Skip to main content
SpringerLink
Log in
Book cover

Extracellular Sugar-Based Biopolymers Matrices pp 517–537Cite as

The Role of Alginate in Bacterial Biofilm Formation

  • Chapter
  • First Online:

Part of the book series: Biologically-Inspired Systems ((BISY,volume 12))

Abstract

Alginates are natural exopolysaccharides produced by seaweeds and bacteria belonging to the genera Pseudomonas and Azotobacter. These natural polymers are important polymeric substances contributing to the formation and development of biofilm matrixes of numerous bacteria enhancing persistence under environmental stresses, antibiotic treatment, and the immune system. Studying bacterial alginates have gained substantial attentions not only for their importance in bacterial pathogenesis but also regarding their biotechnological production for various industrial purposes. The biosynthesis of alginate is unique and has been extensively studied in the opportunistic human pathogen P. aeruginosa. This chapter will present updated data about bacterial production of alginate, its biological function, biosynthesis pathway, and regulation.

This is a preview of subscription content, 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   169.00
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

Learn about institutional subscriptions

References

  • Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the σ(E)-dependent extracytoplasmic stress response. Genes Dev 16:2156–2168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alkawash MA, Soothill JS, Schiller NL (2006) Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114:131–138

    Article  CAS  PubMed  Google Scholar 

  • Allsopp LP, Wood TE, Howard SA, Maggiorelli F, Nolan LM, Wettstadt S, Filloux A (2017) RsmA and AmrZ orchestrate the assembly of all three type VI secretion systems in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 114:7707–7712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker P, Ricer T, Moynihan PJ, Kitova EN, Walvoort MT, Little DJ, Whitney JC, Dawson K, Weadge JT, Robinson H, Ohman DE, Codée JD, Klassen JS, Clarke AJ, Howell PL (2014) P. aeruginosa SGNH hydrolase-like proteins AlgJ and AlgX have similar topology but separate and distinct roles in alginate acetylation. PLoS Pathog 10(8):e1004334

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bakkevig K, Sletta H, Gimmestad M, Aune R, Ertesvåg H, Degnes K, Christensen BE, Ellingsen TE, Valla S (2005) Role of the Pseudomonas fluorescens alginate lyase (AlgL) in clearing the periplasm of alginates not exported to the extracellular environment. J Bacteriol 187:8375–8384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baraquet C, Murakami K, Parsek MR, Harwood CS (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40:7207–7218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhagirath AY, Somayajula D, Li Y, Duan K (2017) CmpX affects virulence in Pseudomonas aeruginosa through the Gac/Rsm signaling pathway and by modulating c-di-GMP levels. J Membr Biol 251(1):35–49

    Article  PubMed  CAS  Google Scholar 

  • Boucher JC, Yu H, Mudd MH, Deretic V (1997) Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect Immun 65:3838–3846

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brencic A, McFarland KA, McManus HR, Castang S, Mogno I, Dove SL, Lory S (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Campa C, Holtan S, Nilsen N, Bjerkan TM, Stokke BT, Skjåk-Braek G (2004) Biochemical analysis of the processive mechanism for epimerization of alginate by mannuronan C-5 epimerase AlgE4. Biochem J 381:155–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cezairliyan BO, Sauer RT (2009) Control of P. aeruginosa AlgW protease cleavage of MucA by peptide signals and MucB. Mol Microbiol 72:368–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chambonnier G, Roux L, Redelberger D, Fadel F, Filloux A, Sivaneson M, de Bentzmann S, Bordi C (2016) The hybrid histidine kinase LadS forms a multicomponent signal transduction system with the GacS/GacA two-component system in Pseudomonas aeruginosa. PLoS Genet 12(5):e1006032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang W-S, 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  PubMed Central  Google Scholar 

  • Chitnis CE, Ohman DE (1993) Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure. Mol Microbiol 8:583–593

    Article  CAS  PubMed  Google Scholar 

  • Clementi F (1997) Alginate production by Azotobacter Vinelandii. Crit Rev Biotechnol 17:327–361

    Article  CAS  PubMed  Google Scholar 

  • Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GCL, Parsek MR (2011) The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog 7(1):e1001264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC, Ryder C, Howell PL, Wozniak DJ, Parsek MR (2012) The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 14:1913–1928

    Article  CAS  PubMed  Google Scholar 

  • Costerton JW (1999) Introduction to biofilm. Int J Antimicrob Agents 11:217–221

    Article  CAS  PubMed  Google Scholar 

  • Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    Article  CAS  PubMed  Google Scholar 

  • Damron FH, Yu HD (2011) Pseudomonas aeruginosa MucD regulates the alginate pathway through activation of MucA degradation via MucP proteolytic activity. J Bacteriol 193:286–291

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114

    Article  CAS  PubMed  Google Scholar 

  • Delben F, Cesaro À, Paoletti S, Crescenzi V (1982) Monomer composition and acetyl content as main determinants of the ionization behavior of alginates. Carbohydr Res 100:C46–C50

    Article  CAS  Google Scholar 

  • Diaz E, Mosovich LL, Neter E (1970) Serogroups of Pseudomonas aeruginosa and the immune response of patients with cystic fibrosis. J Infect Dis 121:269–274

    Article  CAS  PubMed  Google Scholar 

  • Doggett RG (1969) Incidence of mucoid Pseudomonas aeruginosa from clinical sources. Appl Microbiol 18:936–937

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doggett RG, Harrison GM, Stillwell NR, Wallis ES (1966) An atypical Pseudomonas aeruginosa associated with cystic fibrosis of the pancreas. J Pediatr 68:215–221

    Article  Google Scholar 

  • Doig P, Smith NR, Todd T, Irvin RT (1987) Characterization of the binding of Pseudomonas aeruginosa alginate to human epithelial cells. Infect Immun 55:1517–1522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Douthit SA, Dlakic M, Ohman DE, Franklin MJ (2005) Epimerase active domain of Pseudomonas aeruginosa AlgG, a protein that contains a right-handed beta-helix. J Bacteriol 187:4573–4583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elston HR, Hoffman KC (1967) Increasing incidence of encapsulated Pseudomonas aeruginosa strains. Am J Clin Pathol 48:519–523

    Article  CAS  PubMed  Google Scholar 

  • Ertesvåg H (2015) Alginate-modifying enzymes: biological roles and biotechnological uses. Front Microbiol 6:523. https://doi.org/10.3389/fmicb.2015.00523

    Article  PubMed  PubMed Central  Google Scholar 

  • Evans LR, Linker A (1973) Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol 116:915–924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Firoved AM, Boucher JC, Deretic V (2002) Global genomic analysis of AlgU (ςsgr;(E))-dependent promoters (sigmulon) in Pseudomonas aeruginosa and implications for inflammatory processes in cystic fibrosis. J Bacteriol 184:1057–1064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Franklin MJ, Ohman DE (2002) Mutant analysis and cellular localization of the AlgI, AlgJ, and AlgF proteins required for O acetylation of alginate in Pseudomonas aeruginosa. J Bacteriol 184:3000–3007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franklin MJ, Douthit SA, McClure MA (2004) Evidence that the algI/algJ gene cassette, required for O acetylation of Pseudomonas aeruginosa alginate, evolved by lateral gene transfer. J Bacteriol 186:4759–4773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fyfe JAM, Govan JRW (1978) A genetic approach to the study of mucoid Pseudomonas aeruginosa. Proc Soc Gen Microbiol 5:54

    Google Scholar 

  • Fyfe JA, Govan JR (1980) Alginate synthesis in mucoid Pseudomonas aeruginosa: a chromosomal locus involved in control. J Gen Microbiol 119:443–450

    CAS  PubMed  Google Scholar 

  • Gellatly SL, Hancock REW (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67:159–173

    Article  CAS  PubMed  Google Scholar 

  • Ghafoor A, Hay ID, Rehm BHA (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimmestad M, Sletta H, Ertesvåg H, Bakkevig K, Jain S, Suh S-j, Skjåk-Bræk G, Ellingsen TE, Ohman DE, Valla S (2003) The Pseudomonas fluorescens AlgG protein, but not its mannuronan C-5-epimerase activity, is needed for alginate polymer formation. J Bacteriol 185:3515–3523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimmestad M, Steigedal M, Ertesvåg H, Moreno S, Christensen BE, Espín G, Valla S (2006) Identification and characterization of an Azotobacter vinelandii type I secretion system responsible for export of the AlgE-type mannuronan C-5-epimerases. J Bacteriol 188:5551–5560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimmestad M, Ertesvåg H, Heggeset TM, Aarstad O, Svanem BI, Valla S (2009) Characterization of three new Azotobacter vinelandii alginate lyases, one of which is involved in cyst germination. J Bacteriol 191:4845–4853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorin P, Spencer J (1966) Exocellular alginic acid from Azotobacter vinelandii. Can J Chem 44:993–998

    Article  CAS  Google Scholar 

  • Govan JRW (1976) Genetic studies on mucoid Pseudomonas aeruginosa. Proc Soc Gen Microbiol 3:187

    Google Scholar 

  • Govan JR, Fyfe JA, Jarman TR (1981) Isolation of alginate-producing mutants of Pseudomonas fluorescens, Pseudomonas putida and Pseudomonas mendocina. J Gen Microbiol 125:217–220

    CAS  PubMed  Google Scholar 

  • Güvener 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

    PubMed  PubMed Central  Google Scholar 

  • Haug A, Smidsrod O (1967) Strontium–calcium selectivity of alginates. Nature 215:757

    Article  CAS  PubMed  Google Scholar 

  • Haug A, Larsen B (1969) Biosynthesis of alginate. Epimerisation of D-mannuronic to L-guluronic acid residues in the polymer chain. Biochim Biophys Acta 192:557–559

    Article  CAS  PubMed  Google Scholar 

  • Haug A, Smidsrod O (1970) Selectivity of some anionic polymers for divalent metal ions. Acta Chem Scand 24:843–854

    Article  CAS  Google Scholar 

  • Hay ID, Gatland K, Campisano A, Jordens JZ, Rehm BHA (2009a) Impact of alginate overproduction on attachment and biofilm architecture of a supermucoid Pseudomonas aeruginosa strain. Appl Environ Microbiol 75:6022–6025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hay ID, Remminghorst U, Rehm BH (2009b) MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 75:1110–1120

    Article  CAS  PubMed  Google Scholar 

  • Hay ID, Rehman ZU, Rehm BH (2010) Membrane topology of outer membrane protein AlgE, which is required for alginate production in Pseudomonas aeruginosa. Appl Environ Microbiol 76:1806–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hay ID, Schmidt O, Filitcheva J, Rehm BH (2012) Identification of a periplasmic AlgK-AlgX-MucD multiprotein complex in Pseudomonas aeruginosa involved in biosynthesis and regulation of alginate. Appl Microbiol Biotechnol 93:215–227

    Article  PubMed  CAS  Google Scholar 

  • Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH (2014) Genetics and regulation of bacterial alginate production. Environ Microbiol 16:2997–3011

    Article  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  PubMed Central  Google Scholar 

  • Higgins PG, Fluit AC, Milatovic D, Verhoef J, Schmitz FJ (2003) Mutations in GyrA, ParC, MexR and NfxB in clinical isolates of Pseudomonas aeruginosa. Int J Antimicrob Agents 21:409–413

    Article  CAS  PubMed  Google Scholar 

  • Hogardt M, Heesemann J (2010) Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 300:557–562

    Article  CAS  PubMed  Google Scholar 

  • Hogardt M, Heesemann J (2013) Microevolution of Pseudomonas aeruginosa to a chronic pathogen of the cystic fibrosis lung. Curr Top Microbiol Immunol 358:91–118

    CAS  PubMed  Google Scholar 

  • Høiby N (2017) A short history of microbial biofilms and biofilm infections. APMIS 125:272–275

    Article  PubMed  Google Scholar 

  • Irie Y, Starkey M, Edwards AN, Wozniak DJ, Romeo T, Parsek MR (2010) Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78:158–172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain S, Ohman DE (1998) Deletion of algK in mucoid Pseudomonas aeruginosa blocks alginate polymer formation and results in uronic acid secretion. J Bacteriol 180:634–641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain S, Ohman DE (2005) Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect Immun 73:6429–6436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain S, Franklin MJ, Ertesvåg H, Valla S, Ohman DE (2003) The dual roles of AlgG in C-5-epimerization and secretion of alginate polymers in Pseudomonas aeruginosa. Mol Microbiol 47:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I, Secor PR, Tseng BS, Scian M, Filloux A, Wozniak DJ, Howell PL, Parsek MR (2015) Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc Natl Acad Sci USA 112:11353–11358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65

    Article  CAS  PubMed  Google Scholar 

  • Keiski CL, Harwich M, Jain S, Neculai AM, Yip P, Robinson H, Whitney JC, Riley L, Burrows LL, Ohman DE, Howell PL (2010) AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure 18:265–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamppa JW, Griswold KE (2013) Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother 57:137–145

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Lee K, Lim EJ, Kim KS, Huang S-L, Veeranagouda Y, Rehm BHA (2014) An alginate-like exopolysaccharide biosynthesis gene cluster involved in biofilm aerial structure formation by Pseudomonas alkylphenolia. Appl Microbiol Biotechnol 98:4137–4148

    Article  CAS  PubMed  Google Scholar 

  • Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li K, Yang G, Debru AB, Li P, Zong L, Xu T, Wu W, Jin S, Bao Q (2017) SuhB regulates the motile-sessile switch in Pseudomonas aeruginosa through the Gac/Rsm pathway and c-di-GMP signaling. Front Microbiol 8:1045. https://doi.org/10.3389/fmicb.2017.01045

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Z, Chen JH, Hao Y, Nair SK (2012) Structures of the PelD cyclic diguanylate effector involved in pellicle formation in Pseudomonas aeruginosa PAO1. J Biol Chem 287:30191–30204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Y, de Kreuk M, van Loosdrecht MCM, Adin A (2010) Characterization of alginate-like exopolysaccharides isolated from aerobic granular sludge in pilot-plant. Water Res 44:3355–3364

    Article  CAS  PubMed  Google Scholar 

  • Lin YM, Sharma PK, van Loosdrecht MCM (2013) The chemical and mechanical differences between alginate-like exopolysaccharides isolated from aerobic flocculent sludge and aerobic granular sludge. Water Res 47:57–65

    Article  CAS  PubMed  Google Scholar 

  • Linker A, Jones RS (1964) A polysaccharide resembling alginic acid from a Pseudomonas microorganism. Nature 204:187–188

    Article  CAS  PubMed  Google Scholar 

  • Linker A, Jones RS (1966) A new polysaccharide resembling alginic acid isolated from pseudomonads. J Biol Chem 241:3845–3851

    CAS  PubMed  Google Scholar 

  • Mah T-FC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39

    Article  CAS  PubMed  Google Scholar 

  • Manilla-Pérez E, Reers C, Baumgart M, Hetzler S, Reichelt R, Malkus U, Kalscheuer R, Wältermann M, Steinbüchel A (2010) Analysis of lipid export in hydrocarbonoclastic bacteria of the genus Alcanivorax: identification of lipid export-negative mutants of Alcanivorax borkumensis SK2 and Alcanivorax jadensis T9. J Bacteriol 192:643–656

    Article  PubMed  CAS  Google Scholar 

  • Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JI, Jensen P, Johnsen AH, Givskov M, Ohman DE, Molin S, Høiby N, Kharazmi A (1999) Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145:1349–1357

    Article  CAS  PubMed  Google Scholar 

  • McEachran DW, Irvin RT (1985) Adhesion of Pseudomonas aeruginosa to human buccal epithelial cells: evidence for two classes of receptors. Can J Microbiol 31:563–569

    Article  CAS  PubMed  Google Scholar 

  • Meng S, Liu Y (2013) Alginate block fractions and their effects on membrane fouling. Water Res 47:6618–6627

    Article  CAS  PubMed  Google Scholar 

  • Merighi MT, Lee V, 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 

  • Moradali FM, Donati I, Sims IM, Ghods S, Rehm BH (2015) Alginate polymerization and modification are linked in Pseudomonas aeruginosa. MBio 6(3):e00453–e00415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moradali MF, Ghods S, Rehm BH (2017a) Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 7:39. https://doi.org/10.3389

    Google Scholar 

  • Moradali MF, Ghods S, Rehm BHA (2017b) Activation mechanism and cellular localization of membrane-anchored alginate polymerase in Pseudomonas aeruginosa. Appl Environ Microbiol 83(9):e03499–e03416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moradali MF, Ghods S, Rehm BHA (2018) Alginate biosynthesis and biotechnological production. In: Rehm BHA, Moradali MF (eds) Alginates and their biomedical applications. Springer series in biomaterials science and engineering, vol 11. Springer, Singapore

    Google Scholar 

  • Moresi M, Bruno M, Parente E (2004) Viscoelastic properties of microbial alginate gels by oscillatory dynamic tests. J Food Eng 64:179–186

    Article  Google Scholar 

  • Muhammadi, Ahmed N (2007) Genetics of bacterial alginate: alginate genes distribution, organization and biosynthesis in bacteria. Curr Genomics 8:191–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulet M, Sánchez D, Lalucat J, Lee K, García-Valdés E (2015) Pseudomonas alkylphenolica sp. Nov., a bacterial species able to form special aerial structures when grown on p-cresol. Int J Syst Evol Microbiol 65:4013–4018

    Article  CAS  PubMed  Google Scholar 

  • Mørch ÝA, Donati I, Strand BL (2006) Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules 7:1471–1480

    Article  PubMed  CAS  Google Scholar 

  • Müller JM, Monte Alegre R (2007) Alginate production by Pseudomonas mendocina in a stirred draft fermenter. World J Microbiol Biotechnol 23:691–695

    Article  CAS  Google Scholar 

  • Narbad A, Russell NJ, Gacesa P (1988) Radiolabelling patterns in alginate of Pseudomonas aeruginosa synthesized from specifically-labelled 14C-monosaccharide precursors. Microbios 54:171–179

    CAS  PubMed  Google Scholar 

  • Narbad A, Gacesa P, Russell NJ (1990) Biosynthesis of alginate. In: Gacesa P, Russell NJ (eds) Pseudomonas infection and alginates. Springer, Dordrecht

    Google Scholar 

  • Oglesby LL, Jain S, Ohman DE (2008) Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154:1605–1615

    Article  CAS  PubMed  Google Scholar 

  • Ohman DE, Chakrabarty AM (1981) Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect Immun 33:142–148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ouwerx C, Velings N, Mestdagh MM, Axelos MAV (1998) Physico-chemical properties and rheology of alginate gel beads formed with various divalent cations. Polym Gels Netw 6:393–408

    Article  CAS  Google Scholar 

  • Peteiro C (2018) Alginate production from marine macroalgae, with emphasis on kelp farming. In: Rehm BHA, Moradali MF (eds) Alginates and their biomedical applications. Springer series in biomaterials science and engineering, vol 11. Springer, Singapore

    Google Scholar 

  • Pier GB, Matthews WJ, Eardley DD (1983) Immunochemical characterization of the mucoid exopolysaccharide of Pseudomonas aeruginosa. J Infect Dis 147:494–503

    Article  CAS  PubMed  Google Scholar 

  • Qiu D, Eisinger VM, Rowen DW, Yu HD (2007) Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 104:8107–8112

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Rau MH, Hansen SK, Johansen HK, Thomsen LE, Workman CT, Nielsen KF, Jelsbak L, Høiby N, Yang L, Molin S (2010) Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ Microbiol 12:1643–1658

    CAS  PubMed  Google Scholar 

  • Rehm BH (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8:578–592

    Article  CAS  PubMed  Google Scholar 

  • Rehm BH, Valla S (1997) Bacterial alginates: biosynthesis and applications. Appl Microbiol Biotechnol 48:281–288

    Article  CAS  PubMed  Google Scholar 

  • Rehm BH, Boheim G, Tommassen J, Winkler UK (1994) Overexpression of algE in Escherichia coli: subcellular localization, purification, and ion channel properties. J Bacteriol 176:5639–5647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehman ZU, Wang Y, Moradali MF, Hay ID, Rehm BH (2013) Insights into the assembly of the alginate biosynthesis machinery in Pseudomonas aeruginosa. Appl Environ Microbiol 79:3264–3272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiling SA, Jansen JA, Henley BJ, Singh S, Chattin C, Chandler M, Rowen DW (2005) Prc protease promotes mucoidy in mucA mutants of Pseudomonas aeruginosa. Microbiology 151:2251–2261

    Article  CAS  PubMed  Google Scholar 

  • Remminghorst U, Rehm BH (2006a) Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa. FEBS Lett 580:3883–3888

    Article  CAS  PubMed  Google Scholar 

  • Remminghorst U, Rehm BH (2006b) Bacterial alginates: from biosynthesis to applications. Biotechnol Lett 28:1701–1712

    Article  CAS  PubMed  Google Scholar 

  • Remminghorst U, Hay ID, Rehm BH (2009) Molecular characterization of Alg8, a putative glycosyltransferase, involved in alginate polymerisation. J Biotechnol 140:176–183

    Article  CAS  PubMed  Google Scholar 

  • Reynolds HY, Di Sant’Agnese PA, Zierdt CH (1976) Mucoid Pseudomonas aeruginosa. A sign of cystic fibrosis in young adults with chronic pulmonary disease? JAMA 236:2190–2192

    Article  CAS  PubMed  Google Scholar 

  • Robles-Price A, Wong TY, Sletta H, Valla S, Schiller NL (2004) AlgX is a periplasmic protein required for alginate biosynthesis in Pseudomonas aeruginosa. J Bacteriol 186:7369–7377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roychoudhury S, May TB, Gill JF, Singh SK, Feingold DS, Chakrabarty AM (1989) Purification and characterization of guanosine diphospho-D-mannose dehydrogenase. A key enzyme in the biosynthesis of alginate by Pseudomonas aeruginosa. J Biol Chem 264:9380–9385

    CAS  PubMed  Google Scholar 

  • Ryan RP, Fouhy Y, Lucey JF, Dow JM (2006) Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J Bacteriol 188:8327–8334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sherbrock-Cox V, Russell NJ, Gacesa P (1984) The purification and chemical characterisation of the alginate present in extracellular material produced by mucoid strains of Pseudomonas aeruginosa. Carbohydr Res 135:147–154

    Article  CAS  PubMed  Google Scholar 

  • Sikorski P, Mo F, Skjåk-Bræk G, Stokke BT (2007) Evidence for egg-box-compatible interactions in calcium−alginate gels from fiber X-ray diffraction. Biomacromolecules 8:2098–2103

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Koehler B, Fett WF (1992) Effect of osmolarity and dehydration on alginate production by fluorescent pseudomonads. Curr Microbiol 25:335–339

    Article  CAS  Google Scholar 

  • Skjåk-Bræk G, Paoletti S, Gianferrara T (1989) Selective acetylation of mannuronic acid residues in calcium alginate gels. Carbohydr Res 185:119–129

    Article  Google Scholar 

  • Smidsrød O, Glover RM, Whittington SG (1973) The relative extension of alginates having different chemical composition. Carbohydr Res 27:107–118

    Article  Google Scholar 

  • Sonnenschein C (1927) Die mucosus form des Pyocyaneus-Bakteriums, bacterium pyocyaneum mucosum. Zentralblatt für Bakteriologie [Naturwiss] 104:365–373

    Google Scholar 

  • Stacey SD, Williams DA, Pritchett CL (2017) The Pseudomonas aeruginosa two-component regulator AlgR directly activates rsmA expression in a phosphorylation independent manner. J Bacteriol 199(18):e00048–e00017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanford E (1883) On align: a new substance obtained from some of the commoner species of marine algae. Chem News 47:254–257

    Google Scholar 

  • Stewart PS, William Costerton J (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138

    Article  CAS  PubMed  Google Scholar 

  • Straatmann A, Windhues T, Borchard W (2004) Effects of acetylation on thermodynamic properties of seaweed alginate in sodium chloride solutions. In: Lechner MD, Börger L (eds) Analytical ultracentrifugation VII. Springer, Berlin/Heidelberg, pp 26–30

    Chapter  Google Scholar 

  • Strempel N, Neidig A, Nusser M, Geffers R, Vieillard J, Lesouhaitier O, Brenner-Weiss G, Overhage J (2013) Human host defense peptide LL-37 stimulates virulence factor production and adaptive resistance in Pseudomonas aeruginosa. PLoS One 8(12):e82240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tavares IM, Leitão JH, Fialho AM, Sá-Correia I (1999) Pattern of changes in the activity of enzymes of GDP-D-mannuronic acid synthesis and in the level of transcription of algA, algC and algD genes accompanying the loss and emergence of mucoidy in Pseudomonas aeruginosa. Res Microbiol 150:105–116

    Article  CAS  PubMed  Google Scholar 

  • van der Hoek JP, de Fooij H, Struker A (2016) Wastewater as a resource: strategies to recover resources from Amsterdam’s wastewater. Resour Conserv Recycl 113(Suppl C):53–64

    Article  Google Scholar 

  • Wang Y, Hay ID, Rehman ZU, Rehm BH (2015) Membrane-anchored MucR mediates nitrate-dependent regulation of alginate production in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 99:7253–7265

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Moradali MF, Goudarztalejerdi A, Sims IM, Rehm BH (2016) Biological function of a polysaccharide degrading enzyme in the periplasm. Sci Rep 6:31249. https://doi.org/10.1038/srep31249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webber RE, Shull KR (2004) Strain dependence of the viscoelastic properties of alginate hydrogels. Macromolecules 37:6153–6160

    Article  CAS  Google Scholar 

  • Whitney JC, Hay ID, Li C, Eckford PD, Robinson H, Amaya MF, Wood LF, Ohman DE, Bear CE, Rehm BH, Howell PL (2011) Structural basis for alginate secretion across the bacterial outer membrane. Proc Natl Acad Sci USA 108:13083–13088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitney JC, Whitfield GB, Marmont LS, Yip P, Neculai AM, Lobsanov YD, Robinson H, Ohman DE, Howell PL (2015) Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa. J Biol Chem 290:12451–12462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams RJ, Govan JR (1973) Pyocine typing of mucoid strains of Pseudomonas aeruginosa isolated from children with cystic fibrosis. J Med Microbiol 6:409–412

    Article  CAS  PubMed  Google Scholar 

  • Winstanley C, O’Brien S, Brockhurst MA (2016) Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 24:327–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289–340

    Article  CAS  PubMed  Google Scholar 

  • Wood LF, Ohman DE (2009) Use of cell wall stress to characterize sigma 22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Mol Microbiol 72:183–201

    Article  CAS  PubMed  Google Scholar 

  • Wood LF, Ohman DE (2012) Identification of genes in the σ(22) regulon of Pseudomonas aeruginosa required for cell envelope homeostasis in either the planktonic or the sessile mode of growth. MBio 3(3):e00094–e00012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood RE, Boat TF, Doershuk CF (1976) Cystic fibrosis. Am Rev Respir Dis 113:833–878

    CAS  PubMed  Google Scholar 

  • Wozniak DJ, Sprinkle AB, Baynham PJ (2003) Control of Pseudomonas aeruginosa algZ expression by the alternative sigma factor AlgT. J Bacteriol 185:7297–7300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yorgey P, Rahme L, Tan MW, Ausubel F (2001) The roles of mucD and alginate in the virulence of Pseudomonas aeruginosa in plants, nematodes and mice. Mol Microbiol 41:1063–1076

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the current and former member of the Rehm research group for their invaluable contributions providing insights into alginate biosynthesis in bacteria.

Author information

Authors and Affiliations

  1. Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA

    M. Fata Moradali

  2. Centre for Cell Factories and Biopolymers, Griffith Institute for Drug Discovery, Griffith University, Brisbane, Australia

    Bernd H. A. Rehm

Authors
  1. M. Fata Moradali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernd H. A. Rehm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd H. A. Rehm .

Editor information

Editors and Affiliations

  1. Department of Entomology, The Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

    Ephraim Cohen

  2. School of Science and Technology, Institute of Biology – Molecular Biology, University of Siegen, Siegen, Germany

    Hans Merzendorfer

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Moradali, M.F., Rehm, B.H.A. (2019). The Role of Alginate in Bacterial Biofilm Formation. In: Cohen, E., Merzendorfer, H. (eds) Extracellular Sugar-Based Biopolymers Matrices. Biologically-Inspired Systems, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-030-12919-4_13

Download citation

Publish with us

Policies and ethics

Search

Navigation