Skip to main content
SpringerLink
Log in

Phenazines and Bacterial Biofilms

  • Chapter
  • First Online:
Microbial Phenazines

Abstract

Most bacteria in the environment exist in biofilms—structured, surface-attached multicellular communities that are enmeshed in a self-produced polysaccharide matrix. Biofilms allow bacteria to participate is social interactions, survive under harsh conditions and successfully resist antimicrobials, invasion by competitors, predation, and destruction by components of the immune system. Fluorescent Pseudomonas spp. are prolific biofilm formers and some members of the genus have become model organisms for the study of biofilm biology. Several economically important groups of pseudomonads produce phenazines, pigmented, redox-active metabolites that have long been recognized for their broad-spectrum antibiotic activity. The current chapter focuses on the emerging close link between phenazine production and biofilm formation in Pseudomonas spp., and on the important role of phenazines in biofilms associated with human infectious diseases and highly competitive environmental niches such as soil and the plant rhizosphere.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102:11076–11081

    Article  PubMed  CAS  Google Scholar 

  • Beatson SA, Whitchurch CB, Sargent JL et al (2002) Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184:3605–3613

    Article  PubMed  CAS  Google Scholar 

  • Berlutti F, Morea C, Battistoni A et al (2005) Iron availability influences aggregation, biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderia cenocepacia. Int J Immunopathol Pharmacol 18:661–670

    PubMed  CAS  Google Scholar 

  • Bordi C, de Bentzmann S (2011) Hacking into bacterial biofilms: a new therapeutic challenge. Ann Intensive Care 1:19

    Article  PubMed  Google Scholar 

  • Borlee BR, Goldman AD, Murakami K et al (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75:827–842

    Article  PubMed  CAS  Google Scholar 

  • Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72:612–632

    Article  PubMed  CAS  Google Scholar 

  • Brencic A, McFarland KA, McManus HR et al (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 73:434–445

    Article  PubMed  CAS  Google Scholar 

  • Buchan A, Crombie B, Alexandre GM (2010) Temporal dynamics and genetic diversity of chemotactic-competent microbial populations in the rhizosphere. Environ Microbiol 12:3171–3184

    Article  PubMed  CAS  Google Scholar 

  • Burmolle M, Webb JS, Rao D et al (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923

    Article  PubMed  Google Scholar 

  • Burrowes E, Baysse C, Adams C et al (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152:405–418

    Article  PubMed  CAS  Google Scholar 

  • Caldwell CC, Chen Y, Goetzmann HS et al (2009) Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol 175:2473–2488

    Article  PubMed  CAS  Google Scholar 

  • Cezairliyan B, Vinayavekhin N, Grenfell-Lee D et al (2013) Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog 9:e1003101

    Article  PubMed  CAS  Google Scholar 

  • Chang WS, Halverson LJ (2003) Reduced water availability influences the dynamics, development, and ultrastructural properties of Pseudomonas putida biofilms. J Bacteriol 185:6199–6204

    Article  PubMed  CAS  Google Scholar 

  • Chang WS, van de Mortel M, Nielsen L et al (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189:8290–8299

    Article  PubMed  CAS  Google Scholar 

  • Chang WS, Li XH, Halverson LJ (2009) Influence of water limitation on endogenous oxidative stress and cell death within unsaturated Pseudomonas putida biofilms. Environ Microbiol 11:1482–1492

    Article  PubMed  Google Scholar 

  • Coggan KA, Wolfgang MC (2012) Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr Issues Mol Biol 14:47–70

    PubMed  CAS  Google Scholar 

  • Croda-Garcia G, Grosso-Becerra V, Gonzalez-Valdez A et al (2011) Transcriptional regulation of Pseudomonas aeruginosa rhlR: role of the CRP orthologue Vfr (virulence factor regulator) and quorum-sensing regulators LasR and RhlR. Microbiology 157:2545–2555

    Article  PubMed  CAS  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422

    Article  PubMed  CAS  Google Scholar 

  • Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Davies DG, Parsek MR, Pearson JP et al (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298

    Article  PubMed  CAS  Google Scholar 

  • Denning GM, Wollenweber LA, Railsback MA et al (1998) Pseudomonas pyocyanin increases interleukin-8 expression by human airway epithelial cells. Infect Immun 66:5777–5784

    PubMed  CAS  Google Scholar 

  • Deziel E, Gopalan S, Tampakaki AP et al (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55:998–1014

    Article  PubMed  CAS  Google Scholar 

  • Dietrich LE, Kiley PJ (2011) A shared mechanism of SoxR activation by redox-cycling compounds. Mol Microbiol 79:1119–1122

    Article  PubMed  CAS  Google Scholar 

  • Dietrich LEP, Price-Whelan A, Petersen A et al (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61:1308–1321

    Article  PubMed  CAS  Google Scholar 

  • Dietrich LE, Okegbe C, Price-Whelan A et al (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195:1371–1380

    Article  PubMed  CAS  Google Scholar 

  • Dubern JF, Diggle SP (2008) Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol BioSyst 4:882–888

    Article  PubMed  CAS  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    PubMed  CAS  Google Scholar 

  • Fothergill JL, Panagea S, Hart CA et al (2007) Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol 7:45

    Article  PubMed  Google Scholar 

  • Friedheim EA (1931) Pyocyanine, an accessory respiratory enzyme. J Exp Med 54:207–221

    Article  PubMed  CAS  Google Scholar 

  • Girard G, van Rij ET, Lugtenberg BJ et al (2006) Regulatory roles of psrA and rpoS in phenazine-1-carboxamide synthesis by Pseudomonas chlororaphis PCL1391. Microbiology 152:43–58

    Article  PubMed  CAS  Google Scholar 

  • Gu M, Imlay JA (2011) The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol Microbiol 79:1136–1150

    Article  PubMed  CAS  Google Scholar 

  • Gulez G, Dechesne A, Workman CT et al (2012) Transcriptome dynamics of Pseudomonas putida KT2440 under water stress. Appl Environ Microbiol 78:676–683

    Article  PubMed  CAS  Google Scholar 

  • Ha DG, Merritt JH, Hampton TH et al (2011) 2-Heptyl-4-quinolone, a precursor of the Pseudomonas quinolone signal molecule, modulates swarming motility in Pseudomonas aeruginosa. J Bacteriol 193:6770–6780

    Article  PubMed  CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  PubMed  CAS  Google Scholar 

  • Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102:14422–14427

    Article  PubMed  CAS  Google Scholar 

  • Hilbi H, Weber SS, Ragaz C et al (2007) Environmental predators as models for bacterial pathogenesis. Environ Microbiol 9:563–575

    Article  PubMed  CAS  Google Scholar 

  • Hunter RC, Klepac-Ceraj V, Lorenzi MM et al (2012) Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am J Respir Cell Mol Biol 47:738–745

    Article  PubMed  CAS  Google Scholar 

  • Jacob C, Jamier V, Ba LA (2011) Redox active secondary metabolites. Curr Opin Chem Biol 15:149–155

    Article  PubMed  CAS  Google Scholar 

  • Jain R, Behrens AJ, Kaever V et al (2012) Type IV pilus assembly in Pseudomonas aeruginosa over a broad range of cyclic di-GMP concentrations. J Bacteriol 194:4285–4294

    Article  PubMed  CAS  Google Scholar 

  • Kay E, Humair B, Denervaud V et al (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188:6026–6033

    Article  PubMed  CAS  Google Scholar 

  • Koley D, Ramsey MM, Bard AJ et al (2011) Discovery of a biofilm electrocline using real-time 3D metabolite analysis. Proc Natl Acad Sci USA 108:19996–20001

    Article  PubMed  CAS  Google Scholar 

  • Kulasakara H, Lee V, Brencic A et al (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103:2839–2844

    Article  PubMed  Google Scholar 

  • Lapouge K, Schubert M, Allain FH et al (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67:241–253

    Article  PubMed  CAS  Google Scholar 

  • Lau GW, Goumnerov BC, Walendziewicz CL et al (2003) The Drosophila melanogaster Tol pathway participates in resistance to infection by the Gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun 71:4059–4066

    Article  PubMed  CAS  Google Scholar 

  • Lau GW, Hassett DJ, Ran HM et al (2004a) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599–606

    Article  PubMed  CAS  Google Scholar 

  • Lau GW, Ran HM, Kong FS et al (2004b) Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect Immun 72:4275–4278

    Article  PubMed  CAS  Google Scholar 

  • Lee VT, Matewish JM, Kessler JL et al (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65:1474–1484

    Article  PubMed  CAS  Google Scholar 

  • Lopez D, Vlamakis H, Kolter R (2010) Biofilms. Cold Spring Harb Perspect Biol 2:a000398

    PubMed  Google Scholar 

  • Lugtenberg BJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13

    Article  PubMed  CAS  Google Scholar 

  • Lugtenberg BJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490

    Article  PubMed  CAS  Google Scholar 

  • Maddula VS, Zhang Z, Pierson EA et al (2006) Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb Ecol 52:289–301

    Article  PubMed  CAS  Google Scholar 

  • Maddula VS, Pierson EA, Pierson LS (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J Bacteriol 190:2759–2766

    Article  PubMed  CAS  Google Scholar 

  • Mah TF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39

    Article  PubMed  CAS  Google Scholar 

  • Mahajan-Miklos S, Tan MW, Rahme LG et al (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa–Caenorhabditis elegans pathogenesis model. Cell 96:47–56

    Article  PubMed  CAS  Google Scholar 

  • Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36:893–916

    Article  PubMed  CAS  Google Scholar 

  • Manuel J, Selin C, Fernando WGD et al (2012) Stringent response mutants of Pseudomonas chlororaphis PA23 exhibit enhanced antifungal activity against Sclerotinia sclerotiorum in vitro. Microbiology 158:207–216

    Article  PubMed  CAS  Google Scholar 

  • Matz C, Webb JS, Schupp PJ et al (2008) Marine biofilm bacteria evade eukaryotic predation by targeted chemical defense. PLoS ONE 3:e2744

    Article  PubMed  Google Scholar 

  • Mavrodi DV, Bonsall RF, Delaney SM et al (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465

    Article  PubMed  CAS  Google Scholar 

  • Mavrodi DV, Peever TL, Mavrodi OV et al (2010) Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 76:866–879

    Article  PubMed  CAS  Google Scholar 

  • Mavrodi DV, Mavrodi OV, Parejko JA et al (2012a) Accumulation of the antibiotic phenazine-1-carboxylic acid in the rhizosphere of dryland cereals. Appl Environ Microbiol 78:804–812

    Article  PubMed  CAS  Google Scholar 

  • Mavrodi OV, Mavrodi DV, Parejko JA et al (2012b) Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl Environ Microbiol 78:3214–3220

    Article  PubMed  CAS  Google Scholar 

  • Mazzola M, Cook RJ, Thomashow LS et al (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624

    PubMed  CAS  Google Scholar 

  • McDougald D, Klebensberg J, Tolker-Nielsen T et al (2008) Pseudomonas aeruginosa: a model for biofilm formation. In: Rehm BHA (ed) Pseudomonas. Model organism, pathogen, cell factory. Wiley-VCH, Weinheim, pp 215–253

    Google Scholar 

  • Meissner A, Wild V, Simm R et al (2007) Pseudomonas aeruginosa cupA-encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ Microbiol 9:2475–2485

    Article  PubMed  CAS  Google Scholar 

  • Merighi M, Lee VT, Hyodo M et al (2007) The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65:876–895

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen H, Sivaneson M, Filloux A (2011) Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 13:1666–16681

    Article  PubMed  CAS  Google Scholar 

  • Nielsen L, Li X, Halverson LJ (2011) Cell-cell and cell-surface interactions mediated by cellulose and a novel exopolysaccharide contribute to Pseudomonas putida biofilm formation and fitness under water-limiting conditions. Environ Microbiol 13:1342–1356

    Article  PubMed  CAS  Google Scholar 

  • Or D, Smets BF, Wraith JM et al (2007) Physical constraints affecting bacterial habitats and activity in unsaturated porous media—a review. Adv Water Resour 30:1505–1527

    Article  Google Scholar 

  • Parejko JA, Mavrodi DV, Mavrodi OV et al (2012) Population structure and diversity of phenazine-1-carboxylic acid producing fluorescent Pseudomonas spp. from dryland cereal fields of central Washington State (USA). Microbial Ecol 63:226–241

    Article  Google Scholar 

  • Parejko JA, Mavrodi DV, Mavrodi OV et al (2013) Taxonomy and distribution of phenazine-producing Pseudomonas spp. in dryland agroecosystem of the Inland Pacific Northwest (U.S.). Appl Environ Microbiol 79:3887–3891

    Article  PubMed  CAS  Google Scholar 

  • Patriquin GM, Banin E, Gilmour C et al (2008) Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 190:662–671

    Article  PubMed  CAS  Google Scholar 

  • Pierson LS, Pierson EA (2010) Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 86:1659–1670

    Article  PubMed  CAS  Google Scholar 

  • Pirnay JP, Bilocq F, Pot B et al (2009) Pseudomonas aeruginosa population structure revisited. PLoS ONE 4:e7740

    Article  PubMed  Google Scholar 

  • Rahme LG, Tan MW, Le L et al (1997) Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc Natl Acad Sci USA 94:13245–13250

    Article  PubMed  CAS  Google Scholar 

  • Rahme LG, Ausubel FM, Cao H et al (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97:8815–8821

    Article  PubMed  CAS  Google Scholar 

  • Ramos I, Dietrich LE, Price-Whelan A et al (2010) Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res Microbiol 161:187–191

    Article  PubMed  CAS  Google Scholar 

  • Recinos DA, Sekedat MD, Hernandez A et al (2012) Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci USA 109:19420–19425

    Article  PubMed  CAS  Google Scholar 

  • Romling U (2012) Cyclic di-GMP, an established secondary messenger still speeding up. Environ Microbiol 14:1817–1829

    Article  PubMed  Google Scholar 

  • Sakuragi Y, Kolter R (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189:5383–5386

    Article  PubMed  CAS  Google Scholar 

  • Savchuk SC, Fernando DWG (1994) Effect of timing of application and population dynamics on the degree of biological control of Sclerotinia sclerotiorum by bacterial antagonists. FEMS Microbiol Ecol 49:379–388

    Article  Google Scholar 

  • Schillinger WF, Papendick RI (2008) Then and now: 125 years of dryland wheat farming in the Inland Pacific Northwest. Agronomy J 100:S166–S182

    Google Scholar 

  • Selezska K, Kazmierczak M, Musken M et al (2012) Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure. Environ Microbiol 14:1952–1967

    Article  PubMed  CAS  Google Scholar 

  • Selin C, Habibian R, Poritsanos N et al (2010) Phenazines are not essential for Pseudomonas chlororaphis PA23 biocontrol of Sclerotinia sclerotiorum, but do play a role in biofilm formation. FEMS Microbiol Ecol 71:73–83

    Article  PubMed  CAS  Google Scholar 

  • Shin JH, Singh AK, Cheon DJ et al (2011) Activation of the SoxR regulon in Streptomyces coelicolor by the extracellular form of the pigmented antibiotic actinorhodin. J Bacteriol 193:75–81

    Article  PubMed  CAS  Google Scholar 

  • Smith RS, Wolfgang MC, Lory S (2004) An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect Immun 72:1677–1684

    Article  PubMed  CAS  Google Scholar 

  • Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210

    Article  PubMed  CAS  Google Scholar 

  • Stoodley P, Sauer K, Davies DG et al (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  PubMed  CAS  Google Scholar 

  • Trutko SM, Garagulia AD, Kiprianova EA et al (1988) The physiological role of pyocyanine synthesized by Pseudomonas aeruginosa. Mikrobiologiia 57:957–964

    PubMed  CAS  Google Scholar 

  • Vesper SJ (1987) Production of pili (fimbriae) by Pseudomonas fluorescens and correlation with attachment to corn roots. Appl Environ Microbiol 53:1397–1405

    PubMed  CAS  Google Scholar 

  • Wang Y, Newman DK (2008) Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol 42:2380–2386

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wilks JC, Danhorn T et al (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193:3606–3617

    Article  PubMed  CAS  Google Scholar 

  • Wei Q, Tarighi S, Dotsch A et al (2011) Phenotypic and genome-wide analysis of an antibiotic-resistant small colony variant (SCV) of Pseudomonas aeruginosa. PLoS ONE 6:e29276

    Article  PubMed  CAS  Google Scholar 

  • Whiteley M, Lee KM, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13904–13909

    Article  PubMed  CAS  Google Scholar 

  • Wiehlmann L, Wagner G, Cramer N et al (2007) Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 104:8101–8106

    Article  PubMed  CAS  Google Scholar 

  • Wilson R, Sykes DA, Watson D et al (1988) Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun 56:2515–2517

    PubMed  CAS  Google Scholar 

  • Wolfgang MC, Lee VT, Gilmore ME et al (2003) Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4:253–263

    Article  PubMed  CAS  Google Scholar 

  • Xiao G, Deziel E, He J et al (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors’ research was supported in part by USDA-NRI Grant 2011-67019-30212 from the USDA-NIFA Soil Processes program. The authors thank Drs. Olga Mavrodi, David Weller, and Linda Thomashow for critical review of the manuscript and helpful comments.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, The University of Southern Mississippi, Hattiesburg, MS, 39406, USA

    Dmitri V. Mavrodi

  2. BioTechnology Institute, University of Minnesota- Twin Cities, 1479 Gortner Avenue, St. Paul, MN, 55108-6106, USA

    James A. Parejko

Authors
  1. Dmitri V. Mavrodi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James A. Parejko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dmitri V. Mavrodi .

Editor information

Editors and Affiliations

  1. School of Life Sciences, Department of Microbiology, North Maharashtra University, Jalgaon, Maharashtra, India

    Sudhir Chincholkar

  2. Department of Plant Pathology, Washington State University, Pullman, Washington, USA

    Linda Thomashow

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Mavrodi, D.V., Parejko, J.A. (2013). Phenazines and Bacterial Biofilms. In: Chincholkar, S., Thomashow, L. (eds) Microbial Phenazines. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-40573-0_4

Download citation

Publish with us

Policies and ethics

Search

Navigation