Abstract
Arginine decarboxylase (ADC) catalyzes the decarboxylation of arginine to form agmatine, an important physiological and pharmacological amine, and attracts attention to the enzymatic production of agmatine. In this study, we for the first time overexpressed and characterized the marine Shewanella algae ADC (SaADC) in Escherichia coli. The recombinant SaADC showed the maximum activity at pH 7.5 and 40 °C. The SaADC displayed previously unreported substrate inhibition when the substrate concentration was higher than 50 mM, which was the upper limit of testing condition in other reports. In the range of 1–80 mM l-arginine, the SaADC showed the Km, kcat, Ki, and kcat/Km values of 72.99 ± 6.45 mM, 42.88 ± 2.63 s−1, 20.56 ± 2.18 mM, and 0.59 s/mM, respectively, which were much higher than the Km (14.55 ± 1.45 mM) and kcat (12.62 ± 0.68 s−1) value obtained by assaying at 1–50 mM l-arginine without considering substrate inhibition. Both the kcat values of SaADC with and without substrate inhibition are the highest ones to the best of our knowledge. This provides a reference for the study of substrate inhibition of ADCs.
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Xu, W., Gao, L., Li, T., Shao, A., & Zhang, J. (2018). Neuroprotective role of agmatine in neurological diseases. Current Neuropharmacology, 16, 1296–1305.
Schafer, U., Raasch, W., Qadri, F., Chun, J., & Dominiak, P. (1999). Effects of agmatine on the cardiovascular system of spontaneously hypertensive rats. Annals of the New York Academy of Sciences, 881, 97–101.
Gong, Z. H., Li, Y. F., Zhao, N., Yang, H. J., Su, R. B., Luo, Z. P., & Li, J. (2006). Anxiolytic effect of agmatine in rats and mice. European Journal of Pharmacology, 550, 112–116.
Neis, V. B., Manosso, L. M., Moretti, M., Freitas, A. E., Daufenbach, J., & Rodrigues, A. L. (2014). Depressive-like behavior induced by tumor necrosis factor-alpha is abolished by agmatine administration. Behavioural Brain Research, 261, 336–344.
El-Agamy, D. S., Makled, M. N., & Gamil, N. M. (2014). Protective effects of agmatine against D-galactosamine and lipopolysaccharide-induced fulminant hepatic failure in mice. Inflammopharmacology, 22, 187–194.
Bornscheuer, U. T., Huisman, G. W., Kazlauskas, R. J., Lutz, S., Moore, J. C., & Robins, K. (2012). Engineering the third wave of biocatalysis. Nature, 485, 185–194.
Wang, X., Ying, W., Dunlap, K. A., Lin, G., Satterfield, M. C., Burghardt, R. C., Wu, G., & Bazer, F. W. (2014). Arginine decarboxylase and agmatinase: An alternative pathway for de novo biosynthesis of polyamines for development of mammalian conceptuses. Biology of Reproduction, 90, 1–15.
Molderings, G. J., & Haenisch, B. (2012). Agmatine (decarboxylated L-arginine): Physiological role and therapeutic potential. Pharmacology & Therapeutics, 133, 351–365.
Lin, J., Lee, I. S., Frey, J., Slonczewski, J. L., & Foster, J. W. (1995). Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. Journal of Bacteriology, 177, 4097–4104.
Michael, A. J. (2016). Biosynthesis of polyamines and polyamine-containing molecules. Biochemical Journal, 473, 2315–2329.
Peremarti, A., Bassie, L., Zhu, C., Christou, P., & Capell, T. (2010). Molecular characterization of the Arginine decarboxylase gene family in rice. Transgenic Research, 19, 785–797.
Bliven, K. A., Fisher, D. J., & Maurelli, A. T. (2012). Characterization of the activity and expression of arginine decarboxylase in human and animal Chlamydia pathogens. FEMS Microbiology Letters, 337, 140–146.
Forouhar, F., Lew, S., Seetharaman, J., Xiao, R., Acton, T. B., Montelione, G. T., & Tong, L. (2010). Structures of bacterial biosynthetic arginine decarboxylases. Acta Crystallographica Section F Structural Biology and Crystallization Communications, 66, 1562–1566.
Wu, W. H., & Morris, D. R. (1973). Biosynthetic arginine decarboxylase from Escherichia coli. Subunit interactions and the role of magnesium ion. Journal of Biological Chemistry, 248, 1696–1699.
Toney, M. D. (2011). Controlling reaction specificity in pyridoxal phosphate enzymes. Biochimica et Biophysica Acta, 1814, 1407–1418.
Lin, Y. L., & Gao, J. (2010). Internal proton transfer in the external pyridoxal 5’-phosphate Schiff base in dopa decarboxylase. Biochemistry, 49, 84–94.
Sun, A., Song, W., Qiao, W., Chen, X., Liu, J., Luo, Q., & Liu, L. (2017). Efficient agmatine production using an arginine decarboxylase with substrate-specific activity. Journal of Chemical Technology & Biotechnology, 92, 2383–2391.
Zhang, C., & Kim, S. K. (2010). Research and application of marine microbial enzymes: Status and prospects. Marine Drugs, 8, 1920–1934.
Fernandes, P. (2014). Marine enzymes and food industry: Insight on existing and potential interactions. Frontiers in Marine Science, 1, 46.
Stach, J. E., Maldonado, L. A., Ward, A. C., Goodfellow, M., & Bull, A. T. (2003). New primers for the class Actinobacteria: Application to marine and terrestrial environments. Environmental Microbiology, 5, 828–841.
Imhoff, J. F., Labes, A., & Wiese, J. (2011). Bio-mining the microbial treasures of the ocean: New natural products. Biotechnology Advances, 29, 468–482.
Bull, A. T., Ward, A. C., & Goodfellow, M. (2000). Search and discovery strategies for biotechnology: The paradigm shift. Microbiology and Molecular Biology Reviews, 64, 573–606.
Birolli, W. G., Lima, R. N., & Porto, A. L. M. (2019). Applications of marine-derived microorganisms and their enzymes in biocatalysis and biotransformation, the underexplored potentials. Frontiers in Microbiology, 10, 1453.
Tseng, S. Y., Liu, P. Y., Lee, Y. H., Wu, Z. Y., Huang, C. C., Cheng, C. C., & Tung, K. C. (2018). The pathogenicity of shewanella algae and ability to tolerate a wide range of temperatures and salinities. Canadian Journal of Infectious Diseases and Medical Microbiology, 2018, 1–9.
Bauer, M. J., Stone-Garza, K. K., Croom, D., Andreoli, C., Woodson, P., Graf, P. C. F., & Maves, R. C. (2019). Shewanella algae Infections in United States Naval Special Warfare Trainees. Open Forum Infectious Diseases, 6, ofz442.
Goldschmidt, M. C., & Lockhart, B. M. (1971). Simplified rapid procedure for determination of agmatine and other guanidino-containing compounds. Analytical Chemistry, 43, 1475–1479.
Song, J., Zhou, C., Liu, R., Wu, X., Wu, D., Hu, X., & Ding, Y. (2010). Expression and purification of recombinant arginine decarboxylase (speA) from Escherichia coli. Molecular Biology Reports, 37, 1823–1829.
Alam, M., Srivastava, A., Dutta, A., & Sau, A. K. (2018). Biochemical and biophysical studies of Helicobacter pylori arginine decarboxylase, an enzyme important for acid adaptation in host. International Union of Biochemistry & Molecular Biology Life, 70, 658–669.
Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46, W296–W303.
Guex, N., Peitsch, M. C., & Schwede, T. (2009). Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective. Electrophoresis, 30(Suppl 1), S162-173.
Deng, X., Lee, J., Michael, A. J., Tomchick, D. R., Goldsmith, E. J., & Phillips, M. A. (2010). Evolution of substrate specificity within a diverse family of beta/alpha-barrel-fold basic amino acid decarboxylases: X-ray structure determination of enzymes with specificity for L-arginine and carboxynorspermidine. Journal of Biological Chemistry, 285, 25708–25719.
Burrell, M., Hanfrey, C. C., Murray, E. J., Stanley-Wall, N. R., & Michael, A. J. (2010). Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. Journal of Biological Chemistry, 285, 39224–39238.
Sun, X., Song, W., & Liu, L. M. (2015). Enzymatic production of agmatine by recombinant arginine decarboxylase. Journal of Molecular Catalysis B-Enzymatic, 121, 1–8.
Balbo, P. B., Patel, C. N., Sell, K. G., Adcock, R. S., Neelakantan, S., Crooks, P. A., & Oliveira, M. A. (2003). Spectrophotometric and steady-state kinetic analysis of the biosynthetic arginine decarboxylase of Yersinia pestis utilizing arginine analogues as inhibitors and alternative substrates. Biochemistry, 42, 15189–15196.
Sun, X., Song, W., & Liu, L. (2015). Enzymatic production of agmatine by recombinant arginine decarboxylase. Journal of Molecular Catalysis B: Enzymatic, 121, 1–8.
Shah, R., Akella, R., Goldsmith, E. J., & Phillips, M. A. (2007). X-ray structure of Paramecium bursaria Chlorella virus arginine decarboxylase: Insight into the structural basis for substrate specificity. Biochemistry, 46, 2831–2841.
Osterman, A. L., Brooks, H. B., Jackson, L., Abbott, J. J., & Phillips, M. A. (1999). Lysine-69 plays a key role in catalysis by ornithine decarboxylase through acceleration of the Schiff base formation, decarboxylation, and product release steps. Biochemistry, 38, 11814–11826.
Acknowledgements
This work was financially supported by the Demonstration Project of Innovation and Development for Marine Economy of Beihai “The 13th Five-Year Plan” (Bhsfs010-4), Guangxi Natural Science Foundation (AD18281064) and the Guangxi Science and Technology Major Special Project (AA17204075).
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Pei, XD., Lu, LH., Yue, SY. et al. Characterization of a Novel Shewanella algae Arginine Decarboxylase Expressed in Escherichia coli. Mol Biotechnol 64, 57–65 (2022). https://doi.org/10.1007/s12033-021-00397-6
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DOI: https://doi.org/10.1007/s12033-021-00397-6