Advertisement

Alginate Biosynthesis and Biotechnological Production

  • M. Fata Moradali
  • Shirin Ghods
  • Bernd H. A. RehmEmail author
Chapter
Part of the Springer Series in Biomaterials Science and Engineering book series (SSBSE, volume 11)

Abstract

Alginates are natural exopolysaccharides produced by seaweeds and bacteria belonging to the genera Pseudomonas and Azotobacter. Due to exhibiting unique physicochemical properties, they have been widely applied for various industrial purposes such as in food, agricultural, cosmetic, pharmaceutical, and biomedical industries. In the last two decades, they have found their way into the advanced pharmaceutical and biomedical applications, owing to their biocompatibility and non-toxicity as well as versatility in view of modifications. So far, algal alginates have been the sole commercialized products applied for various purposes, while the potential uses of bacterial alginates remain unharnessed. Importantly, algal and bacteria alginates differ substantially from each other with respect to their composition, modifications, molecular mass, viscoelastic properties, and polydispersity. Indeed, bacterial alginates may meet current needs in the field of advanced pharmaceutical and biomedical engineering. In this chapter, after a brief overview of alginate discovery, general properties, applications, and comparative assessment of algal and bacterial resources, current findings about the biosynthesis of alginates, mainly in bacteria, will be discussed. Furthermore, we will discuss the current understanding of alginate polymerizing and modifying enzymes and their structure-function relationship. Knowledge about alginate biosynthesis/modification enzymes provides foundation for rational design of cell factories for producing tailor-made alginates. As a conclusion, advanced understanding of alginate biosynthesis pathway and involved enzymes creates an opportunity for bioengineering and synthetic biology approaches toward the production of alginates exhibiting desired material properties suitable for pharmaceutical and biomedical applications.

Keywords

Alginate Seaweeds Pseudomonas Tailor-made alginate Pharmaceutical and biomedical developments 

Notes

Acknowledgment

This research was supported in part by the Deutsche Forschungsgemeinschaft (Germany) and Massey University (New Zealand). The authors are grateful to the current and former member of the Rehm research group for their invaluable contributions providing insight into alginate biosynthesis by bacteria.

References

  1. 1.
    Stanford ECC (1883) On align: a new substance obtained from some of the commoner species of marine algae. Chem News 47:254–257Google Scholar
  2. 2.
    Lesser MA (1947) Alginates in drugs and cosmetics. Drug Cosmet Ind 61(6):761–842Google Scholar
  3. 3.
    Woodward F (1951) The Scottish seaweed research association. J Mar Biol Assoc UK 29(03):719–725CrossRefGoogle Scholar
  4. 4.
    Steiner AB, McNeely WH (1951) Organic derivatives of alginic acid. Ind Eng Chem 43(9):2073–2077CrossRefGoogle Scholar
  5. 5.
    Krefting A (1896) An improved method of treating seaweed to obtain valuable products therefrom. Br Patent 11:538Google Scholar
  6. 6.
    Krefting A (1898) Axel krefting. Google PatentsGoogle Scholar
  7. 7.
    Atsuki K, Tomoda Y (1926) Studies on seaweeds of Japan I. The chemical constituents of Laminaria. J Soc Chem Ind Japan 29:509–517Google Scholar
  8. 8.
    Nelson WL, Cretcher LH (1929) The alginic acid from macrocystis pyrifera. J Am Chem Soc 51(6):1914–1922CrossRefGoogle Scholar
  9. 9.
    Nelson WL, Cretcher LH (1930) The isolation and identification of D-mannuronic acid lactone from the Macrocystis pyrifera. J Am Chem Soc 52(5):2130–2132CrossRefGoogle Scholar
  10. 10.
    Nelson WL, Cretcher LH (1932) The properties of D-mannuronic acid lactone. J Am Chem Soc 54(8):3409–3412CrossRefGoogle Scholar
  11. 11.
    Bird GM, Haas P (1931) On the nature of the cell wall constituents of Laminaria spp. Mannuronic acid. Biochem J 25(2):403CrossRefGoogle Scholar
  12. 12.
    Miwa T (1930) Alginic acid. J Chem Soc Japan 51:738–745Google Scholar
  13. 13.
    Schoeffel E, Link KP (1933) Isolation of α-and β, D-Mannuronic acid. J Biol Chem 100(2):397–405Google Scholar
  14. 14.
    Astbury W (1945) Structure of alginic acid. Nature 155:667–668CrossRefGoogle Scholar
  15. 15.
    Hirst E, Jones J, Jones WO (1939) Structure of alginic acid. Nature 143:857CrossRefGoogle Scholar
  16. 16.
    Fischer F, Dörfel H (1955) Die polyuronsäuren der braunalgen (Kohlenhydrate der Algen I). Hoppe-Seyler’s Zeitschrift für physiologische Chemie 302(1-2):186–203CrossRefGoogle Scholar
  17. 17.
    Linker A, Jones RS (1964) A polysaccharide resembling alginic acid from a Pseudomonas microorganism. Nature 204:187–188CrossRefGoogle Scholar
  18. 18.
    Linker A, Jones RS (1966) A new polysaccharide resembling alginic acid isolated from Pseudomonads. J Biol Chem 241(16):3845–3851Google Scholar
  19. 19.
    Gorin P, Spencer J (1966) Exocellular alginic acid from Azotobacter vinelandii. Can J Chem 44(9):993–998CrossRefGoogle Scholar
  20. 20.
    Govan JR, Fyfe JA, Jarman TR (1981) Isolation of alginate-producing mutants of Pseudomonas fluorescens, Pseudomonas putida and Pseudomonas mendocina. J Gen Microbiol 125(1):217–220Google Scholar
  21. 21.
    Clare K (1993) Algin. Ind Gums:105–143Google Scholar
  22. 22.
    Moradali MF, Donati I, Sims IM, Ghods S, Rehm BH (2015) Alginate polymerization and modification are linked in Pseudomonas aeruginosa. MBio 6(3):e00453-00415Google Scholar
  23. 23.
    Douthit SA, Dlakic M, Ohman DE, Franklin MJ (2005) Epimerase active domain of Pseudomonas aeruginosa AlgG, a protein that contains a right-handed β-helix. J Bacteriol 187(13):4573–4583CrossRefGoogle Scholar
  24. 24.
    SkjÅk-Bræk G, Paoletti S, Gianferrara T (1989) Selective acetylation of mannuronic acid residues in calcium alginate gels. Carbohydr Res 185(1):119–129CrossRefGoogle Scholar
  25. 25.
    Windhues T, Borchard W (2003) Effect of acetylation on physico-chemical properties of bacterial and algal alginates in physiological sodium chloride solutions investigated with light scattering techniques. Carbohydr Polym 52(1):47–52CrossRefGoogle Scholar
  26. 26.
    Mørch ÝA, Donati I, Strand BL, Skjåk-Bræk G (2006) Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules 7(5):1471–1480CrossRefGoogle Scholar
  27. 27.
    Haug A, Smidsrod O (1970) Selectivity of some anionic polymers for divalent metal ions. Acta Chem Scand 24(3):843–854CrossRefGoogle Scholar
  28. 28.
    Haug A, Smidsrød O (1967) Strontium–calcium selectivity of alginates. Nature 215(5102):757–757CrossRefGoogle Scholar
  29. 29.
    Ouwerx C, Velings N, Mestdagh M, Axelos M (1998) Physico-chemical properties and rheology of alginate gel beads formed with various divalent cations. Polym Gels Networks 6(5):393–408CrossRefGoogle Scholar
  30. 30.
    Braccini I, Pérez S (2001) Molecular basis of Ca2+-induced gelation in alginates and pectins: the egg-box model revisited. Biomacromolecules 2(4):1089–1096CrossRefGoogle Scholar
  31. 31.
    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(7):2098–2103CrossRefGoogle Scholar
  32. 32.
    Straatmann A, Windhues T, Borchard W (2004) Effects of acetylation on thermodynamic properties of seaweed alginate in sodium chloride solutions. In: Analytical ultracentrifugation VII. Springer, Berlin, pp 26–30CrossRefGoogle Scholar
  33. 33.
    Delben F, Cesaro A, Paoletti S, Crescenzi V (1982) Monomer composition and acetyl content as main determinants of the ionization behavior of alginates. Carbohydr Res 100(1):C46–C50CrossRefGoogle Scholar
  34. 34.
    Onsøyen E (1997) Alginates. In: Thickening and gelling agents for food. Springer, Boston, pp 22–44CrossRefGoogle Scholar
  35. 35.
    McHugh DJ (1987) Production, properties and uses of alginates. Production and utilization of products from commercial seaweeds. FAO Fish Tech Pap 288:58–115Google Scholar
  36. 36.
    Smith AM, Miri T (2010) 6 alginates in foods. Practical food rheology: an interpretive approach:113Google Scholar
  37. 37.
    Tønnesen HH, Karlsen J (2002) Alginate in drug delivery systems. Drug Dev Ind Pharm 28(6):621–630CrossRefGoogle Scholar
  38. 38.
    Skaugrud Ø, Hagen A, Borgersen B, Dornish M (1999) Biomedical and pharmaceutical applications of alginate and chitosan. Biotechnol Genet Eng Rev 16(1):23–40CrossRefGoogle Scholar
  39. 39.
    Bhattarai N, Li Z, Edmondson D, Zhang M (2006) Alginate-based nanofibrous scaffolds: structural, mechanical, and biological properties. Adv Mater 18(11):1463–1467CrossRefGoogle Scholar
  40. 40.
    Douglas KL, Piccirillo CA, Tabrizian M (2006) Effects of alginate inclusion on the vector properties of chitosan-based nanoparticles. J Control Release 115(3):354–361CrossRefGoogle Scholar
  41. 41.
    Cook W (1986) Alginate dental impression materials: chemistry, structure, and properties. J Biomed Mater Res 20(1):1–24CrossRefGoogle Scholar
  42. 42.
    Craig R (1988) Review of dental impression materials. Adv Dental Res 2(1):51–64CrossRefGoogle Scholar
  43. 43.
    Groves A, Lawrence J (1986) Alginate dressing as a donor site haemostat. Ann R Coll Surg Engl 68(1):27Google Scholar
  44. 44.
    Barnett S, Varley S (1987) The effects of calcium alginate on wound healing. Ann R Coll Surg Engl 69(4):153Google Scholar
  45. 45.
    Hrynyk M, Martins-Green M, Barron AE, Neufeld RJ (2012) Alginate-PEG sponge architecture and role in the design of insulin release dressings. Biomacromolecules 13(5):1478–1485CrossRefGoogle Scholar
  46. 46.
    Barbetta A, Barigelli E, Dentini M (2009) Porous alginate hydrogels: synthetic methods for tailoring the porous texture. Biomacromolecules 10(8):2328–2337CrossRefGoogle Scholar
  47. 47.
    Andersen T, Melvik JE, Gåserød O, Alsberg E, Christensen BE (2012) Ionically gelled alginate foams: physical properties controlled by operational and macromolecular parameters. Biomacromolecules 13(11):3703–3710CrossRefGoogle Scholar
  48. 48.
    Shin S-J, Park J-Y, Lee J-Y, Park H, Park Y-D, Lee K-B, Whang C-M, Lee S-H (2007) “On the fly” continuous generation of alginate fibers using a microfluidic device. Langmuir 23(17):9104–9108CrossRefGoogle Scholar
  49. 49.
    Daemi H, Barikani M, Barmar M (2013) Highly stretchable nanoalginate based polyurethane elastomers. Carbohydr Polym 95(2):630–636CrossRefGoogle Scholar
  50. 50.
    Senuma Y, Lowe C, Zweifel Y, Hilborn J, Marison I (2000) Alginate hydrogel microspheres and microcapsules prepared by spinning disk atomization. Biotechnol Bioeng 67(5):616–622CrossRefGoogle Scholar
  51. 51.
    Bodmeier R, Chen H, Paeratakul O (1989) A novel approach to the oral delivery of micro-or nanoparticles. Pharm Res 6(5):413–417CrossRefGoogle Scholar
  52. 52.
    Kierstan M, Bucke C (1977) The immobilization of microbial cells, subcellular organelles, and enzymes in calcium alginate gels. Biotechnol Bioeng 19(3):387–397CrossRefGoogle Scholar
  53. 53.
    Palmieri G, Giardina P, Desiderio B, Marzullo L, Giamberini M, Sannia G (1994) A new enzyme immobilization procedure using copper alginate gel: application to a fungal phenol oxidase. Enzym Microb Technol 16(2):151–158CrossRefGoogle Scholar
  54. 54.
    Fukushima Y, Okamura K, Imai K, Motai H (1988) A new immobilization technique of whole cells and enzymes with colloidal silica and alginate. Biotechnol Bioeng 32(5):584–594CrossRefGoogle Scholar
  55. 55.
    Zhang W, Zhang Z, Zhang Y (2011) The application of carbon nanotubes in target drug delivery systems for cancer therapies. Nanoscale Res Lett 6(1):555CrossRefGoogle Scholar
  56. 56.
    Barreto JA, O’Malley W, Kubeil M, Graham B, Stephan H, Spiccia L (2011) Nanomaterials: applications in cancer imaging and therapy. Adv Mater 23(12)Google Scholar
  57. 57.
    Serp D, Cantana E, Heinzen C, Von Stockar U, Marison I (2000) Characterization of an encapsulation device for the production of monodisperse alginate beads for cell immobilization. Biotechnol Bioeng 70(1):41–53CrossRefGoogle Scholar
  58. 58.
    Baruch L, Machluf M (2006) Alginate–chitosan complex coacervation for cell encapsulation: effect on mechanical properties and on long-term viability. Biopolymers 82(6):570–579CrossRefGoogle Scholar
  59. 59.
    Orive G, Hernandez R, Gascon A, Igartua M, Pedraz J (2003) Survival of different cell lines in alginate-agarose microcapsules. Eur J Pharm Sci 18(1):23–30CrossRefGoogle Scholar
  60. 60.
    Shapiro L, Cohen S (1997) Novel alginate sponges for cell culture and transplantation. Biomaterials 18(8):583–590CrossRefGoogle Scholar
  61. 61.
    de Vos P, Faas MM, Strand B, Calafiore R (2006) Alginate-based microcapsules for immunoisolation of pancreatic islets. Biomaterials 27(32):5603–5617CrossRefGoogle Scholar
  62. 62.
    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):978–984CrossRefGoogle Scholar
  63. 63.
    Li Z, Ramay HR, Hauch KD, Xiao D, Zhang M (2005) Chitosan–alginate hybrid scaffolds for bone tissue engineering. Biomaterials 26(18):3919–3928CrossRefGoogle Scholar
  64. 64.
    Kuo CK, Ma PX (2001) Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: part 1. Structure, gelation rate and mechanical properties. Biomaterials 22(6):511–521CrossRefGoogle Scholar
  65. 65.
    Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24(24):4337–4351CrossRefGoogle Scholar
  66. 66.
    Lee J, Cuddihy MJ, Kotov NA (2008) Three-dimensional cell culture matrices: state of the art. Tissue Eng B Rev 14(1):61–86CrossRefGoogle Scholar
  67. 67.
    Perka C, Spitzer RS, Lindenhayn K, Sittinger M, Schultz O (2000) Matrix-mixed culture: new methodology for chondrocyte culture and preparation of cartilage transplants. J Biomed Mater Res A 49(3):305–311CrossRefGoogle Scholar
  68. 68.
    Murphy WL, Mooney DJ (1999) Controlled delivery of inductive proteins, plasmid DNA and cells from tissue engineering matrices. J Periodontal Res 34(7):413–419CrossRefGoogle Scholar
  69. 69.
    Kwiatek MA, Roman S, Fareeduddin A, Pandolfino JE, Kahrilas PJ (2011) An alginate-antacid formulation (Gaviscon Double Action Liquid) can eliminate or displace the postprandial ‘acid pocket’ in symptomatic GERD patients. Aliment Pharmacol Ther 34(1):59–66CrossRefGoogle Scholar
  70. 70.
    Washington N (1990) Investigation into the barrier action of an alginate gastric reflux suppressant, liquid Gaviscon®. Drug Investig 2(1):23–30CrossRefGoogle Scholar
  71. 71.
    Andresen I-L, Smidsørod O (1977) Temperature dependence of the elastic properties of alginate gels. Carbohydr Res 58(2):271–279CrossRefGoogle Scholar
  72. 72.
    Indergaard M, Skjåk-Bræk G (1987) Characteristics of alginate from Laminaria digitata cultivated in a high-phosphate environment. In: Twelfth international seaweed symposium, Springer, pp 541–549Google Scholar
  73. 73.
    Kloareg B, Quatrano R (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol 26:259–315Google Scholar
  74. 74.
    Lin T-Y, Hassid W (1966) Pathway of alginic acid synthesis in the marine brown alga, Fucus gardneri Silva. J Biol Chem 241(22):5284–5297Google Scholar
  75. 75.
    Haug A, Larsen B (1969) Biosynthesis of alginate. Epimerisation of D-mannuronic to L-guluronic acid residues in the polymer chain. Biochim Biophy Acta Genl Subj 192(3):557–559CrossRefGoogle Scholar
  76. 76.
    Ryder C, Byrd M, Wozniak DJ (2007) Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 10(6):644–648CrossRefGoogle Scholar
  77. 77.
    Moradali MF, Ghods S, Rehm BHA (2017) Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 7:39CrossRefGoogle Scholar
  78. 78.
    Ghafoor A, Hay ID, Rehm BH (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77(15):5238–5246CrossRefGoogle Scholar
  79. 79.
    Clementi F (1997) Alginate production by Azotobacter vinelandii. Crit Rev Biotechnol 17(4):327–361CrossRefGoogle Scholar
  80. 80.
    Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464CrossRefGoogle Scholar
  81. 81.
    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):583–590CrossRefGoogle Scholar
  82. 82.
    Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH (2014) Genetics and regulation of bacterial alginate production. Environ Microbiol 16(10):2997–3011CrossRefGoogle Scholar
  83. 83.
    Schurr M, Martin D, Mudd M, Hibler N, Boucher J, Deretic V (1992) The algD promoter: regulation of alginate production by Pseudomonas aeruginosa in cystic fibrosis. Cell Mol Biol Res 39(4):371–376Google Scholar
  84. 84.
    Shankar S, Ye RW, Schlictman D, Chakrabarty A (1995) Exopolysaccharide alginate synthesis in Pseudomonas seruginosa: enzymology and regulation of gene expression. Adv Enzymol Relat Areas Mol Biol 70:221–255Google Scholar
  85. 85.
    Paletta JL, Ohman DE (2012) Evidence for two promoters internal to the alginate biosynthesis operon in Pseudomonas aeruginosa. Curr Microbiol 65(6):770–775CrossRefGoogle Scholar
  86. 86.
    Lynn A, Sokatch J (1984) Incorporation of isotope from specifically labeled glucose into alginates of Pseudomonas aeruginosa and Azotobacter vinelandii. J Bacteriol 158(3):1161–1162Google Scholar
  87. 87.
    Narbad A, Russell N, Gacesa P (1987) Radiolabelling patterns in alginate of Pseudomonas aeruginosa synthesized from specifically-labelled 14C-monosaccharide precursors. Microbios 54(220-221):171–179Google Scholar
  88. 88.
    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):4872–4877Google Scholar
  89. 89.
    Zielinski NA, Chakrabarty AM, Berry A (1991) Characterization and regulation of the Pseudomonas aeruginosa algC gene encoding phosphomannomutase. J Biol Chem 266(15):9754–9763Google Scholar
  90. 90.
    Shinabarger D, Berry A, May TB, Rothmel R, Fialho A, Chakrabarty AM (1991) Purification and characterization of phosphomannose isomerase-guanosine diphospho-D-mannose pyrophosphorylase. A bifunctional enzyme in the alginate biosynthetic pathway of Pseudomonas aeruginosa. J Biol Chem 266(4):2080–2088Google Scholar
  91. 91.
    Hay ID, Rehman ZU, Moradali MF, Wang Y, Rehm BH (2013) Microbial alginate production, modification and its applications. Microb Biotechnol 6(6):637–650Google Scholar
  92. 92.
    Roychoudhury S, May T, Gill J, Singh S, Feingold D, 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(16):9380–9385Google Scholar
  93. 93.
    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(7):1745–1754CrossRefGoogle Scholar
  94. 94.
    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(2):105–116CrossRefGoogle Scholar
  95. 95.
    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(10):3264–3272CrossRefGoogle Scholar
  96. 96.
    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(1):215–227CrossRefGoogle Scholar
  97. 97.
    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):4759–4773CrossRefGoogle Scholar
  98. 98.
    Oglesby LL, Jain S, Ohman DE (2008) Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154(6):1605–1615CrossRefGoogle Scholar
  99. 99.
    Remminghorst U, Rehm BH (2006) Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa. FEBS Lett 580(16):3883–3888CrossRefGoogle Scholar
  100. 100.
    Remminghorst U, Hay ID, Rehm BH (2009) Molecular characterization of Alg8, a putative glycosyltransferase, involved in alginate polymerisation. J Biotechnol 140(3):176–183CrossRefGoogle Scholar
  101. 101.
    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(4):876–895CrossRefGoogle Scholar
  102. 102.
    Hay ID, Remminghorst U, Rehm BH (2009) MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 75(4):1110–1120CrossRefGoogle Scholar
  103. 103.
    Moradali MF, Ghods S, Rehm BH (2017) Activation mechanism and cellular localization of membrane-anchored alginate polymerase in Pseudomonas aeruginosa. Appl Environ Microbiol 83:03499–03416CrossRefGoogle Scholar
  104. 104.
    Smidsrød O, Glover R, Whittington SG (1973) The relative extension of alginates having different chemical composition. Carbohydr Res 27(1):107–118CrossRefGoogle Scholar
  105. 105.
    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):1123–1133CrossRefGoogle Scholar
  106. 106.
    Gimmestad M, Sletta H, Ertesvåg H, Bakkevig K, Jain S, S-j S, 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(12):3515–3523CrossRefGoogle Scholar
  107. 107.
    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(15):5551–5560CrossRefGoogle Scholar
  108. 108.
    Ertesvåg H, Valla S (1999) The A modules of the Azotobacter vinelandii mannuronan-C-5-epimerase AlgE1 are sufficient for both epimerization and binding of Ca2+. J Bacteriol 181(10):3033–3038Google Scholar
  109. 109.
    Ullrich MS, Schergaut M, Boch J, Ullrich B (2000) Temperature-responsive genetic loci in the plant pathogen Pseudomonas syringae pv. glycinea. Microbiology 146(10):2457–2468CrossRefGoogle Scholar
  110. 110.
    Bjerkan TM, Bender CL, Ertesvåg H, Drabløs F, Fakhr MK, Preston LA, Skjåk-Bræk G, Valla S (2004) The Pseudomonas syringae genome encodes a combined mannuronan C-5-epimerase and O-acetylhydrolase, which strongly enhances the predicted gel-forming properties of alginates. J Biol Chem 279(28):28920–28929CrossRefGoogle Scholar
  111. 111.
    Ertesvåg H (2015) Alginate-modifying enzymes: biological roles and biotechnological uses. Front Microbiol 6Google Scholar
  112. 112.
    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):726–735CrossRefGoogle Scholar
  113. 113.
    Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188(1):82–97CrossRefGoogle Scholar
  114. 114.
    Tonon T, Rousvoal S, Roeder V, Boyen C (2008) Expression profiling of the mannuronan C5 epimerase multigenic family in the brown alga Laminaria digitata (Phaeophyceae) under biotic stress condition. J Phycol 44(5):1250–1256CrossRefGoogle Scholar
  115. 115.
    Baker P, Ricer T, Moynihan PJ, Kitova EN, Walvoort MT, Little DJ, Whitney JC, Dawson K, Weadge JT, Robinson H (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):e1004334CrossRefGoogle Scholar
  116. 116.
    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):3000–3007CrossRefGoogle Scholar
  117. 117.
    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):2186–2195CrossRefGoogle Scholar
  118. 118.
    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):5057–5065CrossRefGoogle Scholar
  119. 119.
    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(1):289–340CrossRefGoogle Scholar
  120. 120.
    Jain S, Ohman DE (2005) Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect Immun 73(10):6429–6436CrossRefGoogle Scholar
  121. 121.
    Wang Y, Moradali MF, Goudarztalejerdi A, Sims IM, Rehm BH (2016) Biological function of a polysaccharide degrading enzyme in the periplasm. Sci Rep 6Google Scholar
  122. 122.
    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):8375–8384CrossRefGoogle Scholar
  123. 123.
    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):634–641Google Scholar
  124. 124.
    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):7369–7377CrossRefGoogle Scholar
  125. 125.
    Rehm B, Boheim G, Tommassen J, Winkler U (1994) Overexpression of algE in Escherichia coli: subcellular localization, purification, and ion channel properties. J Bacteriol 176(18):5639–5647CrossRefGoogle Scholar
  126. 126.
    Whitney JC, Hay ID, Li C, Eckford PDW, Robinson H, Amaya MF, Wood LF, Ohman DE, Bear CE, Rehm BH, Lynne Howell P (2011) Structural basis for alginate secretion across the bacterial outer membrane. Proc Natl Acad Sci U S A 108(32):13083–13088CrossRefGoogle Scholar
  127. 127.
    Keiski C-L, Harwich M, Jain S, Neculai AM, Yip P, Robinson H, Whitney JC, Riley L, Burrows LL, Ohman DE (2010) AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure 18(2):265–273CrossRefGoogle Scholar
  128. 128.
    Remminghorst U, Rehm BH (2006) In vitro alginate polymerization and the functional role of Alg8 in alginate production by Pseudomonas aeruginosa. Appl Environ Microbiol 72(1):298–305CrossRefGoogle Scholar
  129. 129.
    Skjåk-Bræk G, Donati I, Paoletti S (2015) Alginate hydrogels: properties and applications. In: Matricardi FA P, Coviello T (eds) Polysaccharide hydrogels: characterization and biomedical applications. Pan Stanford Publishing Pte Ltd, SingaporeGoogle Scholar
  130. 130.
    Donati I, Paoletti S (2009) Material properties of alginates. In: Alginates: biology and applications. Springer, Berlin, pp 1–53Google Scholar
  131. 131.
    Conti E, Flaibani A, O’Regan M, Sutherland IW (1994) Alginate from Pseudomonas fluorescens and P. putida: production and properties. Microbiology 140(5):1125–1132CrossRefGoogle Scholar
  132. 132.
    Gacesa P (1988) Alginates. Carbohydr Polym 8(3):161–182CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • M. Fata Moradali
    • 1
  • Shirin Ghods
    • 1
  • Bernd H. A. Rehm
    • 2
    Email author
  1. 1.Department of Oral Biology, College of DentistryUniversity of FloridaGainesvilleUSA
  2. 2.Centre for Cell Factories and Biopolymers, Griffith Institute for Drug DiscoveryGriffith UniversityBrisbaneAustralia

Personalised recommendations