Molecular advancements in the development of thermostable phytases

Applied Microbiology and Biotechnology

Volumn 101, Issue 7, 2017, Pages 2677-2689

  Rebello, Sharrel ^a   Jose, Leny ^b   Sindhu, Raveendran ^c   Aneesh, Embalil Mathachan ^a  

^a St Joseph's College   (India)

^b INDIANA UNIVERSITY   (United States)

^c REGIONAL RESEARCH LABORATORY CSIR   (India)

Author keywords

Aspergillus; Phytases; Phytate; Pichia; Thermostable

Indexed keywords

ASPERGILLUS; EUTROPHICATION; GLOBAL WARMING; GREENHOUSE GASES; PHYSIOLOGY;

ENVIRONMENTAL PROBLEMS; HETEROLOGOUS EXPRESSION; PHYTASES; PHYTATE; PICHIA; PROTEIN ENGINEERING; SIMULTANEOUS REDUCTION; THERMOSTABLE;

ENZYMES;

PHYTASE; PHYTIC ACID; RECOMBINANT PROTEIN;

BIODEGRADATION; CHEMICAL COMPOUND; ENZYME; FUNGUS; GENETIC ENGINEERING; GREENHOUSE GAS; MOLECULAR ANALYSIS; PROTEIN; RECOMBINATION; RESEARCH WORK; TEMPERATURE EFFECT; YEAST;

ANIMAL FOOD; FOOD INDUSTRY; HEAT TOLERANCE; HUMAN; INDUSTRIAL PRODUCTION; NONHUMAN; NUTRITION; POLLUTION; PROTEIN ENGINEERING; RECOMBINANT DNA TECHNOLOGY; REVIEW; THERMOSTABILITY; AGRICULTURE; ASPERGILLUS; CHEMISTRY; ECONOMICS; ENZYME STABILITY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; HEAT; ISOLATION AND PURIFICATION; METABOLISM; PH; PICHIA; PROCEDURES;

ANIMALIA; ASPERGILLUS; PICHIA;

6-PHYTASE; AGRICULTURE; ANIMAL FEED; ASPERGILLUS; ENZYME STABILITY; ESCHERICHIA COLI; HOT TEMPERATURE; HUMANS; HYDROGEN-ION CONCENTRATION; PHYTIC ACID; PICHIA; PROTEIN ENGINEERING; RECOMBINANT PROTEINS;

EID: 85013682940     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-017-8195-7     Document Type: Review

References (111)

1. Acuna J, Gabler S, Menezes-Blackburn D, Greiner R, Jorquera M, Mora MDLL (2014) Isolation of phytase-producing Rhizobacteria from extreme environments. In: 20th World Congress Of Soil Science, pp 421–421.
2. Alves NM, Guimaraes LHS, Piccoli RH, Cardoso PG (2016) Production and partial characterization of an extracellular phytase produced by Muscodor sp. under submerged fermentation. Adv Microbiol 6:23–32. doi:10.4236/aim.2016.6100
3. Azeke MA, Greiner R, Jany KD (2011) Purification and characterization of two intracellular phytases from the tempeh fungus Rhizopus oligosporus. J Food Biochem 35:213–227. doi:10.1111/j.1745-4514.2010. 00377.x
4. Balaban NP, Suleimanova AD, Valeeva LR, Shakirov EV, Sharipova MR (2016) Structural characteristics and catalytic mechanism of Bacillus β-propeller phytases. Biochemist 81(8):785–793. doi:10.1134/S0006297916080010
5. Barrientos L, Scott JJ, Murthy PPN (1994) Specificity of hydrolysis of phytic acid by alkaline phytase from lily pollen. Plant Physiol 106(4):1489–1495. doi:10.1104/pp.106.4.1489
6. Boukhris I, Farhat Khemakhem A, Bouchaala K, Virolle M-J, Chouayekh H (2016) Cloning and characterization of the first actinomycete β propeller phytase from Streptomyces sp. US42. J Basic Microbiol 56(10):1080–1089. doi:10.1002/jobm.201500760
7. Boukhris I, Farhat-Khemakhem A, Blibech M, Bouchaala K, Chouayekh H (2015) Characterization of an extremely salt-tolerant and thermostable phytase from Bacillus amyloliquefaciens US573. Int J Biol Macromolec 80:581–587. doi:10.1016/j.ijbiomac.2015.07.014
8. Chanderman A, Puri AK, Permaul K, Singh S (2016) Production, characteristics and applications of phytase from a rhizosphere isolated Enterobacter sp. ACSS. Bioprocess Biosyst Eng 39(10):1577–1587. doi:10.1007/s00449-016-1632-7
9. Charoenrat T, Antimanon S, Kocharin K, Tanapongpipat S, Roongsawang N (2016) High cell density process for constitutive production of a recombinant phytase in thermotolerant methylotrophic yeast Ogataea thermomethanolica using table sugar as carbon source. Appl Biochem Biotech 180:1618–1634. doi:10.1007/s12010-016-2191-8
10. Cho E-A, Kim E-J, Pan J-G (2011) Adsorption immobilization of Escherichia coli phytase on probiotic Bacillus polyfermenticus spores. Enzym Microb Technol 49(1):66–71. doi:10.1016/j. enzmictec.2011.03.006
11. Chu HM, Guo RT, Lin TW, Chou CC, Shr HL, Lai HL, Tang TY, Cheng KJ, Selinger BL, Wang AHJ (2004) Structures of Selenomonas ruminantium phytase in complex with persulfated phytate: DSP phytase fold and mechanism for sequential substrate hydrolysis. Structure 12(11):2015–2024. doi:10.1016/j. str.2004.08.010
12. Coban HB, Demirci A, Turhan I (2015) Microparticle-enhanced Aspergillus ficuum phytase production and evaluation of fungal morphology in submerged fermentation. Bioprocess Biosyst Eng 38:1075–1080. doi:10.1007/s00449-014-1349-4
13. De Jong JA, DeRouchey JM, Tokach MD, Goodband RD, Woodworth JC, Jones CK, Stark CR, Bradley CL, Loughmiller JA, Bergstrom JR (2016) Stability of commercial phytase products stored under different environmental conditions. J Anim Sci 94:114. doi:10.2527/msasas 2016–241
14. Debnath D, Sahu NP, Pal AK, Baruah K, Yengkokpam S, Mukherjee SC (2005) Present scenario and future prospects of phytase in aquafeed. Asian-Aust J Anim Sci 18:1800–1812. doi:10.5713/ajas.2005.1800
15. Eida MF, Nagaoka T, Wasaki J, Kouno K (2013) Phytate degradation by fungi and bacteria that inhabit sawdust and coffee residue composts. Microbes Environ 28:71–80. doi:10.1264/ jsme2.ME12083
16. Erpel F, Restovic F, Arce-Johnson P (2016) Development of phytase-expressing Chlamydomonas reinhardtii for monogastric animal nutrition. BMC Biotechnol 16:1–7. doi:10.1186/s12896-016-0258-9
17. Farhat-Khemakhem A, Ali MB, Boukhris I, Khemakhem B, Maguin E, Bejar S, Chouayekh H (2013) Crucial role of Pro 257 in the thermostability of Bacillus phytases: biochemical and structural investigation. Int J Biol Macromolec 54:9–15. doi:10.1016/j.ijbiomac.2012.11.020
18. Fei B, Xu H, Zhang F, Li X, Ma S, Cao Y, Xie J, Qiao D, Cao Y (2013) Relationship between Escherichia coli AppA phytase’s thermostability and salt bridges. J Biosci Bioeng 115:623–627. doi:10.1016/j.jbiosc. 2012.12.010
19. Fonseca-Maldonado R, Maller A, Bonneil E, Thibault P, Botelho-Machado C, Ward RJ, Polizeli MLTM (2014) Biochemical properties of glycosylation and characterization of a histidine acid phosphatase (phytase) expressed in Pichia pastoris. Protein Expr Purif 99:43–49. doi:10.1016/ j.pep.2014.03.006
20. Fredrikson M, Biot P, Alminger ML, Carlsson N-G, Sandberg A-S (2001) Production process for high-quality pea-protein isolate with low content of oligosaccharides and phytate. J Agric Food Chem 49:1208–1212. doi:10.1021/jf000708x
21. Fu D, Huang H, Meng K, Wang Y, Luo H, Yang P, Yuan T, Yao B (2009) Improvement of Yersinia frederiksenii phytase performance by a single amino acid substitution. Biotechnol Bioeng 103(5):857–864. doi:10.1002/bit.22315
22. Gaind S, Singh S (2015) Production, purification and characterization of neutral phytase from thermotolerant Aspergillus flavus ITCC 6720. Int Biodeterioration Biodegrad 99:15–22. doi:10.1016/j.ibiod.2014.12.013
23. Greiner R, Koneitzny, U. (2011) Phytases: biochemistry, enzymology and characteristics relevant to animal feed. In: Partridge MRBaGG (ed) Enzymes in farm animal nutrition. 2nd edn. CAB International
24. Greiner R, Konietzny U (2006) Phytase for food application. Food Technol Biotechnol 44(2):125–140
25. Greppi A, Krych L, Costantini A, Rantsiou K, Hounhouigan DJ, Arneborg N, Cocolin L, Jespersen L (2015) Phytase-producing capacity of yeasts isolated from traditional African fermented food products and PHYPk gene expression of Pichia kudriavzevii strains. Int J Food Microbiol 205:81–89. doi:10.1016/j.ijfoodmicro.2015.04.011
26. Guerrero-Olazaran M, Rodriguez-Blanco L, Carreon-Trevino JG, Gallegos-Lopez JA, Viader-Salvado JM (2010) Expression of a Bacillus phytase C gene in Pichia pastoris and properties of the recombinant enzyme. Appl Environ Microbiol 76:5601–5608. doi:10.1128/AEM.00762-10
27. Ha NC, Oh BC, Shin S, Kim HJ, Oh TK, Kim YO, Choi KY, Oh BH (2000) Crystal structures of a novel, thermostable phytase in partially and fully calcium-loaded states. Nat Struct Mol Biol 7:147–153. doi:10.1038/72421
28. Han Y, Wilson DB, Gen Lei X (1999) Expression of an Aspergillus niger phytase gene (phyA) in Saccharomyces cerevisiae. Appl Environ Microbiol 65:1915–1918
29. Hara A, Ebina S, Kondo A, Funaguma T (1985) A new type of phytase from pollen of Typha latifolia L. Agric Biol Chem 49(12):3539–3544
30. Hesham El Enshasy NZO, Roslinda Abd Malek (2014) Industrial platform design for fungal phytase production in semi-industrial scale. Paper presented at the 14 AIChE Annual Meeting, Atlanta, GA
31. Jain J, Singh B (2016) Characteristics and biotechnological applications of bacterial phytases. Process Biochem 51:159–169. doi:10.1016/j.procbio.2015.12.004
32. Joseph B, Chacko M, Rebello S, Ks R, Ng RB, Karthikeyan S (2016) Molecular taxonomic identification, biosynthesis and in vitro antibacterial activity of ZNO nanoparticles using Boerhavia diffusa against MRSA. Int J Toxicol Pharma Res 8:40–44
33. Kaur P, Singh B, Boer E, Straube N, Piontek M, Satyanarayana T, Kunze G (2010) Pphy—a cell-bound phytase from the yeast Pichia anomala: molecular cloning of the gene PPHY and characterization of the recombinant enzyme. J Biotechnol 149:8–15. doi:10.1016/j.jbiotec.2010.06.017
34. Kim Y-O, Kim H-K, Bae K-S, Yu J-H, Oh T-K (1998) Purification and properties of a thermostable phytase from Bacillus sp. DS11. Enzy Microb Technol 22:2–7
35. Kim M-S, Weaver JD, Lei XG (2008) Assembly of mutations for improving thermostability of Escherichia coli AppA2 phytase. Appl Microbiol Biotechnol 79:751–758. doi:10.1007/s00253-008-1478-2
36. Klabunde T, Strater N, Frohlich R, Witzel H, Krebs B (1996) Mechanism of Fe (III)-Zn (II) purple acid phosphatase based on crystal structures. J Mol Biol 259(4):737–748. doi:10.1006/jmbi.1996.0354
37. Kostrewa D, Wyss M, D’arcy A, van Loon APGM (1999) Crystal structure of Aspergillus niger pH 2.5 acid phosphatase at 2.4 Å resolution1. J Mol Biol 288(5):965–974. doi:10.1006/ jmbi.1999.2736
38. Kumar V, Singh D, Sangwan P, Gill PK (2015) Management of environmental phosphorus pollution using phytases: current challenges and future prospects. In: Applied environmental biotechnology: present scenario and future trends. Springer, pp 97–114.
39. Kumar V, Sinha A, Makkar H, Becker K (2010) Dietary roles of phytate and phytase in human nutrition: a review. Food Chem 120(4):945–959. doi:10.1016/j.foodchem.2009.11.052
40. Lee SH, Cho J, Bok J, Kang S, Choi Y, Lee PCW (2015) Characterization, gene cloning, and sequencing of a fungal phytase, PhyA, from Penicillium oxalicum PJ3. Prep Biochem Biotechnol 45:336–347. doi:10.1080/10826068.2014.923446
41. Lei XG, Porres JM, Mullaney EJ, Brinch-Pedersen H (2007) Phytase: source, structure and application. In Industrial enzymes. Springer. pp. 505–529.
42. Lei XG, Stahl CH (2000) Nutritional benefits of phytase and dietary determinants of its efficacy. J Appl Anim Res 17:97–112. doi:10.1080/09712119.2000.9706294
43. Lei X, Stahl C (2001) Biotechnological development of effective phytases for mineral nutrition and environmental protection. Appl Microbiol Biotechnol 57:474–481. doi:10.1007/s002530100795
44. Li X, Chi Z, Liu Z, Li J, Wang X, Hirimuthugoda NY (2008) Purification and characterization of extracellular phytase from a marine yeast Kodamaea ohmeri BG3. Mar Biotechnol 10:190–197. doi:10.1007/ s10126 -007-9051-z
45. Li C, Lin Y, Huang Y, Liu X, Liang S (2014) Citrobacter amalonaticus phytase on the cell surface of Pichia pastoris exhibits high pH stability as a promising potential feed supplement. PLoS One 9:e114728. doi:10.1371/journal.pone.0114728
46. Li RJ, Lu W-j, Guo C-j, Li XJ, Gu J-T, Xiao K (2012) Molecular characterization and functional analysis of OsPHY1, a purple acid phosphatase (PAP)-type phytase gene in rice (Oryza sativa L.) J Integr Agric 11:1217–1226. doi:10.1016/S2095-3119(12)60118-X
47. Li X, Wu Z, Li W, Yan R, Li L, Li J, Li Y, Li M (2007) Growth promoting effect of a transgenic Bacillus mucilaginosus on tobacco planting. Appl Microbiol Biotechnol 74:1120–1125. doi:10.1007/s00253-006-0750-6
48. Liu B-L, Jong C-H, Tzeng Y-M (1999) Effect of immobilization on pH and thermal stability of Aspergillus ficuum phytase. Enzym Microb Technol 25:517–521. doi:10.1016/S0141-0229(99)00076-9
49. Luangthongkam P, Fang L, Noomhorm A, Lamsal B (2015) Addition of cellulolytic enzymes and phytase for improving ethanol fermentation performance and oil recovery in corn dry grind process. Ind Crop Prod 77:803–808. doi:10.1016/j.indcrop.2015.09.060
50. Lung S-C, Chan W-L, Yip W, Wang L, Yeung EC, Lim BL (2005) Secretion of beta-propeller phytase from tobacco and Arabidopsis roots enhances phosphorus utilization. Plant Sci 169:341–349. doi:10.1016/j.plantsci.2005.03.006
51. Madeira JV, Macedo JA, Macedo GA (2011) Detoxification of castor bean residues and the simultaneous production of tannase and phytase by solid-state fermentation using Paecilomyces variotii. Bioresource Technol 102:7343–7348. doi:10.1016/j.biortech.2011.04.099
52. Maenz DD, Classen HL (1998) Phytase activity in the small intestinal brush border membrane of the chicken. Poult Sci 77:557–563. doi:10.1093/ps/77.4.557
53. Manobhavan M, Sridhar M, Ajith S, Shet D, Pal DT, Gowda NKS, Elangovan AV (2015) Efficacy of fungal phytase on growth performance and bone mineralization in broiler chicken. Anim Nutr Feed Techn 15:129–136. doi:10.5958/0974-181X.2015.00014.1
54. Marlida Y, Delfita R, Adnadi P, Ciptaan G (2010a) Isolation, characterization and production of phytase from endophytic fungus its application for feed. Pak J Nutr 9:471–474. doi:10.3923/pjn.2010.471.474
55. Marlida Y, Delfita R, Gusmanizar N, Ciptaan G (2010b) Identification characterization and production of phytase from endophytic fungi. World Acad Sci Eng Technol 65:1043–1046. doi:10.3923/pjn. 2010.471.474
56. Mayer AF, Hellmuth K, Schlieker H, Lopez-Ulibarri R, Oertel S, Dahlems U, Strasser AW, Van Loon AP (1999) An expression system matures: a highly efficient and cost-effective process for phytase production by recombinant strains of Hansenula polymorpha. Biotechnol Bioeng 63:373–381. doi:10.1002/(SICI)1097-0290(19990505)63:3<373::AID-BIT14>3.0.CO;2-T
57. Memenza M, Mostacero E, Camarena F, Zuniga D (2016) Disease control and plant growth promotion (PGP) of selected bacterial strains in Phaseolus vulgaris. In: Biological nitrogen fixation and beneficial plant-microbe interaction. Springer, pp 237–245.
58. Menezes-Blackburn D, Jorquera M, Gianfreda L, Rao M, Greiner R, Garrido E, de la Luz MM (2011) Activity stabilization of Aspergillus niger and Escherichia coli phytases immobilized on allophanic synthetic compounds and montmorillonite nanoclays. Bioresource Technol 102:9360–9367. doi:10.1016/j.biortech.2011.07.054
59. Mittal A, Gupta V, Singh G, Yadav A, Aggarwal NK (2013) Phytase: a boom in food industry. Octa J Biosci 1(2):158–169. doi:10.1007/s11248-007-9138-3. 9
60. Mittal A, Singh G, Goyal V, Yadav A, Aneja KR, Gautam SK, Aggarwal NK (2016) Isolation and biochemical characterization of acido-thermophilic extracellular phytase producing bacterial strain for potential application in poultry feed. Jundishapur J Microbiol 4(4):273–282
61. Mullaney EJ, Ullah AHJ (2005) Conservation of cysteine residues in fungal histidine acid phytases. Biochem Biophys Res Commun 328(2):404–408. doi:10.1016/j.bbrc.2004.12.181
62. Nakamura T, Suzuki T, Tokuda J, Kato N, Sakai Y, Mochizuki D, Takhashi H (1999) Secretory manufacture of Schwanniomyces occidentalis phytase using a Candida boidinii host. Eur Patent Appl Ep 931:837
63. Nampoothiri KM, Tomes GJ, Roopesh K, Szakacs G, Nagy V, Soccol CR, Pandey A (2004) Thermostable phytase production by Thermoascus aurantiacus in submerged fermentation. Appl Biochem Biotechnol 118:–214. doi:10.1385/ABAB:118:1–3:205
64. Nielsen PH, Wenzel H (2007) Environmental assessment of Ronozyme® P5000 CT phytase as an alternative to inorganic phosphate supplementation to pig feed used in intensive pig production. Int J LCA 12:514–520. doi:10.1065/lca2006.08.265.2
65. Niu C, Luo H, Shi P, Huang H, Wang Y, Yang P, Yao B (2016) 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 82:1004–1014. doi:10.1128/AEM.02881-15
66. Nuobariene L, Cizeikiene D, Gradzeviciute E, Hansen AS, Rasmussen SRK, Juodeikiene G, Vogensen FK (2015) Phytase-active lactic acid bacteria from sourdoughs: isolation and identification. LWT Food Sci Technol 63:766–772. doi:10.1016/j.lwt.2015.03. 018
67. Olczak M, Morawiecka B, Watorek W (2003) Plant purple acid phosphatases—genes, structures and biological function. Acta Biochim Pol 50(4):1245–1256
68. Onem H, Cicek S, Nadaroglu H (2016) Immobilization of a thermostable phytase from Pinar melkior (Lactarius piperatus) onto magnetite chitosan nanoparticles CyTA. J Food 14:74–83. doi:10.1080/19476337.2015
69. Pandey A (2016) Kluyveromyces lactis as a cell factory for secreted production of a thermostable phytase from fungal source. Paper presented at the INDO-US Workshop on Cell Factories, IIT Bombay, Mumbai, India, 18–20 March 2016
70. Pandey A, Szakacs G, Soccol CR, Rodriguez-Leon JA, Soccol VT (2001) Production, purification and properties of microbial phytases. Bioresource Technol 77:203–214
71. Parashar D, Satyanarayana T (2016) Enhancing the production of recombinant acidic α-amylase and phytase in Pichia pastoris under dual promoters [constitutive (GAP) and inducible (AOX)] in mixed fed batch high cell density cultivation. Process Biochem. doi:10.1016/j.procbio.2016.07.027
72. Parhamfar M, Badoei-Dalfard A, Khaleghi M, Hassanshahian M (2015) Purification and characterization of an acidic, thermophilic phytase from a newly isolated Geobacillus stearothermophilus strain DM12. Prog Biol Sci 5:61–73
73. Pasamontes L, Haiker M, Wyss M, Tessier M, Van Loon AP (1997) Gene cloning, purification, and characterization of a heat-stable phytase from the fungus Aspergillus fumigates. Appl Environ Microbiol 63:1696–1700
74. Phillippy BQ (2001) Stability of plant and microbial phytases. CRC Press, Boca Raton, FL
75. Rani R, Ghosh S (2011) Production of phytase under solid-state fermentation using Rhizopus oryzae: novel strain improvement approach and studies on purification and characterization. Bioresource Technol 102:10641–10649. doi:10.1016/j.biortech.2011. 08.075
76. Ranjan B, Satyanarayana T (2016) Recombinant HAP phytase of the thermophilic mold Sporotrichum thermophile: expression of the codon-optimized phytase gene in Pichia pastoris and applications. Mol Biotechnol 58:137–147. doi:10.1007/s12033-015-9909-7
77. Reddy CS, Achary VMM, Manna M, Singh J, Kaul T, Reddy MK (2015) Isolation and molecular characterization of thermostable phytase from Bacillus subtilis (BSPhyARRMK33). Appl Biochem Biotechnol 175(6):3058–3067. doi:10.1007/s12010-015-1487-4
78. Ribeiro Correa TL, de Queiroz MV, de Araajo EF (2015) Cloning, recombinant expression and characterization of a new phytase from Penicillium chrysogenum. Microbiol Res 170:205–212. doi:10.1016/j.micres.2014.06.005
79. Rishad KS, Rebello S, Nathan VK, Shabanamol S, Jisha MS (2016) Optimised production of chitinase from a novel mangrove isolate, Bacillus pumilus MCB-7 using response surface methodology. Biocatal Agric Biotechnol 5:143–149. doi:10.1016/j.bcab. 2016.01.009
80. Roongsawang N, Puseenam A, Kitikhun S, Sae-Tang K, Harnpicharnchai P, Ohashi T, Fujiyama K, Tirasophon W, Tanapongpipat S (2016) A novel potential signal peptide sequence and overexpression of ER-resident chaperones enhance heterologous protein secretion in thermotolerant methylotrophic yeast Ogataea thermomethanolica. Appl Biochem Biotechnol 178:710–724. doi:10.1007/s12010-015-1904-8
81. Roy MP, Mazumdar D, Dutta S, Saha SP, Ghosh S (2016) 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 11:e0145745. doi:10.1371/journal.pone.0145745
82. Roy S, Mehta A, Mishra RR (2013) Production and characterization of extracellular phytase: an industrial enzyme Vegetos. Int J Plant Res 26:83–87. doi:10.5958/j.2229-4473.26.1.012
83. Salmon DNX, Fendrich RC, Cruz MA, Montibeller VW, Vandenberghe LPS, Soccol CR, Spier MR (2016) Bioprocess for phytase production by Ganoderma sp. MR-56 in different types of bioreactors through submerged cultivation. Biochem Eng J. doi:10.1016/j.bej.2016.07.015
84. Sano K, Fukuhara H, Nakamura Y (1999) Phytase of the yeast Arxula adeninivorans. Biotechnol Lett 21:33–38. doi:10.1023/A:1005438121763
85. Sato VS, Jorge JA, Guimaraes LHS (2016) Characterization of a thermotolerant phytase produced by Rhizopus microsporus var. microsporus biofilm on an inert support using sugarcane bagasse as carbon source. Appl Biochem Biotechnol 179:610–624. doi:10.1007/s12010-016-2018-7
86. Schoene C, Bennett SP, Howarth M (2016) SpyRing interrogation: analyzing how enzyme resilience can be achieved with phytase and distinct cyclization chemistries. Sci Rep 6:21151. doi:10.1038/ srep21151
87. Shetty JK, Paulson B, Pepsin M, Chotani G, Dean B, Hruby M (2008) Phytase in fuel ethanol production offers economical and environmental benefits. Int Sugar J 110(1311):160–174
88. Singh B, Kunze G, Satyanarayana T (2011) Developments in biochemical aspects and biotechnological applications of microbial phytases. Biotechnol Mol Biol Rev 6:69–87
89. Singh B, Satyanarayana T (2014) Fungal phytases: characteristics and amelioration of nutritional quality and growth of non-ruminants. J Anim Physiol Anim Nutr 99:646–660. doi:10.1111/jpn.12236
90. Speight R Biotechnology in the development of improved phytases. In: 27th Annual Australian Poultry Science Symposium, Sydney, N.S.W., 14–17 February 2016.
91. Tan H, Wu X, Xie L, Huang Z, Peng W, Gan B (2016) Identification and characterization of a mesophilic phytase highly resilient to high-temperatures from a fungus-garden associated metagenome. Appl Microbiol Biotechnol 100:2225–2241. doi:10.1007/s00253-015-7097-9
92. Tan WQ, Yee PC, Chin SC, Chin YB, Vui LC, Abdullah N, Radu S, Wan HY (2015) Cloning of a novel phytase from an anaerobic rumen bacterium, Mitsuokella jalaludinii, and its expression in Escherichia coli. J Integr Agric 14:1816–1826. doi:10.1016/S2095-3119(14)60960-6
93. Tomschy A, Brugger R, Lehmann M, Svendsen A, Vogel K, Kostrewa D, Lassen SF, Burger D, Kronenberger A, van Loon AP, Pasamontes L (2002) Engineering of phytase for improved activity at low pH. Appl Environ Microbiol 68:1907–1913. doi:10.1128/AEM.68.4.1907-1913.2002
94. Tran TT, Hashim SO, Gaber Y, Mamo G, Mattiasson B, Hatti-Kaul R (2011) Thermostable alkaline phytase from Bacillus sp. MD2: effect of divalent metals on activity and stability. J Inorg Biochem 105:1000–1007. doi:10.1016/j.jinorgbio.2011.04.005
95. Tran TT, Mamo G, Mattiasson B, Hatti-Kaul R (2010) A thermostable phytase from Bacillus sp. MD2: cloning, expression and high-level production in Escherichia coli. J Ind Microbiol Biotechnol 37:279–287
96. Ushasree MV, Sumayya HBS, Pandey A (2011) Adopting structural elements from intrinsically stable phytase--a promising strategy towards thermostable phytases. Indian J Biotechnol 10:458–467
97. Ushasree MV, Vidya J, Pandey A (2014) Extracellular expression of a thermostable phytase (phyA) in Kluyveromyces lactis. Process Biochem 49:1440–1447
98. Vats P, Banerjee UC (2004) Production studies and catalytic properties of phytases (myo-inositol hexakisphosphate phosphohydrolases): an overview. Enzy Microb Technol 35:3–14. doi:10.1016/j.enzmictec.2004.03.010
99. Viader-Salvado JM, Gallegos-Lopez JA, Carreon-Trevino JG, Castillo-Galvan M, Rojo-Dominguez A, Guerrero-Olazaran M (2010) Design of thermostable beta-propeller phytases with activity over a broad range of pHs and their overproduction by Pichia pastoris. Appl Environ Microbiol 76:6423–6430. doi:10.1128/AEM.00253-10
100. Vihnudas J, Jojula M, Singaracharya MA (2012) A culturing of fungi for phytase production by solid state from different sources. Curr World Environ 7:187–190
101. Vincent JB, Crowder MW, Averill BA (1992) Hydrolysis of phosphate monoesters: a biological problem with multiple chemical solutions. Trends Biochem Sci 17(3):105–110. doi:10.1016/0968-0004(92)90246-6
102. Vishnupriya CS, Sunish KS, Rebello S (2016) Molecular characterisation of alkaline protease producing Bacillus subtilis from soil. Int J Res Pharm Chem 6:485–490
103. Wulandari R, Sari EN, Ratriyanto A, Weldekiros H, Greiner R (2015) Phytase-producing bacteria from extreme regions in Indonesia. Braz Arch Biol Technol 58:711–717. doi:10.1590/S1516-89132015050173
104. Wyss M, Pasamontes L, Rémy R, Kohler J, Kusznir E, Gadient M, Muller F, van Loon AP (1998) Comparison of the thermostability properties of three acid phosphatases from molds: Aspergillus fumigates phytase, A. niger phytase, and A. niger pH 2.5 acid phosphatase. Appl Environ Microbiol 64:4446–4451
105. Yan M, Yu L, Zhang L, Guo Y, Dai K, Chen Y (2014) Phosphatase activity and culture conditions of the yeast Candida mycoderma sp. and analysis of organic phosphorus hydrolysis ability. J Environ Sci 26:2315–2321. doi:10.1016/j.jes.2014.09.008
106. Yao M-Z, Zhang Y-H, Lu W-L, Hu M-Q, Wang W, Liang A-H (2012) Phytases: crystal structures, protein engineering and potential biotechnological applications. J Appl Microbiol 112:1–14. doi:10.1111/j. 1365–2672.2011.05181.x
107. Yip W, Wang L, Cheng C, Wu W, Lung S, Lim B-L (2003) The introduction of a phytase gene from Bacillus subtilis improved the growth performance of transgenic tobacco. Biochem Biophys Res Commun 310:1148–1154. doi:10.1016/ j.bbrc.2003.09.136
108. Yu P, Chen Y (2013) Purification and characterization of a novel neutral and heat-tolerant phytase from a newly isolated strain Bacillus nealsonii ZJ0702. BMC Biotechnol 13:78. doi:10.1186/1472-6750-13-78
109. Zhang W, Mullaney EJ, Lei XG (2007) Adopting selected hydrogen bonding and ionic interactions from Aspergillus fumigatus phytase structure improves the thermostability of Aspergillus niger PhyA phytase. Appl Environ Microbiol 73:3069–3076. doi:10.1128/AEM.02970-06
110. Zhao Q, Liu H, Zhang Y, Zhang Y (2010) Engineering of protease-resistant phytase from Penicillium sp.: high thermal stability, low optimal temperature and pH. J Biosci Bioeng 110:638–645. doi:10.1016/j.jbiosc. 2010.08.003
111. Zhou X-L, Shen W, Zhuge J, Wang Z-X (2006) Biochemical properties of a thermostable phytase from Neurospora crassa. FEMS Microbiol Lett 258:61–66. doi:10.1111/j.1574-6968.2006.00205.x