Skip to main content

Advertisement

SpringerLink
Log in

Bacterial alginates: from biosynthesis to applications

  • Review
  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Alginate is a polysaccharide belonging to the family of linear (unbranched), non-repeating copolymers, consisting of variable amounts of β-d-mannuronic acid and its C5-epimer α- l-guluronic acid linked via β-1,4-glycosidic bonds. Like DNA, alginate is a negatively charged polymer, imparting material properties ranging from viscous solutions to gel-like structures in the presence of divalent cations. Bacterial alginates are synthesized by only two bacterial genera, Pseudomonas and Azotobacter, and have been extensively studied over the last 40 years. While primarily synthesized in form of polymannuronic acid, alginate undergoes chemical modifications comprising acetylation and epimerization, which occurs during periplasmic transfer and before final export through the outer membrane. Alginate with its unique material properties and characteristics has been increasingly considered as biomaterial for medical applications. The genetic modification of alginate producing microorganisms could enable biotechnological production of new alginates with unique, tailor-made properties, suitable for medical and industrial applications.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aarons SJ, Sutherland IW, Chakrabarty AM, Gallagher MP (1997) A novel gene, algK, from the alginate biosynthesis cluster of Pseudomonas aeruginosa. Microbiology 143(Pt 2):641–652

    PubMed  CAS  Google Scholar 

  • Akama H, Matsuura T, Kashiwagi S, Yoneyama H, Narita S, Tsukihara T, Nakagawa A, Nakae T (2004) Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J Biol Chem 279(25):25939–25942

    Article  PubMed  CAS  Google Scholar 

  • Albrecht MT, Schiller NL (2005) Alginate lyase (AlgL) activity is required for alginate biosynthesis in Pseudomonas aeruginosa. J Bacteriol 187(11):3869–3872

    Article  PubMed  CAS  Google Scholar 

  • Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22(1):3–6

    Article  PubMed  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(24):8375–8384

    Article  PubMed  CAS  Google Scholar 

  • Bjerkan TM, Lillehov BE, Strand WI, Skjåk-Bræk G, Valla S, Ertesvåg H (2004) Construction and analyses of hybrid Azotobacter vinelandii mannuronan C-5 epimerases with new epimerization pattern characteristics. Biochem J 381(Pt 3):813–821

    PubMed  CAS  Google Scholar 

  • Boyd A, Ghosh M, May TB, Shinabarger D, Keogh R, Chakrabarty AM (1993) Sequence of the algL gene of Pseudomonas aeruginosa and purification of its alginate lyase product. Gene 131(1):1–8

    Article  PubMed  CAS  Google Scholar 

  • Campos M, Martinez-Salazar JM, Lloret L, Moreno S, Nunez C, Espin G, Soberon-Chavez G (1996) Characterization of the gene coding for GDP-mannose dehydrogenase (algD) from Azotobacter vinelandii. J Bacteriol 178(7):1793–1799

    PubMed  CAS  Google Scholar 

  • Chitnis CE, Ohman DE (1990) Cloning of Pseudomonas aeruginosa algG, which controls alginate structure. J Bacteriol 172(6):2894–2900

    PubMed  CAS  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(3):583–593

    PubMed  CAS  Google Scholar 

  • Costerton JW (2001) Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 9(2):50–52

    Article  PubMed  CAS  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193

    Article  PubMed  CAS  Google Scholar 

  • Ertesvåg H, Høidal HK, Schjerven H, Svanem BI, Valla S (1999) Mannuronan C-5-epimerases and their application for in vitro and in vivo design of new alginates useful in biotechnology. Metab Eng 1(3):262–269

    Article  PubMed  Google Scholar 

  • Favre-Bonte S, Pache JC, Robert J, Blanc D, Pechere JC, van Delden C (2002) Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients. Microb Pathog 32(3):143–147

    Article  PubMed  CAS  Google Scholar 

  • Firoved AM, Deretic V (2003) Microarray analysis of global gene expression in mucoid Pseudomonas aeruginosa. J Bacteriol 185(3):1071–1081

    Article  PubMed  CAS  Google Scholar 

  • Franklin MJ, Ohman DE (1993) Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J Bacteriol 175(16):5057–5065

    PubMed  CAS  Google Scholar 

  • Franklin MJ, Ohman DE (1996) Identification of algI and algJ in the Pseudomonas aeruginosa alginate biosynthetic gene cluster which are required for alginate O acetylation. J Bacteriol 178(8):2186–2195

    PubMed  CAS  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(11):3000–3007

    Article  PubMed  CAS  Google Scholar 

  • Franklin MJ, Chitnis CE, Gacesa P, Sonesson A, White DC, Ohman DE (1994) Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase. J Bacteriol 176(7):1821–1830

    PubMed  CAS  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(14):4759– 4773

    Article  PubMed  CAS  Google Scholar 

  • Gacesa P, Russell NJ (1990) The structure and property of alginate. In: Pseudomonas infection and alginates. London, Chapman & Hall, pp 29–49

  • 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  PubMed  CAS  Google Scholar 

  • Goldberg JB, Hatano K, Pier GB (1993) Synthesis of lipopolysaccharide O side chains by Pseudomonas aeruginosa PAO1 requires the enzyme phosphomannomutase. J Bacteriol 175:1605–1611

    PubMed  CAS  Google Scholar 

  • Grabert E, Wingender J, Winkler UK (1990) An outer membrane protein characteristic of mucoid strains of Pseudomonas aeruginosa. FEMS Microbiol Lett 56(1–2):83–87

    Article  PubMed  CAS  Google Scholar 

  • Gutsche J, Remminghorst U, Rehm BHA (2006) Biochemical analysis of alginate biosynthesis protein AlgX from Pseudomonas aeruginosa: purification of an AlgX-MucD (AlgY) protein complex. Biochimie 88(3–4):245–251

    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(2):95–108

    Article  PubMed  CAS  Google Scholar 

  • Høidal HK, Glaerum Svanem BI, Gimmestad M, Valla S (2000) Mannuronan C-5 epimerases and cellular differentiation of Azotobacter vinelandii. Environ Microbiol 2(1):27–38

    Article  PubMed  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(3):634–641

    PubMed  CAS  Google Scholar 

  • Jain S, Ohman DE (2005) Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect Immun 73(10):6429–6436

    Article  PubMed  CAS  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(4):1123–1133

    Article  PubMed  CAS  Google Scholar 

  • King A, Strand B, Rokstad AM, Kulseng B, Andersson A, Skjåk-Bræk G, Sandler S (2003) Improvement of the biocompatibility of alginate/poly-l-lysine/alginate microcapsules by the use of epimerized alginate as a coating. J Biomed Mater Res A 64(3):533–539

    Article  PubMed  CAS  Google Scholar 

  • Kulseng B, Skjåk-Bræk G, Ryan L, Andersson A, King A, Faxvaag A, Espevik T (1999) Transplantation of alginate microcapsules: generation of antibodies against alginates and encapsulated porcine islet-like cell clusters. Transplantation 67(7):978–984

    Article  PubMed  CAS  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-γ-mediated macrophage killing. J Immunol 175(11):7512–7518

    PubMed  CAS  Google Scholar 

  • Lin TY, Hassid WZ (1966) Pathway of alginic acid synthesis in the marine brown alga, Fucus gardneri Silva. J Biol Chem 241(22):5284–5297

    PubMed  CAS  Google Scholar 

  • Lloret L, Barreto R, Leon R, Moreno S, Martinez-Salazar J, Espin G, Soberon-Chavez G (1996) Genetic analysis of the transcriptional arrangement of Azotobacter vinelandii alginate biosynthetic genes: identification of two independent promoters. Mol Microbiol 21(3): 449–457

    PubMed  CAS  Google Scholar 

  • Mathee K, Sternberg C, Ciofu O, Jensen P, Campbell J, Givskov M, Ohman DE, Hoiby N, Molin S, 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

    PubMed  CAS  Google Scholar 

  • May TB, Shinabarger D, Boyd A, Chakrabarty AM (1994) Identification of amino acid residues involved in the activity of phosphomannose isomerase-guanosine 5′-diphospho-d-mannose pyrophosphorylase. A bifunctional enzyme in the alginate biosynthetic pathway of Pseudomonas aeruginosa. J Biol Chem 269(7):4872–4877

    PubMed  CAS  Google Scholar 

  • Mirshafiey A, Matsuo H, Nakane S, Rehm BHA, Koh CS, Miyoshi S (2005) Novel immunosuppressive therapy by M2000 in experimental multiple sclerosis. Immunopharmacol Immunotoxicol 27(2):255–265

    Article  PubMed  CAS  Google Scholar 

  • Monday SR, Schiller NL (1996) Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J Bacteriol 178(3):625–632

    PubMed  CAS  Google Scholar 

  • Moreno S, Najera R, Guzman J, Soberon-Chavez G, Espin G (1998) Role of alternative sigma factor algU in encystment of Azotobacter vinelandii. J Bacteriol 180(10):2766–2769

    PubMed  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(220–221):171–179

    PubMed  CAS  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(3):1047–1057

    Article  PubMed  CAS  Google Scholar 

  • Nyvall P, Corre E, Boisset C, Barbeyron T, Rousvoal S, Scornet D, Kloareg B, Boyen C (2003) Characterization of mannuronan C-5-epimerase genes from the brown alga Laminaria digitata. Plant Physiol 133(2):726–735

    Article  PubMed  CAS  Google Scholar 

  • Olvera C, Goldberg JB, Sanchez R, Soberon-Chavez G (1999) The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol Lett 179(1):85–90

    Article  PubMed  CAS  Google Scholar 

  • Pandey R, Khuller GK (2004) Chemotherapeutic potential of alginate-chitosan microspheres as anti-tubercular drug carriers. J Antimicrob Chemother 53(4):635–640

    Article  PubMed  CAS  Google Scholar 

  • Rehm BHA (1996) The Azotobacter vinelandii gene algJ encodes an outer membrane protein presumably involved in export of alginate. Microbiology 142:873–880

    PubMed  CAS  Google Scholar 

  • Rehm BHA (2005) Biosynthesis and applications of alginates. In: Francis T (ed) Encyclopedia of biomaterials and biomedical engineering, vol 1, pp 1–9

  • Rehm BHA, Valla S (1997) Bacterial alginates: biosynthesis and applications. Appl Microbiol Biotechnol 48(3):281–288

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Rehm BHA, Ertesvåg H, Valla S (1996) A new Azotobacter vinelandii mannuronan C-5-epimerase gene (algG) is part of an alg gene cluster physically organized in a manner similar to that in Pseudomonas aeruginosa. J Bacteriol 178(20):5884–5889

    PubMed  CAS  Google Scholar 

  • Rehm BHA, Grabert E, Hein J, Winkler UK (1994b) Antibody response of rabbits and cystic fibrosis patients to an alginate-specific outer membrane protein of a mucoid strain of Pseudomonas aeruginosa. Microb Pathog 16(1):43–51

    Article  CAS  Google Scholar 

  • Remminghorst U, Rehm BHA (2006a) Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa. FEBS Lett (in press)

  • Remminghorst U, Rehm BHA (2006b) In vitro alginate polymerization and the functional role of Alg8 in alginate production by Pseudomonas aeruginosa. Appl Environ Microbiol 72(1):298–305

    Article  CAS  Google Scholar 

  • Richard A, Margaritis A (2004) Empirical modeling of batch fermentation kinetics for poly(glutamic acid) production and other microbial biopolymers. Biotechnol Bioeng 87(4):501–515

    Article  PubMed  CAS  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(21):7369–7377

    Article  PubMed  CAS  Google Scholar 

  • Rokstad AM, Kulseng B, Strand BL, Skjåk-Bræk G, Espevik T (2001) Transplantation of alginate microcapsules with proliferating cells in mice: capsular overgrowth and survival of encapsulated cells of mice and human origin. Ann NY Acad Sci 944: 216–225

    Article  PubMed  CAS  Google Scholar 

  • Römling U, Amikam D (2006) Cyclic di-GMP as a second messenger. Curr Opin Microbiol 9(2):218–228

    Article  PubMed  CAS  Google Scholar 

  • Salzig M, Rehm BHA (2006) Microbial production of alginates: self assembly and applications. In: Rehm BHA (ed) Microbial bionanotechnology: biological self-assembly systems and biopolymer-based nanostructures. Horizon Bioscience, pp 125–152

  • Saxena IM, Brown RM Jr (2000) Cellulose synthases and related enzymes. Curr Opin Plant Biol 3(6):523–531

    Article  PubMed  CAS  Google Scholar 

  • Saxena IM, Brown RM Jr, Dandekar T (2001) Structure–function characterization of cellulose synthase: relationship to other glycosyltransferases. Phytochemistry 57(7):1135–1148

    Article  PubMed  CAS  Google Scholar 

  • Saxena IM, Brown RM Jr, Fevre M, Geremia RA, Henrissat B (1995) Multidomain architecture of beta-glycosyl transferases: implications for mechanism of action. J Bacteriol 177(6):1419–1424

    PubMed  CAS  Google Scholar 

  • Schiller NL, Monday SR, Boyd CM, Keen NT, Ohman DE (1993) Characterization of the Pseudomonas aeruginosa alginate lyase gene (algL): cloning, sequencing, and expression in Escherichia coli. J Bacteriol 175(15):4780–4789

    PubMed  CAS  Google Scholar 

  • Schmitt-Andrieu L, Hulen C (1996) Alginates of Pseudomonas aeruginosa: a complex regulation of the pathway of biosynthesis. C R Acad Sci III 319(3): 153–160

    PubMed  CAS  Google Scholar 

  • Shankar S, Ye RW, Schlictman D, Chakrabarty AM (1995) Exopolysaccharide alginate synthesis in Pseudomonas aeruginosa: enzymology and regulation of gene expression. Adv Enzymol Relat Areas Mol Biol 70:221–255

    PubMed  CAS  Google Scholar 

  • Shinabarger D, May TB, Boyd A, Ghosh M, Chakrabarty AM (1993) Nucleotide sequence and expression of the Pseudomonas aeruginosa algF gene controlling acetylation of alginate. Mol Microbiol 9(5):1027–1035

    PubMed  CAS  Google Scholar 

  • Tatnell PJ, Russell NJ, Gacesa P (1994) GDP-mannose dehydrogenase is the key regulatory enzyme in alginate biosynthesis in Pseudomonas aeruginosa: evidence from metabolite studies. Microbiology 140(Pt 7):1745–1754

    Article  PubMed  CAS  Google Scholar 

  • Thomas S (2000) Alginate dressings in surgery and wound management – Part 1. J Wound Care 9(2):56–60

    PubMed  CAS  Google Scholar 

  • Trujillo-Roldan MA, Moreno S, Espin G, Galindo E (2004) The roles of oxygen and alginate-lyase in determining the molecular weight of alginate produced by Azotobacter vinelandii. Appl Microbiol Biotechnol 63(6):742–747

    Article  PubMed  CAS  Google Scholar 

  • Trujillo-Roldan MA, Moreno S, Segura D, Galindo E, Espin G (2003) Alginate production by an Azotobacter vinelandii mutant unable to produce alginate lyase. Appl Microbiol Biotechnol 60(6):733–737

    PubMed  CAS  Google Scholar 

  • Valla S, Li J, Ertesvåg H, Barbeyron T, Lindahl U (2001) Hexuronyl C5-epimerases in alginate and glycosaminoglycan biosynthesis. Biochimie 83(8):819–830

    Article  PubMed  CAS  Google Scholar 

  • Vazquez A, Moreno S, Guzman J, Alvarado A, Espin G (1999) Transcriptional organization of the Azotobacter vinelandii algGXLVIFA genes: characterization of algF mutants. Gene 232(2):217–222

    Article  PubMed  CAS  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(8):3134–3137

    Article  PubMed  CAS  Google Scholar 

  • Wu W, Badrane H, Arora S, Baker HV, Jin S (2004) MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J Bacteriol 186(22):7575–7585

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Molecular BioSciences, Massey University, Private Bag 11222, Palmerston North, New Zealand

    Uwe Remminghorst & Bernd H. A. Rehm

Authors
  1. Uwe Remminghorst
    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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Remminghorst, U., Rehm, B.H.A. Bacterial alginates: from biosynthesis to applications. Biotechnol Lett 28, 1701–1712 (2006). https://doi.org/10.1007/s10529-006-9156-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10529-006-9156-x

Keywords

Search

Navigation