Regulatory role of cysteines in (2R, 3R)-butanediol dehydrogenase BdhA of Bacillus velezensis strain GH1-13

Journal of Microbiology - Tập 60 - Trang 411-418 - 2022
Yunhee Choi1, Yong-Hak Kim2
1Agricultural Microbiology Division, National Institute of Agricultural Science, Rural Development Administration, Wanju, Republic of Korea
2Department of Microbiology, Daegu Catholic University School of Medicine, Daegu, Republic of Korea

Tóm tắt

Bacillus velezensis strain GH1-13 contains a (2R,3R)-butanediol dehydrogenase (R-BDH) BdhA which converts acetoin to R-BD reversibly, however, little is known about its regulatory cysteine and biological significance. We performed site-directed mutation of three cysteines in BdhA. The C37S mutant had no enzyme activity and the C34S and C177S mutants differed from each other and wild type (WT). After zinc affinity chromatography, 1 mM ZnCl2 treatment resulted in a 3-fold enhancement of the WT activity, but reduced activity of the C34S mutant by more than 2 folds compared to the untreated ones. However, ZnCl2 treatment did not affect the activity of the C177S mutant. Most of the double and triple mutant proteins (C34S/C37S, C34S/C177S, C37S/C177S, and C34S/C37S/C177S) were aggregated in zinc resins, likely due to the decreased protein stability. All of the purified WT and single mutant proteins increased multiple intermolecular disulfide bonds in the presence of H2O2 as the buffer pH decreased from 7.5 to 5.5, whereas an intramolecular disulfide bond of cysteine 177 and another cysteine in the CGIC motif region was likely formed at pH higher than pKa of 7.5. When pH varied, WT and its C34S or C177S mutants reduced acetoin to R-BD at the optimum pH 5.5 and oxidized R-BD to acetoin at the optimum pH 10. This study demonstrated that cysteine residues in BdhA play a regulatory role for the production of acetoin and R-BD depending on pH as well as metal binding and oxidative stress.

Tài liệu tham khảo

Aleti, G., Sessitsch, A., and Brader, G. 2015. Genome mining: prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Comput. Struct. Biotechnol. J. 13, 192–203. Arnaouteli, S., Ferreira, A.S., Schor, M., Morris, R.J., Bromley, K.M., Jo, J., Cortez, K.L., Sukhodub, T., Prescott, A.R., Dietrich, L., et al. 2017. Bifunctionality of a biofilm matrix protein controlled by redox state. Proc. Natl. Acad. Sci. USA 114, E6184–E6191. Baker, P.J., Britton, K.L., Fisher, M., Esclapez, J., Pire, C., Bonete, M.J., Ferrer, J., and Rice, D.W. 2009. Active site dynamics in the zinc-dependent medium chain alcohol dehydrogenase superfamily. Proc. Natl. Acad. Sci. USA 106, 779–784. Bao, T., Zhang, X., Rao, Z., Zhao, X., Zhang, R., Yang, T., Xu, Z., and Yang, S. 2014. Efficient whole-cell biocatalyst for acetoin production with NAD+ regeneration system through homologous co-expression of 2,3-butanediol dehydrogenase and NADH oxidase in engineered Bacillus subtilis. PLoS ONE 9, e102951. Bednar, R.A. 1990. Reactivity and pH dependence of thiol conjugation to N-ethylmaleimide: detection of a conformational change in chalcone isomerase. Biochemistry 29, 3684–3690. Blessing, H., Kraus, S., Heindl, P., Bal, W., and Hartwig, A. 2004. Interaction of selenium compounds with zinc finger proteins involved in DNA repair. Eur. J. Biochem. 271, 3190–3199. Celińska, E. and Grajek, W. 2009. Biotechnological production of 2,3-butanediol-current state and prospects. Biotechnol. Adv. 27, 715–725. Chan, Y.A., Podevels, A.M., Kevany, B.M., and Thomas, M.G. 2009. Biosynthesis of polyketide synthase extender units. Nat. Prod. Rep. 26, 90–114. Choi, Y., Pham, H., Nguyen, M.P., Tran, L.V.H., Kim, J., Kim, S., Lee, C.W., Song, J., and Kim, Y.H. 2021. A native conjugative plasmid confers potential selective advantages to plant growth-promoting Bacillus velezensis strain GH1-13. Commum. Biol. 4, 582. Collet, J.F., D’Souza, J.C., Jakob, U., and Bardwell, J.C.A. 2003. Thioredoxin 2, an oxidative stress-induced protein, contains a high affinity zinc binding site. J. Biol. Chem. 278, 45325–45332. Deponte, M. 2013. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 1830, 3217–3266. Dwyer, D.S. 2005. Electronic properties of amino acid side chains: quantum mechanics calculation of substituent effects. BMC Chem. Biol. 5, 2. Elmahmoudy, M., Elfeky, N., Zhongji, P., Zhang, Y., and Bao, Y. 2021. Identification and characterization of a novel 2R,3R-Butanediol dehydrogenase from Bacillus sp. DL01. Electron. J. Biotechnol. 49, 56–63. Esteban-Torres, M., Alvarez, Y., Acebrón, I., de las Rivas, B., Muñoz, R., Kohring, G.W., Roa, A.M., Sobrino, M., and Mancheño, J.M. 2012. The crystal structure of galactitol-1-phosphate 5-dehydrogenase from Escherichia coli K12 provides insights into its anomalous behavior on IMAC processes. FEBS Lett. 586, 3127–3133. Fan, B., Wang, C., Song, X., Ding, X., Wu, L., Wu, H., Gao, X., and Borriss, R. 2018. Bacillus velezensis FZB42 in 2018: the Grampositive model strain for plant growth promotion and biocontrol. Front. Microbiol. 9, 2491. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. 2011. Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem. Res. Toxicol. 24, 434–450. Fomenko, D.E. and Gladyshev, V.N. 2003. Genomics perspective on disulfide bond formation. Antioxid. Redox Signal. 5, 397–402. Fomenko, D.E., Marino, S.M., and Gladyshev, V.N. 2008. Functional diversity of cysteine residues in proteins and unique features of catalytic redox-active cysteines in thiol oxidoreductases. Mol. Cells 26, 228–235. Fu, J., Huo, G., Feng, L., Mao, Y., Wang, Z., Ma, H., Chen, T., and Zhao, X. 2016. Metabolic engineering of Bacillus subtilis for chiral pure meso-2,3-butanediol production. Biotechnol. Biofuels 9, 90. Giles, N.M., Watts, A.B., Giles, G.I., Fry, F.H., Littlechild, J.A., and Jacob, C. 2003. Metal and redox modulation of cysteine protein function. Chem. Biol. 10, 677–693. Gong, F.Q., Liu, Q.S., Tan, H.D., Li, T., Tan, C.U., and Yin, H. 2019. Cloning, expression and characterization of a novel (2R,3R)-2,3-butanediol dehydrogenase from Bacillus thuringiensis. Biocat. Agric. Biotechnol. 22, 101372. González, E., Fernández, M.R., Larroy, C., Solà, L., Pericàs, M.A., Parés, X., and Biosca, J.A. 2000. Characterization of a (2R,3R)-2,3-butanediol dehydrogenase as the Saccharomyces cerevisiae YAL060W gene product. Disruption and induction of the gene. J. Biol. Chem. 275, 35876–35885. Gustafsson, C., Govindarajan, S., and Minshull, J. 2004. Codon bias and heterologous protein expression. Trends Biotechnol. 22, 346–353. Hanson, G. and Coller, J. 2018. Codon optimality, bias and usage in translation and mRNA decay. Nat. Rev. Mol. Cell Biol. 19, 20–30. Ji, X.J., Huang, H., Du, J., Zhu, J.G., Ren, L.J., Hu, N., and Li, S. 2009a. Enhanced 2,3-butanediol production by Klebsiella oxytoca using a two-stage agitation speed control strategy. Bioresour. Technol. 100, 3410–3414. Ji, X.J., Huang, H., Du, J., Zhu, J.G., Ren, L.J., Li, S., and Nie, Z.K. 2009b. Development of an industrial medium for economical 2,3-butanediol production through co-fermentation of glucose and xylose by Klebsiella oxytoca. Bioresour. Technol. 100, 5214–5218. Kandasamy, V., Liu, J., Dantoft, S.H., Solem, C., and Jensen, P.R. 2016. Synthesis of (3R)-acetoin and 2,3-butanediol isomers by metabolically engineered Lactococcus lactis. Sci. Rep. 6, 36769. Kane, J.F. 1995. Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6, 494–500. Kim, Y.H., Choi, Y., Oh, Y.Y., Ha, N.C., and Song, J. 2019. Plant growth-promoting activity of beta-propeller protein YxaL secreted from Bacillus velezensis strain GH1-13. PLoS ONE 14, e0207968. Kim, Y.H., Song, W., Kim, J.S., Jiao, L., Lee, K., and Ha, N.C. 2015. Structural and mechanistic insights into the Pseudomonas fluorescens 2-nitrobenzoate 2-nitroreductase NbaA. Appl. Environ. Microbiol. 81, 5266–5277. Kim, S.Y., Song, H., Sang, M.K., Weon, H.Y., and Song, J. 2017. The complete genome sequence of Bacillus velezensis strain GH1-13 reveals agriculturally beneficial properties and a unique plasmid. J. Biotechnol. 259, 221–227. Kim, Y.H. and Yu, M.H. 2012. Overexpression of reactive cysteine-containing 2-nitrobenzoate nitroreductase (NbaA) and its mutants alters the sensitivity of Escherichia coli to reactive oxygen species by reprogramming a regulatory network of disulfide-bonded proteins. J. Proteome Res. 11, 3219–3230. Kolodkin-Gal, I., Elsholz, A.K.W., Muth, C., Girguis, P.R., Kolter, R., and Losick, R. 2013. Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane embedded histidine kinase. Genes Dev. 27, 887–899. Li, W., Bottrill, A.R., Bibb, M.J., Buttner, M.J., Paget, M.S.B., and Kleanthous, C. 2003. The role of zinc in the disulphide stressregulated anti-sigma factor RsrA from Streptomyces coelicolor. J. Mol. Biol. 333, 461–472. Nicholson, W.L. 2008. The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-butanediol dehydrogenase. Appl. Environ. Microbiol. 74, 6832–6838. Okegbe, C., Price-Whelan, A., and Dietrich, L.E.P. 2014. Redox-driven regulation of microbial community morphogenesis. Curr. Opin. Microbiol. 18, 39–45. Ortiz de Orué Lucana, D., Wedderhoff, I., and Groves, M.R. 2011. ROS-mediated signalling in bacteria: zinc-containing Cys-X-X-Cys redox centres and iron-based oxidative stress. J. Signal Transduct. 2012, 605905. Pace, N.J. and Weerapana, E. 2014. Zinc-binding cysteines: diverse functions and structural motifs. Biomolecules 4, 419–434. Peng, G., Zhao, X., Li, Y., Wang, R., Huang, Y., and Qi, G. 2019. Engineering Bacillus velezensis with high production of acetoin primes strong induced systemic resistance in Arabidopsis thaliana. Microbiol. Res. 227, 126297. Poole, L.B. 2015. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 80, 148–157. Qiu, Y., Zhang, J., Li, L., Wen, Z., Nomura, C.T., Wu, S., and Chen, S. 2016. Engineering Bacillus licheniformis for the production of meso-2,3-butanediol. Biotechnol. Biofuels 9, 117. Rabbee, M.F., Ali, M.S., Choi, J., Hwang, B.S., Jeong, S.C., and Baek, K.H. 2019. Bacillus velezensis: a valuable member of bioactive molecules within plant microbiomes. Molecules 24, 1046. Raedts, J., Siemerink, M.A., Levisson, M., van der Oost, J., and Kengen, S.W. 2014. Molecular characterization of an NADPH-dependent acetoin reductase/2,3-butanediol dehydrogenase from Clostridium beijerinckii NCIMB 8052. Appl. Environ. Microbiol. 80, 2011–2020. Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Kloepper, J.W., and Paré, P.W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134, 1017–1026. Sabra, W., Quitmann, H., Zeng, A.P., Dai, J.Y., and Xiu, Z.L. 2011. Microbial production of 2,3-butanediol. In Moo-Young, M. (ed.), Comprehensive Biotechnology, 2nd edn., pp. 87–97. Academic Press, Amsterdam, The Netherlands. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56, 845–857. Song, C.W., Park, J.M., Chung, S.C., Lee, S.Y., and Song, H. 2019. Microbial production of 2,3-butanediol for industrial applications. J. Ind. Microbiol. Biotechnol. 46, 1583–1601. Takeda, M., Muranushi, T., Inagaki, S., Nakao, T., Motomatsu, S., Suzuki, I., and Koizumi, J. 2011. Identification and characterization of a mycobacterial (2R,3R)-2,3-butanediol dehydrogenase. Biosci. Biotechnol. Biochem. 75, 2384–2389. Ui, S., Hosaka, T., Watanabe, K., and Mimura, A. 1998. Discovery of a new mechanism of 2,3-butanediol stereoisomer formation in Bacillus cereus YUF-4. J. Ferment. Bioeng. 85, 79–83. Ui, S., Odagiri, M., Mimura, A., Kanai, H., Kobayashi, T., and Kudo, T. 1996. Preparation of a chiral acetoinic compound using transgenic Escherichia coli expressing the 2,3-butanediol dehydrogenase gene. J. Ferment. Bioeng. 81, 386–389. Ulrich, K. and Jakob, U. 2019. The role of thiols in antioxidant systems. Free Radic. Biol. Med. 140, 14–27. Wang, X.F., Feng, Y.B., and Ji, F.L. 2018. X-ray crystal structure of 2R,3R-butanediol dehydrogenase from Bacillus subtilis. doi: https://doi.org/10.2210/pdb6ie0/pdb. (released Sep 18, 2019) Yang, T., Rao, Z., Zhang, X., Xu, M., Xu, Z., and Yang, S.T. 2013. Improved production of 2,3-butanediol in Bacillus amyloliquefaciens by over-expression of glyceraldehyde-3-phosphate dehydrogenase and 2,3-butanediol dehydrogenase. PLoS ONE 8, e76149. Yang, T., Rao, Z., Zhang, X., Xu, M., Xu, Z., and Yang, S.T. 2015. Enhanced 2,3-butanediol production from biodiesel-derived glycerol by engineering of cofactor regeneration and manipulating carbon flux in Bacillus amyloliquefaciens. Microb. Cell Fact. 14, 122. Yang, Z. and Zhang, Z. 2018. Production of (2R, 3R)-2,3-butanediol using engineered Pichia pastoris: strain construction, characterization and fermentation. Biotechnol. Biofuels 11, 35. Ying, X. and Ma, K. 2011. Characterization of a zinc-containing alcohol dehydrogenase with stereoselectivity from the hyperthermophilic archaeon Thermococcus guaymasensis. J. Bacteriol. 193, 3009–3019. Yu, M., Huang, M., Song, Q., Shao, J., and Ying, X. 2015. Characterization of a (2R,3R)-2,3-butanediol dehydrogenase from Rhodococcus erythropolis WZ010. Molecules 20, 7156–7173. Yu, B., Sun, J., Bommareddy, R.R., Song, L., and Zeng, A.P. 2011. Novel (2R,3R)-2,3-butanediol dehydrogenase from potential industrial strain Paenibacillus polymyxa ATCC 12321. Appl. Environ. Microbiol. 77, 4230–4233. Zhang, X., Bao, T., Rao, Z., Yang, T., Xu, Z., Yang, S., and Li, H. 2014. Two-stage pH control strategy based on the pH preference of acetoin reductase regulates acetoin and 2,3-butanediol distribution in Bacillus subtilis. PLoS ONE 9, e91187. Zhao, X., Zhang, X., Rao, Z., Bao, T., Li, X., Xu, M., Yang, T., and Yang, S. 2015. Identification and characterization of a novel 2,3-butanediol dehydrogenase/acetoin reductase from Corynebacterium crenatum SYPA5-5. Lett. Appl. Microbiol. 61, 573–579.