Abstract
This work intended to prospect new phytase-producing organisms. In silico genomic analyses allowed the selection of twelve potential phytase-producing fungi. Based on gene sequence, it was possible to identify four well-defined groups of phytate-degrading enzymes: esterase-like, β-propeller phytases (βPP), phosphoglycerate mutase-like, and phytases of the histidine acid phosphatases (HAP) family. Analysis of the predicted genes encoding phytases belonging to the HAP family and βPP phytases and in silico characterization of these enzymes indicated divergence among the catalytic activities. Predicted fungal βPP phytases exhibited higher molecular mass (around 77 kDa) probably due to the epidermal growth factor-like domain. Twelve sequences of phytases contained signal peptides, of which seven were classified as HAP and five as βPP phytases, while ten sequences were predicted as phytases secreted by non-classical pathways. These fungi were grown in liquid or semi-solid medium, and the fungal enzymatic extracts were evaluated for their ability to hydrolyze sodium phytate at 50 °C and pH ranging from 2.0 to 9.0. Seven fungi were identified as phytase producers based on phosphate release under enzyme assay conditions. Results obtained from in silico analyses combining experimental enzymatic activities suggest that some selected fungi could secrete βPP phytases and HAP phytases.
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References
Singh, B., Kunze, G., & Satyanarayana, T. (2011). Biotechnology and Molecular Biology Reviews, 6(3), 69–87.
Raboy, V. (2003). Phytochemistry, 64, 1033–1043.
Vohra, A., & Satyanarayana, T. (2003). Critical Reviews in Biotechnology, 23, 29–60.
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. Journal of Bioscience and Bioengineering, 110(6), 638–645.
Singh, B. (2013). Microbiology and Biotechnology, 40(8), 891–899.
Vats, P., Bhattacharyya, M. S., & Banerjee, U. C. (2005). Critical Reviews in Environmental Science and Technology, 35(5), 469–486.
Nelson, T.S. (1976). The hydrolysis of phytate phosphorus by chicks and laying hens. Poultry Science. 55(6), 2262–2264.
Belho, K., Nongpiur, S. R., & Ambasht, P. K. (2016). Journal of Plant Biochemistry and Biotechnology, 25, 327–330. 32.
Muslim, S. N., Mohammed Ali, A. N., Al-Kadmy, I. M. S., Khazaal, S. S., Ibrahim, S. A., Al-Saryi, N. A., Al-Saadi, L. G., Muslim, S. N., Salman, B. K., & Aziz, S. N. (2018). Screening, nutritional optimization and purification for phytase produced by Enterobacter aerogenes and its role in enhancement of hydrocarbons degradation and biofilm inhibition. Microbial Pathogenesis, 115, 159–167.
Neira-Vielma A. A., Aguilar C. N., Ilyina A., Contreras-Esquivel J. C., Carneiro da-Cunha M. G., Michelena-Álvarez G., & Martínez-Hernández J. L (2018). Biotechnol Reports. Amsterdam, Netherlands. 17, p.49–54.
Sarrouh, B., Santos, T. M., Miyoshi, A., Dias, R., Azevedo, V. (2012). Up-to-date insight on industrial enzymes applications and global market. Journal of Bioprocessing & Biotechniques. S4:002. https://doi.org/10.4172/2155-9821.S4-002.
Ushasree, M. V., Jaiswal, A. K., Krishna, S., & Pandey, A. (2019). Bioresource Technology, 278, 400–407.
Cowieson, A. J., Wilcock, P., & Bedford, M. R. (2011). World's Poultry Science Journal, 67, 225–236.
Shanmugam, G. (2018). International Journal of Current Microbiology and Applied Sciences, 7(3), 1006–1013.
Bhavsar, K., Buddhiwant, P., Soni, S. K., Depan, D., Sarkar, S., & Khire, J. M. (2013). Process Biochemistry, 48, 1618–1625.
Awad, G. E., Helal, M. M., Danial, E. N., & Esawy, M. A. (2014). Saudi Journal of Biological Sciences, 21, 81–88.
Bujna, E., Rezessy-Szabó, J. M., Nguyen, D. V., & Nguyen, D. Q. (2016). Mycosphere, 7(10), 1576–1587.
Shahryari, Z., Fazaelipoor, M. H., Setoodeh, P., Nair, R. B., Mohammad, J., Taherzadeh, M. J., & Ghasemi, Y. (2018). International Journal of Recycling of Organic Waste in Agriculture, 7, 345–355.
Song, H. Y., Sheikha, A. F., & Hu, D. M. (2019). Trends in Food Science and Technology, 86, 553–562.
Lim, D., Golovan, S., Forsberg, C. W., & Jia, Z. (2000). Crystal structures of Escherichia coli phytase and its complex with phytate. Nature Structural Biology, 7(2), 108–113.
Oh, B. C., Kim, M. H., Yun, B. S., Choi, W. C., Park, S. C., Bae, S. C., & Oh, T. K. (2006). Biochem., 45, 9531–9539.
Ha, N. C., Oh, B. C., Shin, S., Kim, H. J., Oh, T. K., Kim, Y. O., Choi, K. Y., & Oh, B. H. (2000). Nature Structural & Molecular Biology, 7, 147–153.
Bhadouria, J., Singh, A. P., Mehra, P., Verma, L., Srivastawa, R., Parida, S. K., & Giri, J. (2017). Scientific Reports, 7, 11012.
Antonyuk, S. V., Olczak, M., Olczak, T., Ciuraszkiewicz, J., & Strange, R. W. (2014). Biology and Medicine, 1, 101–109.
Puhl, A. A., Greiner, R., & Selinger, L. B. (2008). The International Journal of Biochemistry & Cell Biology, 40, 2053–2064.
Kimati, H., Amorim, L., Rezende, J.A.M., Bergamin Filho, A., Camargo. L.E.A. (2005). ed. Manual de Fitopatologia. Volume 2. 4ª Ed. Ed. Agronômica Ceres Ltda. SP. p.666.
Stanke, M., & Morgenstern, B. (2005). AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Research, 33(Web Server issue), W465–W467.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.
Potter, S. C., Luciani, A., Eddy, S. R., Park, Y., Lopez, R., & Finn, R. D. (2018). Nucleic Acids Research Web Server Issue, 46, W200–W204.
Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., & Hochstrasser, D. F. (1999). Methods in Molecular Biology, 112, 531–552.
Gupta, R., Jung, E., & Brunak, S. (2004). Prediction of N-glycosylation sites in human proteins. http://www.cbs.dtu.dk/services/NetNGlyc/.
Stultz, C. M., White, J. M., & Smith, T. F. (1993). Structural analysis based on state-space modeling. Protein Science, 2(3), 305–314.
Petersen, T. N., Brunak, S., Von Heijne, G., & Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods., 8(10), 785–786.
Krogh, A., Larsson, B., Von Heijne, G., & Sonnhammer, E. L. L. (2001). Journal of Molecular Biology, 305(3), 567–580.
McWilliam, H., Li, W., Uludag, M., Squizzato, S., Ym, P., Buso, N., Cowley, A., & Lopez, R. (2013). Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Research, 41(Web Server issue), W597–W600.
Oakley, A. J. (2010). Biochemical and Biophysical Research Communications, 397(4), 745–749.
Ragon, M., Hoh, F., Aumelas, A., Chiche, L., Moulin, G., & Boze, H. (2009). Acta Crystallographica Section F, 65, 321–326.
Zeng, Y. F., Ko, T. P., Lai, H. L., Cheng, Y. S., Wu, T. H., Ma, Y., Chen, C. C., Yang, C. S., Cheng, K. J., Huang, C. H., Guo, R. T., & Liu, J. R. (2011). Journal of Molecular Biology, 409, 214–224.
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2), 111–120.
Kruskal J., & Wish M. (1978). Multidimensional Scaling. Sage Publications, Beverly Hills, California. https://doi.org/10.4135/9781412985130.
Young F, Hamer R. (1987). Lawrence Erlbaum Associates, Hillsdale.
Team R. C. (2013). A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M., & Barton, G. J. (2009). Bioinformatics, 25, 1189–1191.
Gunashree, B., & Venkateswaran, G. (2008). Journal of Industrial Microbiology & Biotechnology, 35, 1587–1596.
Monteiro, P. S., De Melo, R. R., Tavares, M. P., Falkoski, D. L., Guimarães, V. M., Pereira, O. L., & Rezende, S. T. (2012). Revista Brasileira de Agrociên, 18(2-4), 117–132.
Heinonen, J. K., & Lahti, R. J. (1981). A new and convenient colorimetric determination of inorganic orthophosphate and its application to the assay of inorganic pyrophosphatase. Analytical Biochemistry, 113(2), 313–317.
Taussky, H. H., & Skorr, E. (1953). The Journal of Biological Chemistry, 202, 675–685.
Bradford, M. M. (1976). Analytical Biochemistry, 72, 248–254.
Rigden, D. J. (2008). Biochemical Journal, 409, 333–348.
Sacco, F., Perfetto, L., Castagnoli, L., & Cesareni, G. (2012). Letras FEBS, 586(17), 2732–2739.
Singh, B., Sharma, K. K., Amit Kumari, A., Anil Kumar, A., & Gakhar, S. K. (2018). International Journal of Biological Macromolecules, 115, 501–508.
Zhang, H., Yang, L., Ding, W., & Ma, Y. (2018). The Journal of Physical Chemistry B, 122(30), 7530–7538.
Fan, C. M., Wang, Y. H., Fu, C. Y., & Zheng, Y. F. (2013). African Journal of Biotechnology, 12, 1138–1147.
Balaban, N. P., Suleimanovaa, A. D., Shakirova, E. V., & Sharipovaa, M. R. (2018). Microbiology, 87(6), 745–756.
Balaban, N. P., Suleimanova, A. D., Valeeva, L. R., Shakirov, E. V., & Sharipova, M. R. (2016). Biochemistry, 81(8), 785–793.
Kumar, V., Yadav, A. N., Verma, P., Sangwan, P., Saxena, A., Kumar, K., & Singh, B. (2017). International Journal of Biological Macromolecules, 98, 595–609.
Sanangelantoni, A. M., Malatrasi, M., Trivelloni, E., Visioli, G., & Agrimonti, C. (2018). Applied Microbiology and Biotechnology, 102, 8351–8358. https://doi.org/10.1007/s00253-018-9248-2.
Puppala, K. R., Naik, T., Shaik, A., Dastager, S., Kumar, V. R., & Dharne, M. (2018). Biocatalysis and Agricultural Biotechnology, 13, 225–235.
Azeke, M. A., Greiner, R., & Jany, K. D. (2010). Journal of Food Biochemistry, 35(1), 213–237.
Nickel, W., & Seedorf, M. (2008). Annual Review of Cell and Developmental Biology, 24, 287–308. https://doi.org/10.1146/annurev.cellbio.24.110707.175320.
Niu, C., Luo, H., Shi, P., Huang, H., Wang, Y., Yang, P., & Yao, B. (2015). Applied and Environmental Microbiology, 82, 1004–1014.
Wang, X. Y., Meng, F. G., & Zhou, H. M. (2004). Biochemistry and Cell Biology, 82, 329–334.
Kumar, V., Singh, P., Jorquera, M. A., Sangwan, P., Kumar, P., Verma, A. K., & Agrawal, S. (2013). World Journal of Microbiology and Biotechnology, 29(8), 1361–1369.
Boukhris, I., Farhat-Khemakhem, A., Blibech, M., Bouchaala, K., & Chouayekh, H. (2015). International Journal of Biological Macromolecules, 80, 581–587.
Kumar, V., Sangwan, P., Verma, A. K., & Agrawal, S. (2014). Applied Biochemistry and Biotechnology, 173(2), 646–659.
Oh, B. C., Chang, B. S., Park, K. H., Ha, N. C., Kim, H. K., Oh, B. H., & Oh, T. K. (2001). Biochemistry, 40, 9669–9676.
Borgi, M. A., Khila, M., Boudebbouze, S., Aghajari, N., Szukala, F., Pons, N., Maguin, E., & Rhimi, M. (2014). Applied Microbiology and Biotechnology, 98, 5937–5947.
Verma, A., Singh, V. K., & Gaur, S. (2016). Computational Biology and Chemistry, 60, 53–58.
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We acknowledge the Brazilian institutions CAPES for the scholarship granted to the first author, FAPEMIG, and CNPq for the resources provided to complete this study.
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Ferreira, R.C., Tavares, M.P., Morgan, T. et al. Genome-Scale Characterization of Fungal Phytases and a Comparative Study Between Beta-Propeller Phytases and Histidine Acid Phosphatases. Appl Biochem Biotechnol 192, 296–312 (2020). https://doi.org/10.1007/s12010-020-03309-7
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DOI: https://doi.org/10.1007/s12010-020-03309-7