Skip to main content

Origin and evolution of alginate-c5-mannuronan-epimerase gene based on transcriptomic analysis of brown algae

Abstract

The coding product of alginate-c5-mannuronan-epimerase gene (algG gene) can catalyze the conversion of mannuronate to guluronate and determine the M/G ratio of alginate. Most of the current knowledge about genes involved in the alginate biosynthesis comes from bacterial systems. In this article, based on some algal and bacterial algG genes registered on GenBank and EMBL databases, we predicted 94 algG genes open reading frame (ORF) sequences of brown algae from the 1 000 Plant Transcriptome Sequencing Project (OneKP). By method of transcriptomic sequence analysis, gene structure and gene localization analysis, multiple sequence alignment and phylogenetic tree construction, we studied the algal algG gene family characteristics, the structure modeling and conserved motifs of AlgG protein, the origin of alginate biosynthesis and the variation incidents that might have happened during evolution in algae. Although there are different members in the algal algG gene family, almost all of them harbor the conserved epimerase region. Based on the phylogenetic analysis of algG genes, we proposed that brown algae acquired the alginate biosynthesis pathway from an ancient bacterium by horizontal gene transfer (HGT). Afterwards, followed by duplications, chromosome disorder, mutation or recombination during evolution, brown algal algG genes were divided into different types.

This is a preview of subscription content, access via your institution.

References

  1. Arnold K L, Bordoli J, Kopp, et al. 2006. The SWISS-MODEL Workspace: a web-base environment for protein structure homology modeling. Bioinformatics, 22: 195–201

    Article  Google Scholar 

  2. Chitnis C E, Ohman D E. 1990. Cloning of Pseudomonas aeruginosa algG, which controls alginate structure. Bacteriol, 172(6): 2894–2900

    Google Scholar 

  3. Chitnis C E, Ohman D E. 1993. Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure. Mol Microbiol, 8: 583–590

    Article  Google Scholar 

  4. Cook J M, Sterck L, Rouzé P, et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465: 617–621

    Article  Google Scholar 

  5. Douglas S E. 1998. Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev, 8: 655–661

    Article  Google Scholar 

  6. Ertesvåg H, Doseth B, Larsen B, et al. 1994. Cloning and expression of an Azotobacter vinelandii mannuronan C-5-epimerase gene. J Bacteriol, 176: 2846–2853

    Google Scholar 

  7. Ertesvåg H, Høidal H K, Hals I K, et al. 1995. A family of modular type mannuronan C-5-epimerase genes controls alginate structure in Azotobacter vinelandii. Mol Microbiol, 9: 719–731

    Article  Google Scholar 

  8. Ertesvåg H, Høidal H K, Skjåk-Bræk G, et al. 1998. The Azotobacter vinelandii mannuronan C-5-epimerase AlgE1 consists of two separate catalytic domains. J Biol Chem, 273: 30927–30932

    Article  Google Scholar 

  9. 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: 3033–3038

    Google Scholar 

  10. Flagel L, Wendel J. 2009. Gene duplication and evolutionary novelty in plants. New Phytologist, 183: 557–564

    Article  Google Scholar 

  11. Franklin M J, Chitnis C E, Gacesa P, et al. 1994. Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase. J Bacteriol, 176: 1821–1830

    Google Scholar 

  12. Gimmestad M, Sletta H, Ertesvag H, et al. 2003. The Pseudomonas fluorescens AlgG protein, but not itsmannuronan C-5-epimerase activity, is needed for alginate polymer formation. J Bacteriol, 185: 3515–3523

    Article  Google Scholar 

  13. Gorin P A, Spencer J F. 1966. Exocellular alginic acid from Azotobacter vinelandii. Can J Chem, 44: 993–998

    Article  Google Scholar 

  14. Govan J R W, Fyfe J A M, Jarman T R. 1981. Isolation of alginate producing mutants of Pseudomonas fluorescens, Pseudomonas putida and Pseudomonas mendocina. J Gen Microbiol, 125: 217–220

    Google Scholar 

  15. Guex N, Peitsch M C. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis, 18: 2714–2723

    Article  Google Scholar 

  16. Gurvan M, Thierry T, Delphine S, et al. 2010. The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytologist, 188: 82–97

    Article  Google Scholar 

  17. Rozeboom H J, Bjerkan T M, Kalk K H, et al. 2008. Structural and Mutational Characterization of the Catalytic A-module of the Mannuronan C-5-epimerase AlgE4 from Azotobacter vinelandii. J Biol Chem, 283: 23819–23828

    Article  Google Scholar 

  18. Hughes T, Liberles D A. 2007. The pattern of evolution of smaller-scale gene duplicates in mammalian genomes is more consistent with neo-than subfunctionalisation. J Mol Evol, 65(5): 574–588

    Article  Google Scholar 

  19. Jain S, Franklin M J, Ertesvag H, et al. 2003. The dual roles of AlgG in C-5-epimerization and secretion of alginate polymers in Pseudomonas aeruginosa. Mol Microbiol, 47: 1123–1133

    Article  Google Scholar 

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

    Google Scholar 

  21. Jenkins J, Shevchik V E, Hugouvieux-Cotte-Pattat N, et al. 2004. The crystal structure of pectate lyase Pel9A from Erwinia chrysanthemi. J Biol Chem, 279: 9139–9145

    Article  Google Scholar 

  22. Kloareg B, Quatrano R S. 1988. Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev, 1988: 259–315

    Google Scholar 

  23. Lang B F, Seif E, Gray M W, et al. 1999. A comparative genomics approach to the evolution of eukaryotes and their mitochondria. J Eukaryot Microbiol, 46: 320–326

    Article  Google Scholar 

  24. Linker A, Jones R S. 1966. A new polysaccharide resembling alginic acid isolated from pseudomonas. J Biol Chem, 241: 3845–385

    Google Scholar 

  25. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics, 154(1): 459–473

    Google Scholar 

  26. Morch Y A, Holtan S, Donati I, et al. 2008. Mechanical properties of C-5 epimerized alginates. Biomacromolecules, 9: 2360–2368

    Article  Google Scholar 

  27. Moreira D, Le Guyader H, Philippe H. 2000. The origin of red algae and the evolution of chloroplasts. Nature, 405: 69–72

    Article  Google Scholar 

  28. Nyvall P, Erwan C, Claire B, et al. 2003. Characterization of Mannuronan C-5-Epimerase Genes from the Brown Alga Laminaria digitata. Plant Physiology, 133(2): 726–735

    Article  Google Scholar 

  29. Okasaki M, Furuya K, Tsukayama K, et al. 1982. Isolation and identification of alginic acid from a calcareous red alga Serraticardia maxima. Botanica Marina, 25: 123–131

    Google Scholar 

  30. Okasaki M, Shiroto C, Furuya K. 1984. Relationship between the location of polyuronides and calcification sites in the calcareous red algae Serraticardia maxima and Lithothamnion japonica (Rhodophyta, Corallinaceae). Jap J Phycol, 32: 364–372

    Google Scholar 

  31. Page R D. 1996. TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12: 357–358

    Google Scholar 

  32. Panikkar R, Brasch D J. 1996. Composition and block structure of alginates from New Zealand brown seaweeds. Carbohydr Res, 293: 119–132

    Article  Google Scholar 

  33. Pedersen S S, Hoiby N, Espersen F, et al. 1992. Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax, 47: 6–13

    Article  Google Scholar 

  34. Penaloza-Vazquez A, Kidambi S P, Chakrabarty A M, et al. 1997. Characterization of the alginate biosynthetic gene cluster in Pseudomonas syringae pv. syringae. J Bacteriol, 179: 4464–4472

    Google Scholar 

  35. Posada D, Crandall K A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14: 817–818

    Article  Google Scholar 

  36. Rehm B H A, 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. Bacteriol, 178: 5884–5889

    Google Scholar 

  37. Rehm B H A, Valla S. 1997. Bacterial alginates: biosynthesis and applications. Appl Microbiol Biotechnol, 48: 281–288

    Article  Google Scholar 

  38. Reyes-Prieto A, Weber A P, Bhattacharya D. 2007. The origin and establishment of the plastid in algae and plants. Annual Review of Genetics, 41: 147–168

    Article  Google Scholar 

  39. Robles-Price A, Wong T Y, Sletta H, et al. 2004. AlgX is a periplasmic protein required for alginate biosynthesis in Pseudomonas aeruginosa. J Bacteriol, 186: 7369–7377

    Article  Google Scholar 

  40. Ronquist F, Huelsenbeck J P. 2003. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574

    Article  Google Scholar 

  41. Sadoff H L. 1975. Encystment and germination of Azotobacter vinelandii. Bacteriol Rev, 39: 516–539

    Google Scholar 

  42. Schwede T, Kopp J, Guex N, et al. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Research, 31: 3381–3385

    Article  Google Scholar 

  43. Skjåk-Bræk G, Espevik T. 1996. Application of alginate gels in biotechnology and biomedicine. Carbohydr Eur, 14: 19–25

    Google Scholar 

  44. Smidsrød O, Draget K I. 1996. Chemistry and physical properties of alginates. Carbohydr Eur, 14: 6–13

    Google Scholar 

  45. Stephanie A, Douthit D, Mensur E O, et al. 2005. Epimerase Active Domain of Pseudomonas aeruginosa AlgG, a Protein That Contains a Right-Handed β-Helix. Journal of Bacteriology, 187(13): 4573–4583

    Article  Google Scholar 

  46. Svanem B I, Skjåk-Bræk G, Ertesvåg H, et al. 1999. Cloning and expression of three new Azotobacter vinelandii genes closely related to a previously described gene family encoding mannuronan C-5-epimerases. Bacteriol, 181: 68–77

    Google Scholar 

  47. Thompson J D, Gibson T J, Plewniak F, et al. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 25: 4876–4882

    Article  Google Scholar 

  48. Usov A I, Bilan M I, Klochkova N G. 1995. Polysaccharides of algae. 48. Polysaccharide composition of several calcareous red algae: isolation of alginate from Corallina pilulifera P. et R. (Rhodophyta, Corallinaceae). Botanica Marina, 38: 43–52

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Tao Liu or Shan Chi.

Additional information

Foundation item: The National High Technology Research and Development Program of China under contract No. 2012AA10A406; the National Natural Science Foundation of China under contract Nos 41206116, 31140070 and 31271397; Technology Project of Ocean and Fisheries of Guangdong Province under contract No. A201201E03; the Fundamental Research Funds for the Central Universities under contract No. 201262003; China Postdoctoral Science Foundation under contract No. 2011M501167; the algal transcriptome sequencing was supported by 1KP Project (www.onekp.com).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wang, R., Wang, X., Zhang, Y. et al. Origin and evolution of alginate-c5-mannuronan-epimerase gene based on transcriptomic analysis of brown algae. Acta Oceanol. Sin. 33, 73–85 (2014). https://doi.org/10.1007/s13131-014-0443-4

Download citation

Key words

  • transcriptomic sequencing
  • alginate-c5-mannuronan-epimerase gene
  • gene family
  • alginate
  • phylogenetic analysis