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http://dx.doi.org/10.4014/jmb.1207.07030

Heterologous Expression of a Putative $K^+/H^+$ Antiporter of S. coelicolor A3(2) Enhances $K^+$, Acidic-pH Shock Tolerances, and Geldanamycin Secretion  

Song, Jae Yang (Bio Lab, Energy R&D Center, SK Innovation Global Technology)
Seo, Young Bin (Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology)
Hong, Soon-Kwang (Division of Bioscience and Bioinformatics, Myung-Ji University)
Chang, Yong Keun (Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology)
Publication Information
Journal of Microbiology and Biotechnology / v.23, no.2, 2013 , pp. 149-155 More about this Journal
Abstract
Heterologous expression of a putative $K^+/H^+$ antiporter of Streptomyces coelicolor A3(2) (designated as sha4) in E. coli and Streptomyces hygroscopicus JCM4427 showed enhanced tolerance to $K^+$ stress, acidic-pH shock, and/or geldanamycin production under $K^+$ stress. In a series of $K^+$ extrusion experiments with sha4-carrying E. coli deficient in the $K^+/H^+$ antiporter, a restoration of impaired $K^+$ extrusion activity was observed. Based on this, it was concluded that sha4 was a true $K^+/H^+$ antiporter. In different sets of experiments, the sha4-carrying E. coli showed significantly improved tolerances to $K^+$ stresses and acidic-pH shock, whereas sha4-carrying S. hygroscopicus showed an improvement in $K^+$ stress tolerance only. The sha4-carrying S. hygroscopicus showed much higher geldanamycin productivity than the control under $K^+$ stress condition. In another set of experiments with a production medium, the secretion of geldanamycin was also significantly enhanced by the expression of sha4.
Keywords
$K^+/H^+$ antiporter; salt tolerance; pH shock tolerance; geldanamycin;
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1 Apse, M. P., G. S. Aharon, W. A. Snedden, and E. Blumward. 1999. Salt tolerance conferred by overexpression of a vacuolar $Na^{+}/H^{+}$ antiporter in Arabidopsis. Science 285: 1256-1258.   DOI   ScienceOn
2 Breed, R. and W. D. Dotterrer. 1916. The number of colonies allowable on satisfactory agar plates. J. Bacteriol. 1: 321-331.
3 Bakker, E. P., I. R. Booth, U. Dinnbier, W. Epstein, and A. Gajewsak. 1987. Evidence for multiple $K^{+}$ export system in Escherichia coli. J. Bacteriol. 169: 3743-3749.   DOI
4 Bently, S. D., K. F. Chater, A.-M. Cerdeno-Tarraga, G. L. Chaliis, N. R. Thomson, K. D. James, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.   DOI   ScienceOn
5 Song, J. Y., Y. J. Kim, Y.-S. Hong, and Y. K. Chang. 2008. Enhancement of geldanamycin production by pH shock in batch culture of Streptomyces hygroscopicus subsp. duamyceticus. J. Microbiol. Biotechnol. 18: 897-900.
6 Renzo, G. D., S. Amoroso, A. Bassi, A. Fatatis, M. Cataldi, A. M. Colao, et al. 1995. Role of the $Na^{+}-Ca^{2+}$ and $Na^{+}/H^{+}$ antiporters in prolactin release from anterior pituitary cells in primary culture. Euro. J. Phamacol. 294: 11-15.   DOI   ScienceOn
7 Schuldiner, S. and E. Padan. 1992. $Na^{+}$ transport systems in prokaryotes, pp. 25-51. In E. P. Bakker (ed.). Alkali Cation Transport System in Prokaryotes. CRC Press, Boca Raton, FL.
8 Shijuku, T., T. Yamashino, H. Ohashi, H. Saito, T. Kakegawa, M. Ohta, and H. Kobayashi. 2002. Expression of chaA, a sodium ion extrusion system of Escherichia coli, is regulated by osmolarity and pH. Biochim. Biophys. Acta 1556: 142-148.   DOI   ScienceOn
9 Verkhovskaya, M. L., B. Barquera, M. I. Verhovsky, and M. Wikström. 1998. The $Na^{+}$ and $K^{+}$ transport deficiency of an E. coli mutant lacking the NhaA and NhaB proteins is apparent and caused by impaired osmoregulation. FEBS Lett. 439: 271-274   DOI   ScienceOn
10 Waditee, R., T. Hibino, T. Nakamura, A. Incharoensakdi, and T. Takabe. 2002. Overexpression of a $Na^{+}/H^{+}$ antiporter confers salt tolerance on a freshwater cyanobacterium, making it capable of growth in sea water. Proc. Natl. Acad. Sci. USA 99: 4109-4114.   DOI   ScienceOn
11 Wu, L., Z. Fan, L. Guo, Y. Li, Z.-L. Chen, and L. J. Qu. 2005. Over-expression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Sci. 168: 297-302.   DOI   ScienceOn
12 Yoshinaka, T., H. Takasu, R. Tomizawa, S. Kosono, and T. Kudo. 2003. A shaE deletion mutant showed lower Na+ sensitivity compared to other deletion mutants in the Bacillus subtilis sodium/hydrogen antiporter (Sha) system. J. Biosci. Bioeng. 95: 306-309.   DOI
13 Cagnac, O., M. Leterrir, M. Yeager, and E. Bumwald. 2007. Identification and characterization of Vnx1p, a novel type of vacuolar monovalent cation/$H^{+}$ antiporter of Saccharomyces cerevisiae. J. Biol. Chem. 282: 24284-24293.   DOI   ScienceOn
14 Bierman, M., R. Logan, K. O'Brien, E. T. Seno, R. N. Rao, and B. E. Schoner. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.   DOI   ScienceOn
15 Brini, F., M. Hanin, I. Mezghani, G. A. Bekowitz, and K. Masmoudi. 2007. Overexpression of wheat $Na^{+}/H^{+}$ antiporter TNHX1 and $H^{+}$-pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. J. Exper. Bot. 58: 301-308.
16 Bystrykh, L. V., M. A. Fernandez-Moreno, J. K. Herrema, F. Malpartida, D. A. Hopwood, and L. Dijkhuizen. 1996. Production of actinorhodin-related "blue pigments" by Streptomyces coelicolor A3(2). J. Bacteriol. 178: 2238-2244.   DOI
17 Cheng, J., A. A. Guffanti, and T. A. Krulwich. 1994. The chromosomal tetracycline resistance locus of Bacillus subtilis encodes a $Na^{+}/H^{+}$ antiporter that is physiologically important at elevated pH. J. Biol. Chem. 269: 27365-27371.
18 Gaxiola, R. A., R. Rao, A. Sherman, P. Grisafi, S. L. Alper, and G. R. Fink. 1999. The Arabidopsis thaliana proton transporter, AtNhx and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA 96: 1480-1485.   DOI   ScienceOn
19 Clyne, M., A. Labigne, and B. Drumm. 1995. Helicobacter pylori requires an acidic environment to survive in the presence of urea. Infect. Immun. 63: 1669-1673.
20 Doull, J. C., S. Y. Ayer, A. K. Singh, and P. Thibault. 1993. Production of a novel polyketide antibiotic, jadomycin B, by Streptomyces venezuelae following heat shock. J. Antibiot. 44: 869-871.
21 Flett, F. V., V. Mersenias, and C. P. Smith. 1998. High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol. Lett. 155: 223-229.
22 Kim, Y. J. 2007. Gene-expression analyses of acidic pH shock effects on actinorhodin production in Streptomyces coelicolor A3(2). Ph.D. Thesis, KAIST, Daejeon, Korea.
23 Zhao, J., N.-H. Cheng, C. M. Motes, E. B. Blancaflor, M. Moor, N. Gonzales, et al. 2003. AtCHX13 is a plasma membrane $K^{+}$ transporter. Plant Physiol. 148: 796-807.
24 Goldberg, B. G., T. Arbel, J. Chen, R. Karpel, G. A. Mackie, S. Schuldiner, and E. Padan. 1987. Characterization of a $Na^{+}/H^{+}$ antiporter gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 84: 2615-2619.   DOI   ScienceOn
25 Guffanti, A. A., D. E. Cohen, H. R. Kaback, and T. A. Krulwich. 1981. Relationship between the $Na^{+}/H^{+}$ antiporter and $Na^{+}$/substrate symport in Bacillus alcalophilus. Proc. Natl. Acad. Sci. USA 78: 1481-1484.   DOI   ScienceOn
26 Hallam, T. J. and A. H. Tashjian. 1987. Thyrotropin-releasing hormone activates $Na^{+}/H^{+}$ exchange in rat pituitary cells. J. Biochem. 242: 411-416.   DOI
27 Hayes, A., G. Hobbs, C. P. Smith, S. G. Oliver, and P. R. Butler. 1997. Environmental signals triggering methylenomycin production by Streptomyces coelicolor A(3)2. J. Bacteriol. 179: 5511-5515.   DOI
28 Katiyar-Agarwal, S., J. Zhu, K. Kim, M. Agarwal, X. Fu, A. Huang, and J.-K. Zhu. 2006. The plasma membrane $Na^{+}/H^{+}$ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 103: 18816-18821.   DOI   ScienceOn
29 Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces Genetics, pp. 161-206. The John Innes Foundation, Norwich, UK.
30 Killham, K. and M. K. Firesone. 1984. Salt stress control of intracellular solutes in Streptomyces indigenous to saline soils. Appl. Environ. Microbiol. 47: 301-306.
31 Kim, C. J., Y. K. Chang, and G.-T. Chun. 2000. Enhancement of kasugamycin production by pH shock in batch cultures of Streptomyces kasugaensis. Biotechnol. Prog. 16: 548-552.   DOI   ScienceOn
32 Kim, Y. J., M. H. Moon, J. S. Lee, S. K. Hong, and Y. K. Chang. 2011. Roles of putative sodium-hydrogen antiporter (SHA) genes in S. coelicolor A3(2) culture with pH variation. J. Microbiol. Biotechnol. 21: 979-987.   DOI   ScienceOn
33 Krishnamurth, P., M. Parlow, J. B. Zitzer, N. B. Vakil, H. L. Mobley, M. Levy, et al. 1998. Helicobacter pylori containing only cytoplasmic urease is susceptible to acid. Infect. Immun. 66: 5060-5066.
34 Kim, Y. J., J. Y. Song, M. H. Moon, C. P. Smith, S. K. Hong, and Y. K. Chang. 2007. pH shock induces overexpression of regulatory and biosynthetic genes for actinorhodin production in Streptomyces coelicolor A3(2). Appl. Microbiol. Biotechnol. 76: 1119-1130.   DOI   ScienceOn
35 Kosono, S., Y. Ohashi, F. Kawamura, M. Kitada, and T. Kudo. 2000. Function of a principal $Na^{+}/H^{+}$ antiporter, ShaA, is required for initiation of sporulation in Bacillus subtilis. J. Bacteriol. 182: 898-904.   DOI   ScienceOn
36 Padan, E. and S. Schuldiner. 1993. $Na^{+}/H^{+}$ antiporters, molecular devices that couple the $Na^{+}$ and$H^{+}$ circulation in cells. J. Bioenerg. Biomembr. 25: 647-669.
37 Liew, C. W., R. M. Illias, N. M. Mahadi, and N. Najimudin. 2007. Expression of the $Na^{+}/H^{+}$ antiporter gene (g1-nhaC) of alkaliphilic Bacillus sp. G1 in Escherichia coli. FEMS Microbiol. Lett. 276: 114-122.   DOI   ScienceOn
38 Ohyama, T., R. Imaizumi, K. Igarashi, and H. Kobayashi. 1992. Escherichia coli is able to grow with negligible sodium ion extrusion activity at alkaline pH. J. Bacteriol. 174: 7743-7749.   DOI
39 Pinner, E., Y. Kolter, E. Padan, and S. Schuldiner. 1993. Physiological role of nhaB, a specific $Na^{+}/H^{+}$ antiporter in Escherichia coli. J. Biol. Chem. 268: 1729-1734.
40 Padan, E. and S. Schuldiner. 1994. Molecular physiology of $Na^{+}/H^{+}$ antiporters, key transporters in circulation of $Na^{+}$ and $H^{+}$ in cells. Biochim. Biophys. Acta 1185: 129-151.   DOI   ScienceOn
41 Padan, E., M. Venture, Y. Gerchman, and N. Dover. 2001. $Na^{+}/H^{+}$ antiporters. Biochim. Biophys. Acta 1505: 144-157.   DOI   ScienceOn
42 Rausch, T., M. Kirsch, R. Low, A. Lehr, R. Viereck, and A. Zhigang. 1996. Salt stress responses of higher plants: The role of proton pump and $Na^{+}/H^{+}$ antiporters J. Plant Physiol. 148: 425-433.   DOI   ScienceOn