Skip to main content
SpringerLink
Log in

Role of Alginate in Bacterial Biofilms

  • Chapter
  • First Online:
Alginates: Biology and Applications

Part of the book series: Microbiology Monographs ((MICROMONO,volume 13))

Abstract

The prevalence of obtaining alginate overproducing stains from lungs of patients with cystic fibrosis and since alginate is an epiphytic fitness and plant pathogenic virulence trait has promoted inquires into the biological function of alginate. Clues into the role of alginate have been revealed by exploring biofilm matrix composition and alginate biosynthesis regulation at the transcriptional and the posttranslational level. Thus, we are refining our appreciation of the types of environmental stressor that activate alginate production and how surface growth may be an important attribute necessary for alginate production. Alginate production likely occurs under conditions in which cues of environmental stresses and biofilm development processes are integrated into regulatory networks controlling alginate production in a fashion that promotes survival of biofilm residents.

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
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
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

  • Axtell CA, Beattie GA (2002) Construction and characterization of a proU-gfp transcriptional fusion that measures water availability in a microbial habitat. Appl Environ Microbiol 68:4604–4612

    Article  CAS  PubMed  Google Scholar 

  • 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 beta-lactamase and alginate production. Antimicrob Agents Chemother 48:1175–1187

    Article  CAS  PubMed  Google Scholar 

  • Bragonzi A, Worlitzsch D, Pier GB, Timpert P, Ulrich M, Hentzer M, Andersen JB, Givskov M, Conese M, Doring G (2005) Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J Infect Dis 192:410–419

    Article  PubMed  Google Scholar 

  • Burns JL, Gibson RL, McNamara S, Yim D, Emerson J, Rosenfeld M, Hiatt P, McCoy K, Castile R, Smith AL, Ramsey BW (2001) Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183:444–452

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chang WS, van de Mortel M, Nielsen L, Nino de Guzman G, Li X, Halverson LJ (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  CAS  PubMed  Google Scholar 

  • Ciofu O, Lee B, Johannesson M, Hermansen NO, Meyer P, Hoiby N, The Scandinavian Cystic Fibrosis Study C (2008) Investigation of the algT operon sequence in mucoid and non-mucoid Pseudomonas aeruginosa isolates from 115 Scandinavian patients with cystic fibrosis and in 88 in vitro non-mucoid revertants. Microbiology 154:103–113

    Article  CAS  PubMed  Google Scholar 

  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

    Article  CAS  PubMed  Google Scholar 

  • Cote GL, Krull LH (1988) Characterization of the exocellular polysaccharides from Azotobacter chroococcum. Carbohydr Res 181:143–152

    Article  CAS  Google Scholar 

  • Davies DG, Geesey GG (1995) Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl Environ Microbiol 61:860–867

    CAS  PubMed  Google Scholar 

  • Davies DG, Chakrabarty AM, Geesey GG (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59:1181–1186

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Fett WF, Dunn MF (1989) Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts. Plant Physiol 89:5–9

    Article  CAS  PubMed  Google Scholar 

  • Fett WF, Wijey C, Lifson ER (1992) Occurrence of alginate gene sequences among members of the pseudomonad rRNA homology groups I-IV. FEMS Microbiol Lett 78:151–157

    CAS  PubMed  Google Scholar 

  • Firoved AM, Deretic V (2003) Microarray analysis of global gene expression in mucoid Pseudomonas aeruginosa. J Bacteriol 185:1071–1081

    Article  CAS  PubMed  Google Scholar 

  • Firoved AM, Wood SR, Ornatowski W, Deretic V, Timmins GS (2004) Microarray analysis and functional characterization of the nitrosative stress response in nonmucoid and mucoid Pseudomonas aeruginosa. J Bacteriol 186:4046–4050

    Article  CAS  PubMed  Google Scholar 

  • Friedman L, Kolter R (2004a) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690

    Article  CAS  Google Scholar 

  • Friedman L, Kolter R (2004b) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457–4465

    Article  CAS  Google Scholar 

  • Gacesa P (1998) Bacterial alginate biosynthesis - recent progress and future prospects. Microbiology 144:1133–1143

    Article  CAS  PubMed  Google Scholar 

  • Galperin MY (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6:552–567

    Article  CAS  PubMed  Google Scholar 

  • Guvener ZT, Harwood CS (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66:1459–1473

    CAS  PubMed  Google Scholar 

  • Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M, Parsek MR (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183:5395–5401

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hoffmann N, Lee B, Hentzer M, Rasmussen TB, Song Z, Johansen HK, Givskov M, Hoiby N (2007) Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr(–/–) mice. Antimicrob Agents Chemother 51:3677–3687

    Article  CAS  PubMed  Google Scholar 

  • Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ (2004) Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186:4466–4475

    Article  CAS  PubMed  Google Scholar 

  • Keith LMW, Bender CL (1999) AlgT (σ22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181:7176–7184

    CAS  PubMed  Google Scholar 

  • Keith RC, Keith LMW, Hernandez-Guzman G, Uppalapati SR, Bender CL (2003) Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and non-host plants. Microbiology 149:1127–1138

    Article  CAS  PubMed  Google Scholar 

  • Kidambi SP, Sundin GW, Palmer DA, Chakrabarty AM, Bender CL (1995) Copper as a signal for alginate synthesis in Pseudomonas syringae pv. syringae. Appl Environ Microbiol 61:2172–2179

    CAS  PubMed  Google Scholar 

  • Laue H, Schenk A, Li H, Lambertsen L, Neu TR, Molin S, Ullrich MS (2006) Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152:2909–2918

    Article  CAS  PubMed  Google Scholar 

  • Learn DB, Brestel EP, Seetharama S (1987) Hypochlorite scavenging by Pseudomonas aeruginosa alginate. Infect Immun 55:1813–1818

    CAS  PubMed  Google Scholar 

  • Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65:1474–1484

    Article  CAS  PubMed  Google Scholar 

  • Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175:7512–7518

    CAS  PubMed  Google Scholar 

  • Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ (2006) Analysis of Pseudomonas aeruginosa conditional Psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188:8213–8221

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Lu H, Sprinkle A, Parsek MR, Wozniak DJ (2007) Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189:8353–8356

    Article  CAS  PubMed  Google Scholar 

  • Mai GT, McCormack JG, Seow WK, Pier GB, Jackson LA, Thong YH (1993a) Inhibition of adherence of mucoid Pseudomonas aeruginosa by alginase, specific monoclonal antibodies, and antibiotics. Infect Immun 61:4338–4343

    CAS  Google Scholar 

  • Mai GT, Seow WK, Pier GB, McCormack JG, Thong YH (1993b) Suppression of lymphocyte and neutrophil functions by Pseudomonas aeruginosa mucoid exopolysaccharide (alginate): reversal by physicochemical, alginase, and specific monoclonal antibody treatments. Infect Immun 61:559–564

    CAS  Google Scholar 

  • Mall M, Grubb BR, Harkema JR, O’Neal WK, Boucher RC (2004) Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10:487–493

    Article  CAS  PubMed  Google Scholar 

  • Martin DW, Schurr MJ, Yu H, Deretic V (1994) Analysis of promoters controlled by the putative sigma factor AlgU regulating conversion to mucoidy in Pseudomonas aeruginosa: relationship to σE and stress response. J Bacteriol 176:6688–6696

    CAS  PubMed  Google Scholar 

  • Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC (1998) Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95:1005–1015

    Article  CAS  PubMed  Google Scholar 

  • Matsui H, Verghese MW, Kesimer M, Schwab UE, Randell SH, Sheehan JK, Grubb BR, Boucher RC (2005) Reduced three-dimensional motility in dehydrated airway mucus prevents neutrophil capture and killing bacteria on airway epithelial surfaces. J Immunol 175:1090–1099

    CAS  PubMed  Google Scholar 

  • Matsui H, Wagner VE, Hill DB, Schwab UE, Rogers TD, Button B, Taylor RM, II, Superfine R, Rubinstein M, Iglewski BH, Boucher RC (2006) A physical linkage between cystic fibrosis airway surface dehydration and Pseudomonas aeruginosa biofilms. Proc Nat Acad Sci U S A 103:18131–18136

    Article  CAS  Google Scholar 

  • Matsukawa M, Greenberg EP (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186:4449–4456

    Article  CAS  PubMed  Google Scholar 

  • Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S (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  CAS  PubMed  Google Scholar 

  • Nivens DE, Ohman DE, Williams J, Franklin MJ (2001) Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J Bacteriol 183:1047–1057

    Article  CAS  PubMed  Google Scholar 

  • Pedersen SS, Espersen F, Hoiby N, Jensen T (1990) Immunoglobulin A and immunoglobulin G antibody responses to alginates from Pseudomonas aeruginosa in patients with cystic fibrosis. J Clin Microbiol 28:747–755

    CAS  PubMed  Google Scholar 

  • Pier GB, Boyer D, Preston M, Coleman FT, Llosa N, Mueschenborn-Koglin S, Theilacker C, Goldenberg H, Uchin J, Priebe GP, Grout M, Posner M, Cavacini L (2004) Human monoclonal antibodies to Pseudomonas aeruginosa alginate that protect against infection by both mucoid and nonmucoid strains. J Immunol 173:5671–5678

    CAS  PubMed  Google Scholar 

  • Ramphal R, Pier GB (1985) Role of Pseudomonas aeruginosa mucoid exopolysaccharide in adherence to tracheal cells. Infect Immun 47:1–4

    CAS  PubMed  Google Scholar 

  • Ramsey DM, Wozniak DJ (2005) Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol Microbiol 56:309–322

    Article  CAS  PubMed  Google Scholar 

  • Sarkisova S, Patrauchan MA, Berglund D, Nivens DE, Franklin MJ (2005) Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J Bacteriol 187:4327–4337

    Article  CAS  PubMed  Google Scholar 

  • Schnider-Keel U, Lejbølle KB, Baehler E, Haas D, Keel C (2001) The sigma factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHA0. Appl Environ Microbiol 67:5683–5693

    Article  CAS  PubMed  Google Scholar 

  • Schurr MJ, Yu H, Martínez-Salazar JM, Boucher JC, Deretic V (1996) Control of AlgU, a member of the σE-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol 178:4997–5004

    CAS  PubMed  Google Scholar 

  • Simpson JA, Smith SE, Dean RT (1989) Scavenging by alginate of free radicals released by macrophages. Free Radic Biol Med 6:347–353

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764

    Article  CAS  PubMed  Google Scholar 

  • Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Kharazmi A, Høiby N, Mathee K (2004) Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 53:679–690

    Article  CAS  PubMed  Google Scholar 

  • Suh S-J, Silo-Suh L, Woods DE, Hassett DJ, West SE, Ohman DE (1999) Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa. J Bacteriol 181:3890–3897

    CAS  PubMed  Google Scholar 

  • van de Mortel M, Halverson LJ (2004) Cell envelope components contributing to biofilm growth and survival of Pseudomonas putida in low-water-content habitats. Mol Microbiol 52:735–750

    Article  CAS  PubMed  Google Scholar 

  • Wood LF, Ohman DE (2006) Independent regulation of MucD, an HtrA-like protease in Pseudomonas aeruginosa, and the role of its proteolytic motif in alginate gene regulation. J Bacteriol 188:3134–3137

    Article  CAS  PubMed  Google Scholar 

  • Wood LF, Leech AJ, Ohman DE (2006) Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: roles of sigma (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62:412–426

    Article  CAS  PubMed  Google Scholar 

  • Wozniak DJ, Wyckoff TJO, Starkey M, Keyser R, Azadi P, O’Toole GA, Parsek MR (2003) Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci U S A 100:7907–7912

    Article  CAS  PubMed  Google Scholar 

  • Wright CA, Beattie GA (2004) Pseudomonas syringae pv. tomato cells encounter inhibitory levels of water stress during the hypersensitive response of Arabidopsis thaliana. Proc Natl Acad Sci U S A 101:3269–3274

    Article  CAS  PubMed  Google Scholar 

  • Xie ZD, Hershberger CD, Shankar S, Ye RW, Chakrabarty AM (1996) Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J Bacteriol 178:4990–4996

    CAS  PubMed  Google Scholar 

  • Yu H, Schurr MJ, Deretic V (1995) Functional equivalence of Escherichia coli σE and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa. J Bacteriol 177:3259–3268

    CAS  PubMed  Google Scholar 

  • Yu J, Peñaloza-Vázquez A, Chakrabarty AM, Bender CL (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33:712–720

    Article  CAS  PubMed  Google Scholar 

  • Zielinski NA, Chakrabarty AM, Berry A (1991) Characterization and regulation of the Pseudomonas aeruginosa algC gene encoding phosphomannomutase. J Biol Chem 266:9754–9763

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author is indebted to the many thoughtful discussions with colleagues that contributed to the ideas expressed in this chapter. I also acknowledge the financial support provided by the US National Science Foundation and Department of Agriculture to pursue our interest in how water availability influences bacterial alginate production.

Author information

Authors and Affiliations

  1. Department of Plant Pathology, Iowa State University, Ames, IA, 50011, USA

    Larry J. Halverson

Authors
  1. Larry J. Halverson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Larry J. Halverson .

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and permissions

    Copyright information

    © 2009 Springer-Verlag Berlin Heidelberg

    About this chapter

    Cite this chapter

    Halverson, L.J. (2009). Role of Alginate in Bacterial Biofilms. In: Rehm, B. (eds) Alginates: Biology and Applications. Microbiology Monographs, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-92679-5_6

    Download citation

    Publish with us

    Policies and ethics

    Search

    Navigation