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Histidine Acid Phytases of Microbial Origin

Abstract

This review is focused on analysis of the biological diversity of phytase-producing microorganisms capable of degrading phytate to inorganic phosphate. General approaches to microbial phytase classification are discussed, with a particular emphasis on histidine acid phytases (HAPs), which catalyze specific cleaving of myo-inositol hexakisphosphate. The effect of glycosylation and various effectors on enzyme thermostability and activity of phytases are described. The data on the biosynthesis of histidine acid phytases, their substrate specificity, and on the mechanism of myo-inositol hexakisphosphate hydrolysis are considered. A conclusion is made concerning the biotechnological potential of this group of microbial enzymes.

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REFERENCES

  1. 1

    Abel S., Ticconi C., Delatorre C. Phosphate sensing in higher plants, Physiol. Plantarum., 2002, vol. 115, pp. 1–8.

    Article  CAS  Google Scholar 

  2. 2

    Akhmetova, A.I., Mukhametzyanova, A.D., and Sharipova, M.R., Microbial phytases as a basis for new technologies in animal feeding, Uch. Zap. Kazan. Univ. Nat. Sci., 2012, vol. 154, no. 2, pp. 1–8.

    Google Scholar 

  3. 3

    Andlid, T.A., Veide, J., and Sandberg, A.S., Metabolism of extracellular inositol hexaphosphate (phytate) by Saccharomyces cerevisiae, Int. J. Food Microbiol., 2004, vol. 97, pp. 157–169.

    Article  CAS  PubMed  Google Scholar 

  4. 4

    Balaban, N.P., Suleimanova, A.D., Valeeva, L.R., Shakirov, E.V., and Sharipova, M.R., Structural characteristics and catalytic mechanism of Bacillus β-propeller phytases, Biochemistry (Moscow), 2016, vol. 81, pp. 785–793.

    CAS  PubMed  Google Scholar 

  5. 5

    Balaban, N.P., Suleimanova, A.D., Valeeva, L.R., Chastukhina, I.B., Rudakova, N.L., Sharipova, M.R., and Shakirov, E.V., Microbial phytases and phytate: exploring opportunities for sustainable phosphorus management in agriculture, Amer. J. Mol. Biol., 2017, vol. 7, pp. 11–29.

    Article  Google Scholar 

  6. 6

    Balaban, N.P., Suleimanova, A.D., Valeeva, L.R., Chastukhina, I.B. and Sharipova, M.R., Inositol phosphates and their biological effects, Biomed. Pharmacol. J., 2014, vol. 7, pp. 433–437.

    Article  Google Scholar 

  7. 7

    Barrientos, L., Scott, J.J., and Murthy, P.P.N., Specificity of hydrolysis of phytic acid by alkaline phytase from lily pollen, Plant Physiol., 1994, vol. 106, pp. 1489–1495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 8

    Bohn, L., Meyer, A.S., and Rasmussen, S.K., Phytate: impact on environment and human nutrition. A challenge for molecular breeding, J. Zhejiang Univ. (Sci.), 2008, vol. 9, pp. 165–191.

    Article  Google Scholar 

  9. 9

    Borgi, M.A., Boudebbouze, S., Mkaouar, H., Maguin, E., and Rhimi, M., Bacillus phytases: current status and future prospects, Bioengineered, 2015, vol. 6, pp. 233–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Cangussu, A.S.R., Almeida, D.A., Aguiar, R.W.S., Bordignon-Junior, S.E., Viana, K.F., Barbosa, L.C., Cangussu, E.W., Brandi, I.V., Portella, A.C.F., Santos, G.R., Sobrinho, E.M., and Lima, W.J.N., Characterization of the catalytic structure of plant phytase, protein tyrosine phosphatase-like phytase, and histidine acid phytases and their biotechnological applications, Hindawi Enzyme Res., 2018, vol. 2018, article ID 8240698, p. 12. https://doi.org/ 10.1155/2018/8240698.

  11. 11

    Chen, C.C. and Cheng, K.J. Current progresses in phytase research: three-dimensional structure and protein engineering, ChemBioEng Rev., 2015, vol. 2, pp. 1–12.

    Article  Google Scholar 

  12. 12

    Dionisio, G., Brinch-Pedersen, H., Welinder, K.G., and Jorgensen, M., Different site-specific N-glycan types in wheat (Triticum aestivum L.) PAP phytase, Phytochemistry, 2011, vol. 72, pp. 1173–1179.

    Article  CAS  PubMed  Google Scholar 

  13. 13

    Doolette, A.L., Smernik, R.J., and Dougherty, W.J., Rapid decomposition of phytate applied to a calcareous soil demonstrated by a solution 31P NMR study, Europ. J. Soil Sci., 2010, vol. 61, pp. 563–575.

    Article  CAS  Google Scholar 

  14. 14

    Erlich, K.C., Montalbano, B.G., Mullaney, E.J., and Dischinger, H.C., Identification and cloning of a second phytase gene (phyB) from Aspergillus niger (ficuum), Biochem. Biophys. Res. Commun., 1993, vol. 195, pp. 53–57.

    Article  Google Scholar 

  15. 15

    Farias, N., Almeida, I., and Meneses, C., New bacterial phytase through metagenomic prospection, Molecules, 2018, vol. 23, p. 448.

    Article  CAS  PubMed Central  Google Scholar 

  16. 16

    Fugthong, A., Boonyapakron, K., Sornlek, W., Tanapongpipat, S., Eurwilaichitr, L., and Pootanakit, K., Biochemical characterization and in vitro digestibility assay of Eupenicillium parvum (BCC17694) phytase expressed in Pichia pastoris, Protein Expr. Purif., 2010, vol. 70, pp. 60–67.

    Article  CAS  PubMed  Google Scholar 

  17. 17

    Gaxiola, R.A., Edwards, M., and Elser, J.J., A transgenic approach to enhance phosphorus use efficiency in crops as part of a comprehensive strategy for sustainable agriculture, Chemosphere, 2011, vol. 84, pp. 840–845.

    Article  CAS  PubMed  Google Scholar 

  18. 18

    Greiner, R., Carlsson, N.G, and Alminger, M.L., Stereospecificity of myo-inositol hexakisphosphate dephosphorylation by a phytate-degrading enzyme of Escherichia coli, J. Biotechnol., 2000, vol. 84, pp. 53–62.

    Article  CAS  Google Scholar 

  19. 19

    Greiner, R., Phytate-degrading enzymes: regulation of synthesis in microorganisms and plants, in Inositol Phosphates: Linking Agriculture and the Environment, Turner, B.L., Richardson, A.E., and Mullaney, E.J., Eds., CABI, 2007, pp. 78–96.

  20. 20

    Greiner, R., Haller, E., Konietzny, U., and Jany, K.-D., Purification and characterization of a phytase from Klebsiella terrigena, Arch. Biochem. Biophys., 1997, vol. 341, pp. 201–206.

    Article  CAS  PubMed  Google Scholar 

  21. 21

    Greiner, R., Purification and characterization of three phytases from germinated lupine seeds (Lupinus albus var. Amiga), J. Agric. Food Chem., 2002, vol. 50, pp. 6858–6864.

    Article  CAS  PubMed  Google Scholar 

  22. 22

    Greiner, R., Konietzny, U., and Jany K.-D., Purification and characterization of two phytases from Escherichia coli, Arch. Biochem. Biophys., 1993, vol. 303, pp. 107–113.

    Article  CAS  PubMed  Google Scholar 

  23. 23

    Gupta, R.K. and Gangoliya, S.S., Reduction of phytic acid and enhancement of bioavailable micronutrients in food grains, J. Food Sci.Technol., 2015, vol. 52, pp. 676–684.

    Article  CAS  PubMed  Google Scholar 

  24. 24

    Ha, N.-C., Oh, B.-C., Shin, S., Kim, H.-J., Oh, T.-K., Kim, Y.-O., Choi, K.-Y., and Oh, B.-H., Crystal structures of a novel thermostable phytase in partially and fully calcium-loaded states, Nature Struct. Mol. Biol., 2000, vol. 7, pp. 147–153.

    Article  CAS  Google Scholar 

  25. 25

    Haefner, S., Knietsch, A., Sholten, E., Braun, J., Lohscheidt, M., and Zelder, O., Biotechnological production and applications of phytases, Microbiol. Biotechnol., 2005, vol. 68, pp. 588–597.

    Article  CAS  Google Scholar 

  26. 26

    Han, Y., Wilson, D.B., and Lei, X.G., Expression of an Aspergillus niger phytase gene (phyA) in Saccharomyces cerevisiae, Appl. Environ. Microbiol., 1999, vol. 65, pp. 1915–1918.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Jorquera, M.A., Hernander, M.T., Rengel, Z., Marschner, P., and Luz Mora, M., Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil, Biol. Fertil Soils, 2008, vol. 44, pp. 1025–1034.

    Article  CAS  Google Scholar 

  28. 28

    Kalsi, H.K., Singh, R., Dhaliwal, H.S., and Kumar, V., Phytases from Enterobacter and Serratia species with desirable characteristics for food and feed applications, Biotech., 2016, vol. 6, p. 64. doi 10.1007/s13205-016-0378-x

    Google Scholar 

  29. 29

    Kerovuo, J., Rouvinen, J., and Hatzack, F., Analysis of myo-inositol hexakisphosphate hydrolysis by Bacillus phytase: indication of a novel reaction mechanism, Biochem. J., 2000, vol. 352, pp. 623–628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Kim, H.W., Kim, Y.O., Lee, J.H., Kim, K.K., and Kim, Y.J., Isolation and characterization of a phytase with improved properties from Citrobacter braakii, Biotechnol. Lett., 2003, vol. 25, pp. 1231–1234.

    Article  CAS  PubMed  Google Scholar 

  31. 31

    Kim, Y.O., Kim, H.W., Lee, J.H., Kim, K.K., and Lee, S.J., Molecular cloning of the phytase gene from Citrobacter braakii and its expression in Saccharomyces cerevisiae, Biotechnol. Lett., 2006, vol. 28, pp. 33–38.

    Article  CAS  PubMed  Google Scholar 

  32. 32

    Konietzny, U. and Greiner, R., Molecular and catalytic properties of phytate-degrading enzymes (phytases), Int. J. Food Technol., 2002, vol. 37, pp. 781–812.

    Article  Google Scholar 

  33. 33

    Konietzny, U. and Greiner, R., Bacterial phytase: potential application, in vivo function and regulation of its synthesis, Brazil. J. Microbiol., 2004, vol. 35, pp. 11–18.

    Article  CAS  Google Scholar 

  34. 34

    Kostrewa, D., Leitch, F.G., DArcy, A., Broger, C., Mitchell, D., and van Loon, A.P.G.M., Crystal structure of phytase from Aspergillus ficuum at 2.5 Å resolution, Nature Struct. Biol., 1997, vol. 4, pp. 185–190.

    Article  CAS  PubMed  Google Scholar 

  35. 35

    Kostrewa, D., Wyss, M., D’Arcy, A., and van Loon, A.P., Crystal structure of Aspergillus niger pH 2.5 optimum acid phosphatase at 2.4 Å resolution, J. Mol. Biol., 1999, vol. 288, pp. 965–974.

    Article  CAS  PubMed  Google Scholar 

  36. 36

    Lan, G.Q., Abdullah, N., Jalaludin, S., and Ho, Y.W., Culture condition influencing phytase production of Mitsuokella jalaludinii, a new bacterial species from the rumen of cattle, J. Appl. Microbiol., 2002, vol. 93, pp. 668–674.

    Article  CAS  PubMed  Google Scholar 

  37. 37

    Lei, X.G., Weaver, J.D., Mullaney, E.J., Ullah, A.H., and Azain, M.J., Phytase, a new life for an “old” enzyme, Annu. Rev. Anim. Biosci., 2013, vol. 1, pp. 283–309.

    Article  CAS  PubMed  Google Scholar 

  38. 38

    Lei, X.G. and Porres, J.M., Phytase enzymology, applications, and biotechnology, J. Biotechnol. Lett., 2003, vol. 25, pp. 1787–1794.

    Article  CAS  Google Scholar 

  39. 39

    Lei, X.G. and Stahl, C.H., Biotechnological development of effective phytases for mineral nutrition and environmental protection, Appl. Microbiol. Biotechnol., 2001, vol. 57, pp. 474–481.

    Article  CAS  PubMed  Google Scholar 

  40. 40

    Lim, D., Golovan, S., Forsberg, C.W., and Jia, Z., Crystal structures of Escherichia coli phytase and its complex with phytate, Nature Struct. Biol., 2000, vol. 7, pp. 108–113.

    Article  CAS  PubMed  Google Scholar 

  41. 41

    Ma, X.F., Tudor, S., Butler, T., Ge, Y., Xi, Y., Bouton, J., Harrison, M., and Wang, Z.Y., Molecular breeding in plants: moving into the mainstream, Mol. Breeding., 2012, vol. 29, no. 4, pp. 831−832.

    Article  CAS  Google Scholar 

  42. 42

    Mukhametzyanova, A.D., Akhmetova, A.I., and Sharipova, M.R., Microorganisms as phytase producers, Microbiology (Moscow), 2012, vol. 81, pp. 267–275.

    Article  CAS  Google Scholar 

  43. 43

    Mullaney, E.J. and Ullah, A.H.J., Phytases: attributes, catalytic mechanisms and applications, in Inositol Phosphates: Linking Agriculture and the Environment, Turner, B.L., Richardson, A.E., and Mullaney, E.J., Eds., CABI, 2007, pp. 97–111.

  44. 44

    Mullaney, E.J. and Ullah, A.H.J., Conservation of cysteine residues in fungal histidine acid phytases, Biochem. Biophys. Res. Commun., 2005, vol. 328, pp. 404–408.

    Article  CAS  PubMed  Google Scholar 

  45. 45

    Mullaney, E.J. and Ullah, A.H.J., The term phytase comprises several different classes of enzymes, Biochem. Biophys. Res. Commun., 2003, vol. 312, pp. 179–184.

    Article  CAS  PubMed  Google Scholar 

  46. 46

    Mullaney, E.J., Daly, C.B., Kim, T., Porres, J.M., Lei, X.G., and Sethumadhavan, K., Site-directed mutagenesis of Aspergillus niger NRRL 3135 phytase at residue 300 to enhance catalysis at pH 4.0., Biochem. Biophys. Res. Commun., 2002, vol. 297, pp. 1016–1020.

    Article  CAS  PubMed  Google Scholar 

  47. 47

    Mullaney, E.J., Daly, C.B., Sethumadhavan, K., Rodriquez, E., Lei, X.G., and Ullah, A., Phytase activity in Aspergillus fumigatus isolates, Biochem. Biophys. Res. Commun., 2000, vol. 275, pp. 759–763.

    Article  CAS  PubMed  Google Scholar 

  48. 48

    Nakamura, Y., Fukuhara, H., and Sano, K., Secreted phytase activities of yeasts, Biosci. Biotechnol. Biochem., 2000, vol. 64, pp. 841–844.

    Article  CAS  PubMed  Google Scholar 

  49. 49

    Niu, C., Luo, H., Shi, P., Huang, H., Wang, Y., Yang, P., and Yao, B., N-Glycosylation improves the pepsin resistance of histidine acid phosphatase phytases by enhancing their stability at acidic pHs and reducing pepsin’s accessibility to its cleavage sites, Appl. Environ. Microbiol., 2015, vol. 82, pp. 1004–1014.

    Article  CAS  PubMed  Google Scholar 

  50. 50

    Oh, B.C., Choi, W.C., Park, S., Kim, Y.O., and Oh, T.K., Biochemical properties and substrate specificities of alkaline and histidine acid phytases, Appl. Microbiol. Biotechnol., 2004, vol. 63, pp. 362–372.

    Article  CAS  PubMed  Google Scholar 

  51. 51

    Oh, B.-C., Kim, M.H., Yun, B.-S., Choi, W.-C., Park, S.-C., Bae, S.-C., and Oh, T.-K., Ca2+-inositol phosphate chelation mediates the substrate specificity of β-propeller phytase, Biochemistry, 2006, vol. 45, pp. 9531–9539.

    Article  CAS  PubMed  Google Scholar 

  52. 52

    Pasamontes, L., Haiker, M., Wyss, M., Tessier, M., and van Loon, A.P., Gene cloning, purification, and characterization of a heat-stable phytase from the fungus Aspergillus fumigatus, Appl. Environ. Microbiol., 1997, vol. 63, pp. 1696–1700.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53

    Promdonkoy, P., Tang, K., Sornlake, W., Harnpicharnchai, P., Kobayashi, S.R, Ruanglek, V., Upathanpree-cha, T., Vesaratchavest, M., Eurwilaichitr, L., and Tanapongpipat, S., Expression and characterization of Aspergillus thermostable phytases in Pichia pastoris, FEMS Microbiol. Lett., 2009, vol. 290, pp. 18–24.

    Article  CAS  PubMed  Google Scholar 

  54. 54

    Priyodip, P., Prakash, P.Y., and Balaji, S., Phytases of probiotic bacteria: characteristics and beneficial aspects, Indian J. Microbiol., 2017, vol. 57, pp. 148–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Priyodip, P. and Balaji, S., Microbial degradation of myo-inositol hexakisphosphate (IP6): specificity, kinetics, and simulation, 3 Biotech., 2018, vol. 8, p. 268.

  56. 56

    Puhl, A., Greiner, R., and Selinger, L.B., Stereospecificity of myo-inositol hexakisphosphate hydrolysis by a protein tyrosine phosphatase-like inositol polyphosphatase from Megasphaera elsdenii, Appl. Microbiol. Biotechnol., 2009, vol. 82, pp. 95–103.

    Article  CAS  PubMed  Google Scholar 

  57. 57

    Ragon, M., Hoh, F., Aumelas, A., Chiche, L., Moulin, G., and Boze, H., Structure of Debaryomyces castellii CBS 2923 phytase, Acta Cryst., 2009, vol. 65, pp. 321–326.

    CAS  Google Scholar 

  58. 58

    Ragon, M., Neugnot-Roux, V., Chemardin, P., Moulin, G., and Boze, H., Molecular gene cloning and overexpression of the phatase from Debaryomyces castellii CBS 2923, Appl. Microbiol. Biotechnol., 2008, vol. 78, pp. 47–53.

    Article  CAS  PubMed  Google Scholar 

  59. 59

    Rao, K.V., Rao, T.P., and Reddy, V.D., Molecular characterization, physicochemical properties, known and potential applications of phytases: an overview, Crit. Rev. Biotechnol., 2009, vol. 29, pp. 182–198.

    Article  CAS  PubMed  Google Scholar 

  60. 60

    Richadson, A.E., Hadobas, P.A., Hayes, J.E., O’Hara, C.P., and Simpson, R.J., Utilization of phosphorus by pasture plants supplied with myo-inositol hexakisphosphate is enhanced by the presence of soil microorganisms, Plant Soil, 2001, pp. 47–56.

  61. 61

    Richardson, A.E., Hadobas, P.A., and Hayes, J.E., Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate, Plant J., 2001, vol. 25, pp. 641–649.

    Article  CAS  PubMed  Google Scholar 

  62. 62

    Rodriguez, E., Mullaney, E.J., and Ley, X.G., Expression of the Aspergillus fumigatus phytase gene in Pichia pastoris, Biochem. Biophys. Res. Commun., 2000, vol. 268, pp. 373–378.

    Article  CAS  PubMed  Google Scholar 

  63. 63

    Roy, M.P., Mazumdar, D., Dutta, S., and Saha, S.P., Cloning and expression of phytase appA gene from Shigella sp. CD2 in Pichia pastoris and comparison of properties with recombinant enzyme expressed in E. coli, PLoS One, 2016, pp. 11–14.

  64. 64

    Roy, M.P., Poddar, M., Singh, K.K., and Ghosh, S., Purification, characterization and properties of phytase from Shigella sp. CD2, Ind. J. Biochem. Biophys., 2012, vol. 49, pp. 266–271.

    CAS  Google Scholar 

  65. 65

    Secco, D., Bouain, N., Rouached, A., Prom-U-Thai, C., Hanin, M., Pandey, A.K., and Rouached, H., Phosphate, phytate and phytases in plants: from fundamental knowledge gained in Arabidopsis to potential biotechnological applications in wheat, Crit. Rev. Biotechnol., 2017, vol. 37, pp. 898–910.

    Article  CAS  PubMed  Google Scholar 

  66. 66

    Sequeilha, L., Lambrechts, C., Boze, H., Moulin, G., and Galzy, P., Purification and properties of the phytase from Schwanniomyces castellii, J. Ferment. Bioeng., 1992, vol. 74, pp. 7–11.

    Article  Google Scholar 

  67. 67

    Shamsuddin, A.M. and Vucenik, I., IP6 and innositol in cancer prevention and therapy, Curr. Cancer Ther. Rev., 2005, vol. 1, pp. 259–269.

    Article  CAS  Google Scholar 

  68. 68

    Shen, Y., Wang, H., and Pan, G., Improving inorganic phosphorus content in maize seeds by introduction of phytase gene, Biotechnol., 2008, vol. 7, pp. 323–327.

    Article  CAS  Google Scholar 

  69. 69

    Shi, X.-W., Sun, M.-L., Zhou, B., and Wang, X.-Y., Identification, characterization and overexpression of a phytase with potential industrial interest, Can. J. Microbiol., 2009, vol. 55, pp. 599–604.

    Article  CAS  PubMed  Google Scholar 

  70. 70

    Shin, S., Ha, N.C., Oh, B.C., Oh, T.K., and Oh, B.H., Enzyme mechanism and catalytic property of β-propeller phytase, Structure, 2001, vol. 9, pp. 851–858.

    Article  CAS  PubMed  Google Scholar 

  71. 71

    Singh, B. and Satyanarayana, T., Microbial phytases in phosphorus acquisition and plant growth promotion, Physiol. Mol. Biol. Plants, 2011, vol. 17, pp. 93–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Sommerfeld, V., Schollenberger, M., Kuhn, I., and Rodehutscord, M., Interactive effects of phosphorus, calcium, and phytase supplements on products of phytate degradation in the digestive tract of broiler chickens, Poultry Sci., 2018, vol. 97, pp. 1177–1188.

    Article  CAS  Google Scholar 

  73. 73

    Stahl, C.H., Wilson, D.B., and Lei, X.G., Comparison of extracellular Escherichia coli AppA phytases expressed in Streptomyces lividans and Pichia pastoris, Biotechnol. Lett., 2003, vol. 25, pp. 827–831.

    Article  CAS  PubMed  Google Scholar 

  74. 74

    Suleimanova, A.D., Beinhauer, A., Valeeva, L.R., Chastukhina, I.B., Balaban, N.P., Shakirov, E.V., Greiner, R., and Sharipova, M.R., Novel glucose-1-phosphatase with high phytase activity and unusual metal ion activation from soil bacterium Pantoea sp. strain 3.5.1, Appl. Environm. Microbiol., 2015, vol. 81, pp. 1–10.

    Article  CAS  Google Scholar 

  75. 75

    Tomschy, A., Tessier, M., Wyss, M., Brugger, R., and Broger, C., Optimization of the catalytic properties of Aspergillus fumigatus phytase based on the three-dimensional structure, Protein Sci., 2000, vol. 9, pp. 1304–1311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 76

    Touati, E., Dassa, E., Dassa, J., and Boquer, P.l., Acid phosphatase (pH 2.5) of Escherichia coli: regulatory characteristics, in Phosphates Metabolism and Cellular Regulation in Microorganisms, Torriani-Gorini, A., Rothman, F.G., Silver, S., Wrigt, A., and Yagil, E., Eds., Washington: Amer. Soc. Microbiol. 1987, pp. 31–40.

    Google Scholar 

  77. 77

    Tran, T.T., Mamo, G., Bo, M., and Hatti-Kaul, R., A thermostable phytase from Bacillus sp. MD2: cloning, expression and high-level production in Escherichia coli, J. Ind. Microbiol. Biotechnol., 2010, vol. 37, pp. 279–287.

    Article  CAS  PubMed  Google Scholar 

  78. 78

    Tran, T.T., Mamo, G., Búxo, L., Le, N.N., Gaber, Y., Mattiasson, B., and Hatii-Kaul, R., Site-directed mutagnesis of an alkaline phytase influencing specificity, activity and stability in acidic milieu, Enzyme Microb. Technol., 2011, vol. 49, pp. 177–182.

    Article  CAS  PubMed  Google Scholar 

  79. 79

    Turner, B.L., Inositol phosphates in soil: amoumts, forms and significance of the phosphorylated inositol stereoisomers, in Inositol Phosphates: Linking Agriculture and the Environment, Turner, B.L., Richardson, A.E., and Mullaney, E.J., Eds., CABI, 2007, pp. 186–203.

  80. 80

    Ushasree, M.V., Shyam, K., Vidya, J., and Pandey, A., Microbial phytase: impact of advances in genetic engineering in revolutionizing its properties and applications, Bioresource Technol., 2017, vol. 245, part. B, pp. 1790–1799.

  81. 81

    Vats, P. and Banerjee, U.C., Production studies and catalytic properties of phytases (myo-inositol hexakisphosphate phosphohydrolases): an overview, Enzyme Microb. Technol., 2004, vol. 35, pp. 3–14.

    Article  CAS  Google Scholar 

  82. 82

    Vohra, A. and Satyanarayana, T., Phytases: microbial sources, production, purification and potential biotechnological applications, Crit. Rev. Biotechnol., 2003, vol. 23, pp. 29–60.

    Article  CAS  PubMed  Google Scholar 

  83. 83

    Wyss, M., Pasamontes, L., Friedlein, A., Remy, R., Tessier, M., Kronenberger, A., and van Loon, A., Biophysical characterization of fungal phytases (myo-inositol hexakisphosphate phosphohydrolases): molecular size, glycosylation pattern, and engineering of proteolytic resistance, Appl. Environ. Microbiol., 1999b, vol. 65, pp. 359–366.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84

    Wyss, M., Brugger, R., Kronenberger, A., Remy, R., Fimbel, R., Oesterhelt, G., Lehmann, M., and van Loon, A.P., Biochemical characterization of fungal phytases (myo-inositol hexakisphosphate phosphohydrolases): catalytic properties, Appl. Environ. Microbiol., 1999a, vol. 65, pp. 367–373.

    CAS  PubMed  PubMed Central  Google Scholar 

  85. 85

    Wyss, M., Pasamontes, L., Remy, R., Kohler, J., Kusznir, E., Gadient, M., Muller, F., and van Loon, A.P.G.M., Comparison of the termostability properties of three acid phosphatases from molds: Aspergillus fumigatus phytase, A. niger phytase, and A. niger pH 2.5 acid phosphatase, Appl. Environ. Microbiol., 1998, vol. 64, pp. 4446–4451.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86

    Yao, M.Z., Zhang, Y.H., Lu, W.L., Hu, M.Q., Wang, W., and Liang, A.H., Phytases: crystal structures, protein engineering and potential biotechnological applications, J. Appl. Microbiol., 2011, vol. 112, pp. 1–14.

    Article  CAS  PubMed  Google Scholar 

  87. 87

    Yip, W., Wang, L., Cheng, C., Wu, W., Lung, S., and Lim, B.-L., The introduction of a phytase gene from Bacillus subtilis improvedthe growth performance of transgenic tobacco, Biochem. Biophys. Res. Commun., 2003, vol. 310, pp. 1148–1154.

    Article  CAS  PubMed  Google Scholar 

  88. 88

    Yoon, S.M., Kim, S.Y., Li, K.F., Yoon, B.H., Choe, S., and Kuo, M.M., Transgenic microalgae expressing Escherichia coli AppA phytase as feed additive to reduce phytate excretion in the manure of young broiler chicks, Appl. Microbiol. Biotechnol., 2011, vol. 91, pp. 553–563.

    Article  CAS  PubMed  Google Scholar 

  89. 89

    Zamudio, M., Gonzalez, A., and Medina, J.A., Lactobacillus plantarum phytase activity is due to non-specific acid phosphatase, Lett. Appl. Microbiol., 2001, vol. 32, pp. 181–184.

    Article  CAS  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

The work was supported by the State Competitiveness Enhancement Program of the Kazan (Volga region) Federal University among the leading world scientific education centers and by the grant of the Russian Science Foundation no. 16-16-04062.

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Correspondence to N. P. Balaban.

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Translated by E. Makeeva

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Balaban, N.P., Suleimanova, A.D., Shakirov, E.V. et al. Histidine Acid Phytases of Microbial Origin. Microbiology 87, 745–756 (2018). https://doi.org/10.1134/S0026261718060024

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Keywords:

  • histidine acid phytases
  • microorganisms
  • myo-inositol hexakisphosphate
  • biochemical properties
  • substrate specificity
  • phytate hydrolysis