM & D'Enfert C (2004) Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3: 536–545.
- Gilbert P, Allison DG & McBain AJ (2002a) Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? J Appl Microbiol 92: 98S–110S.
- Gilbert P, Maira-Litran T, McBain AJ, Rickard AH & Whyte FW (2002b) The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol 46: 202–256.
- Gillis RJ, White KG, Choi KH, Wagner VE, Schweizer HP & Iglewski BH (2005) Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrob Agents Ch 49: 3858–3867.
- Hancock V & Klemm P (2007) Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun 75: 966–976.
- Henry KW, Nickels JT & Edlind TD (2000) Upregulation of ERG genes in Candida species by azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Ch 44: 2693–2700.
- Heurlier K, Williams F, Heeb S, Domrond C, Pzessi G, Singr D, Camara M, Williams P & Haas D (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186: 2936–2945.
- Hidalgo G, Burns A, Herz E, Hay AG, Houston PL, Wiesner U & Lion LW (2009) Functional tomographic fluorescence imaging of pH microenvironments in microbial biofilms by use of silica nanoparticle sensors. Appl Environ Microb 75: 7426–7435.
- Hoyer LL, Payne TL, Bell M, Myers AM & Scherer S (1998) Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet 33: 451–459.
- Hüttenhoffer A & Vogel J (2006) Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 34: 635–646.
- Ito A, May T, Kawata K & Okabe S (2008) Significance of irpoS during maturation of Escherichia coli biofilms. Biotech Bioeng 99: 1462–1471.
- Ito A, May T, Taniuchi A, Kawata K & Okabe S (2009a) Localized expression profiles of rpoS in Escherichia coli biofilms. Biotechnol Bioeng 103: 975–983.
- Ito A, Taniuchi A, May T, Kawata K & Okabe S (2009b) Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microb 75: 4093–4100.
- Jackson DW, Simecka JW & Romeo T (2002a) Catabolite repression of Escherichia coli biofilm formation. J Bacteriol 184: 3406–3410.
- Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME & Romeo T (2002b) Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184: 290–301.
- Junker LM, Toba FA & Hay AG (2007) Transcription in Escherichia coli PHL628 biofilms. FEMS Microbiol Lett 268: 237–243.
- Kay E, Humair B, Dénervaud V, Riedel K, Spahr S, Eberl L, Valverde C & Haas D (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188: 6026–6033.
- Khot PD, Suci PA, Miller RL, Nelson RD & Tyler BJ (2006) A small subpopulation of blastospores in Candida albicans biofilms exhibit resistance to amphotericin B associated with differential regulation of ergosterol and beta-1,6-glucan pathway genes. Antimicrob Agents Ch 50: 3708–3716.
- Kuhn DM & Ghannoum MA (2004) Candida biofilms: antifungal resistance and emerging therapeutic options. Curr Opin Investig D 5: 186–197.
- LaFleur MD, Kumamoto CA & Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Ch 50: 3839–3846.
- Lapouge K, Schubert M, Allain FHT & Haas D (2008) Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67: 241–253.
- Lazazzera B (2005) Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8: 222–227.
- Lenz AP, Williamson KS, Pitts B, Stewart PS & Franklin MJ (2008) Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microb 74: 4463–4471.
- Levine E, Zhang Z, Kuhlman T & Hwa T (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol 5: e229.
- Liu TT, Lee RE, Barker KS, Lee RE, Wei L, Homayouni R & Rogers PD (2005) Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Ch 49: 2226–2236.
- Lopez-Ribot JL, McAtee RK, Lee LN, Kirkpatrick WR, White TC, Sanglard D & Patterson TF (1998) Distinct patterns of gene expression associated with development of fluconazole resistance in serial Candida albicans isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis. Antimicrob Agents Ch 42: 2932–2937.
- Lucchetti-Miganeh C, Burrowes E, Baysse C & Ermel G (2008) The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154: 16–29.
- MacDonald KJ & Speert DP (2007) Interaction of Burkholderia species with the phagocytic system. Burkholderia: Molecular Microbiology and Genomics ( T Coenye & P Vandamme, eds), pp. 111–127. Horizon Bioscience, Norfolk.
- Mah TF & O'Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9: 34–39.
- Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS & O'Toole GA (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426: 306–310.
- Mahenthiralingam E, Baldwin A & Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104: 1539–1551.
- Marchais V, Kempf M, Licznar P, Lefrançois C, Bouchara JP, Robert R & Cottin J (2005) DNA array analysis of Candida albicans gene expression in response to adherence to polystyrene. FEMS Microbiol Lett 245: 25–32.
- Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24: 133–141.
- Martinez-Gomariz M, Perumal P, Mekala S, Nombela C, Chaffin WL & Gil C (2009) Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans. Proteomics 9: 2230–2252.
- Mateus C, Crow SA Jr & Ahearn DG (2004) Adherence of Candida albicans to silicone induces immediate enhanced tolerance to fluconazole. Antimicrob Agents Ch 48: 3358–3366.
- Mehta P, Goyal S & Wingreen NS (2008) A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 4: 221.
- Miller RV (2001) Environmental bacteriophage–host interactions: factors contributing to natural transduction. Antonie van Leeuwenhoek 79: 141–147.
- Mio T, Yamada-Okabe T, Yabe T, Nakajima T, Arisawa M & Yamada-Okabe H (1997) Isolation of the Candida albicans homologs of Saccharomyces cerevisiaeKRE6 and SKN1: expression and physiological function. J Bacteriol 179: 2363–2372.
- Mukherjee PK, Chandra J, Kuhn DM & Ghannoum MA (2003) Mechanisms of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 71: 4333–4340.
- Murillo LA, Newport G, Lan CY, Habelitz S, Dungan J & Agabian NM (2005) Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell 4: 1562–1573.
- Nailis H, Vandenbroucke R, Tilleman K, Deforce D, Nelis H & Coenye T (2009) Monitoring ALS1 and ALS3 gene expression during in vitroCandida albicans biofilm formation under continuous flow conditions. Mycopathologia 167: 9–17.
- Nailis H, Vandenbosch D, Deforce D, Nelis HJ & Coenye T (2010) Transcriptional response to fluconazole and amphotericin B in Candida albicans biofilms. Res Microbiol, doi:DOI: 10.1016/j.resmic.2010.02.004.
- Nett JE, Lepak AJ, Marchillo K & Andes DR (2009) Time course global gene expression analysis of an in vivoCandida biofilm. J Infect Dis 200: 307–313.
- Ochsner UA, Hassett DJ & Vasil ML (2001) Genetic and physiological characterization of ohr, encoding a protein involved in organic hydroperoxide resistance in Pseudomonas aeruginosa. J Bacteriol 183: 773–778.
- Ozsolak F, Platt AR, Jones DR, Reifenberger JG, Sass LE, McInerney P, Thompson JF, Bowers J, Jarosz M & Milos PM (2009) Direct RNA sequencing. Nature 461: 814–818.
- Panmanee W & Hassett DJ (2009) Differential role of OxyR-controlled antioxidant enzymes alkyl hydroperoxide reductase (AhpCF) and catalase (KatB) in the protection of Pseudomonas aeruginosa against hydrogen peroxide in biofilm vs. planktonic culture. FEMS Microbiol Lett 295: 238–244.
- Papenfort K & Vogel J (2009) Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res Microbiol 160: 278–287.
- Peeters E, Nelis HJ & Coenye T (2008) Evaluation of the efficacy of disinfection procedures against Burkholderia cenocepacia biofilms. J Hosp Infect 70: 361–368.
- Peeters E, Nelis HJ & Coenye T (2009) In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocyclin, tobramycin and co-trimoxazole on planktonic and sessile Burkholderia cepacia complex bacteria. J Antimicrob Chemoth 64: 801–809.
- Peeters E, Sass A, Mahenthiralingam E, Nelis HJ & Coenye T (2010) Transcriptional response of Burkholderia cenocepacia J2315 sessile cells to treatments with high doses of hydrogen peroxide and sodium hypochlorite. BMC Genomics 11: 90.
- Petterson E, Lundeberg J & Ahmadian A (2009) Generation of sequencing technologies. Genomics 93: 105–111.
- Ramage G, Bachmann S, Patterson TF, Wickes BL & Lopez-Ribot JL (2002) Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemoth 49: 973–980.
- Ren D, Bedzyk LA, Thomas SM, Ye RW & Wood TK (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biot 64: 515–524.
- Rogers PD & Barker KS (2003) Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob Agents Ch 47: 1220–1227.
- Romeo T (1998) Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29: 1321–1330.
- Sanglard D (2002) Resistance of human fungal pathogens to antifungal drugs. Curr Opin Microbiol 5: 379–385.
- Sauer K (2003) The genomics and proteomics of biofilm formation. Genome Biol 4: 219.
- Schembri MA, Kjaergaard K & Klemm P (2003) Gene expression in Escherichia coli biofilms. Mol Microbiol 48: 253–267.
- Schleheck D, Barraud N, Klebensberger J, Webb JS, McDougald D, Rice SA & Kjelleberg S (2009) Pseudomonas aeruginosa PAO1 preferentially grows as aggregates in liquid batch cultures and disperses upon starvation. PloS ONE 4: e5513.
- Seneviratne CJ, Wang Y, Jin L, Abiko Y & Samaranayake L (2008) Candida albicans biofilm formation is associated with increased anti-oxidative capacities. Proteomics 8: 2936–2947.
- Sharma CM & Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12: 536–546.
- Shendure J & Hanlee J (2008) Next-generation DNA sequencing. Nat Biotechnol 26: 1135–1145.
- Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, Biham O & Margalit H (2007) Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol Syst Biol 3: 138.
- Stanley NR, Britton RA, Grossman AD & Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185: 1951–1957.
- Stewart PS & Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358: 135–138.
- Stewart PS & Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6: 199–210.
- Sundstrom P (2002) Adhesion in Candida spp. Cell Microbiol 4: 461–469.
- Thomas DP, Bachmann SP & Lopez-Ribot JL (2006) Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6: 5795–5804.
- Vogel J (2009) A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 71: 1–11.
- Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P & Romeo T (2005) CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 56: 1648–1663.
- Waters LS & Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615–628.
- Webb JS, Lau M & Kjelleberg S (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186: 8066–8073.
- White TC (1997) Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob Agents Ch 41: 1482–1487.
- White TC, Marr KA & Bowden RA (1998) Clinical, cellular and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11: 382–402.
- White TC, Holleman S, Dy F, Mirels LF & Stevens DA (2002) Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob Agents Ch 46: 1704–1713.
- Whiteley M, Bangera MG, Bumgarner ME, Parsek MR, Teitzel GM, Lory S & Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413: 860–864.
- Wood TK (2009) Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11: 1–15.
- Yeater KM, Chandra J, Cheng G, Mukherjee PK, Zhao X, Rodriguez-Zas SL, Kwast KE, Ghannoum MA & Hoyer LL (2007) Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153: 2373–2385.
- Yoder-Himes DR, Chain PSG, Zhu Y, Wurtzel O, Rubin EM, Tiedje JM & Sorek R (2009) Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. P Natl Acad Sci USA 106: 3976–3981.
- Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M & Hube B (2007) In vivo transcript profiling of Candidaalbicans identifies a gene essential for interepithelial dissemination. Cell Microbiol 9: 2938–2954.
- Zhang L & Mah TF (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190: 4447–4452.
- Zhang XS, Garcia-Contreras R & Wood TK (2007) YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol 189: 3051–3062.
- Zheng M, Wang X, Templeton LJ, Smulski DR, Larossa RA & Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562–4570.