Breeding of High Daptomycin-Producing Strain by Streptomycin Resistance Superposition

Chu, Shuaibei; Hu, Wenting; Zhang, Kaihong; Hui, Fengli

doi:10.33073/pjm-2022-041

Abstract

Daptomycin is a cyclolipopeptide antibiotic produced by Streptomyces roseosporus. It is widely used to treat drug-resistant bacterial infections; however, daptomycin yield in wild strains is very low. To improve the daptomycin production by the strain BNCC 342432, a modified method of ribosome engineering with superposition of streptomycin resistance was adopted in this study. The highest-yield mutant strain SR-2620 was obtained by increasing streptomycin resistance of BNCC 342432, and achieved daptomycin production of 38.5 mg/l in shake-flask fermentation, 1.79-fold higher than the parent strain and its heredity stability was stable. The morphological characteristics of the two strains were significantly different, and the 440^th base G of the rpsL gene in the mutant strain was deleted, which resulted in a frameshift mutation. Our results demonstrate that gradually increasing strain resistance to streptomycin was an effective breeding method to improve daptomycin yield in S. roseosporus.

References

Andersson DA, Levin BR. The biological cost of antibiotic resistance. Curr Opin Microbiol. 1999 Oct;2(5):489–493. https://doi.org/10.1016/S1369-5274(99)00005-3
Search in Google Scholar Back to article
Cai C, Wang Y, Zheng Y. [Ribosome engineering and microorganism secondary metabolite production] (in Chinese). Biotechnol Bull. 2012;09:51–58. https://doi.org/10.13560/j.cnki.biotech.bull.1985.2012.09.029
Search in Google Scholar Back to article
Gao FX, Yu YQ, Wang KR, Xie Y, Zhang HL, Ran QP, Tian M. [Breeding of high daptomycin-producing strain by ARTP and UV mutagenesis] (in Chinese). Chin J Antibiot. 2016;41(06):425–428. https://doi.org/10.13461/j.cnki.cja.005748
Search in Google Scholar Back to article
Jung D, Rozek A, Okon M, Hancock REW. Structural transitions as determinants of the action of the calcium-dependent antibiotic daptomycin. Chem Biol. 2004 Jul;11(7):949–957. https://doi.org/10.1016/j.chembiol.2004.04.020
Search in Google Scholar Back to article
Liao G, Shi T, Xie J. Regulation mechanisms underlying the biosynthesis of daptomycin and related lipopeptides. J Cell Biochem. 2012 Mar; 113(3):735–741. https://doi.org/10.1002/jcb.23414
Search in Google Scholar Back to article
Liu HH, Chen YH, Chen M. [Breeding of high avilamycin-producing strains by ribosome engineering] (in Chinese). J Agr Biotechnol. 2019a;27(07):1322–1330.
Search in Google Scholar Back to article
Liu J, Zhang Y, He W. [Construction of a novel carrimycin-producing strain by using CRISPR-Cas9 and ribosome engineering techniques] (in Chinese). Chin J Biotech. 2021a;37(06):2116–2126. https://doi.org/10.13345/j.cjb.200763
Search in Google Scholar Back to article
Liu WT, Chen EZ, Yang L, Peng C, Wang Q, Xu Z, Chen DQ. Emerging resistance mechanisms for 4 types of common anti-MRSA antibiotics in Staphylococcus aureus: A comprehensive review. Microb Pathog. 2021b Jul; 156:104915. https://doi.org/10.1016/j.micpath.2021.104915
Search in Google Scholar Back to article
Liu X, Zhou S, Sun K. [Study on response surface methodology for doxymycin fermentation] (in Chinese). J South-Cent Univ Natl (Nat Sci Edit). 2019b;38(01):76–80.
Search in Google Scholar Back to article
Lopatniuk M, Myronovskyi M, Nottebrock A, Busche T, Kalinowski J, Ostash B, Fedorenko V, Luzhetskyy A. Effect of “ribosome engineering” on the transcription level and production of S. albus indigenous secondary metabolites. Appl Microbiol Biotechnol. 2019 Sep;103(17):7097–7110. https://doi.org/10.1007/s00253-019-10005-y
Search in Google Scholar Back to article
Lu F, Hou Y, Li X, He L, Chu Y, Xia H, Tian Y. [Breeding of high milbemycin-producing strain by ribosomal engineering] (in Chinese). Chin J Antibiot. 2018;43(07):811–816. https://doi.org/10.13461/j.cnki.cja.006299
Search in Google Scholar Back to article
Matsuo T, Mori N, Sakurai A, Kanie T, Mikami Y, Uehara Y, Furukawa K. Effectiveness of daptomycin against infective endocarditis caused by highly penicillin-resistant viridans group streptococci. IDCases. 2021 Apr 5;24:e01113. https://doi.org/10.1016/j.idcr.2021.e01113
Search in Google Scholar Back to article
Ng IS, Ye C, Zhang Z, Lu Y, Jing K. Daptomycin antibiotic production processes in fed-batch fermentation by Streptomyces roseosporus NRRL11379 with precursor effect and medium optimization. Bioprocess Biosyst Eng. 2014 Mar;37(3):415–423. https://doi.org/10.1007/s00449-013-1007-2
Search in Google Scholar Back to article
Nishimura K, Hosaka T, Tokuyama S, Okamoto S, Ochi K. Mutations in rsmG, encoding a 16S rRNA methyltransferase, result in low-level streptomycin resistance and antibiotic overproduction in Streptomyces coelicolor A3(2). J Bacteriol. 2007 May; 189(10):3876–3883. https://doi.org/10.1128/JB.01776-06
Search in Google Scholar Back to article
Ochi K, Okamoto S, Tozawa Y, Inaoka T, Hosaka T, Xu J, Kurosawa K. Ribosome engineering and secondary metabolite production. Adv Appl Microbiol. 2004;56:155–184. https://doi.org/10.1016/S0065-2164(04)56005-7
Search in Google Scholar Back to article
Ochi K. From microbial differentiation to ribosome engineering. Biosci Biotechnol Biochem. 2007 Jun;71(6):1373–1386. https://doi.org/10.1271/bbb.70007
Search in Google Scholar Back to article
Osorio C, Garzón L, Jaimes D, Silva E, Bustos RH. Impact on antibiotic resistance, therapeutic success, and control of side effects in therapeutic drug monitoring (TDM) of daptomycin: A scoping review. Antibiotics (Basel). 2021 Mar 5;10(3):263. https://doi.org/10.3390/antibiotics10030263
Search in Google Scholar Back to article
Tamehiro N, Hosaka T, Xu J, Hu H, Otake N, Ochi K. Innovative approach for improvement of an antibiotic-overproducing industrial strain of Streptomyces albus. Appl Environ Microbiol. 2003 Nov; 69(11):6412–6417. https://doi.org/10.1128/AEM.69.11.6412-6417.2003
Search in Google Scholar Back to article
Tótoli EG, Garg S, Salgado HR. Daptomycin: physicochemical, analytical, and pharmacological properties. Ther Drug Monit. 2015 Dec;37(6):699–710. https://doi.org/10.1097/FTD.0000000000000222
Search in Google Scholar Back to article
Wang G, Hosaka T, Ochi K. Dramatic activation of antibiotic production in Streptomyces coelicolor by cumulative drug resistance mutations. Appl Environ Microbiol. 2008 May;74(9):2834–2840. https://doi.org/10.1128/AEM.02800-07
Search in Google Scholar Back to article
Wang JP. [Study on screening of daptomycin producing strains and fermentation conditions] [MD Thesis] (in Chinese). Tianjin (China): Tianjin University, Department of Chemical Engineering; 2007. https://doi.org/10.7666/d.y1357552
Search in Google Scholar Back to article
Wang YQ, Yan YZ, Hu B, Liao JX, Tang F, Zhou H, Cao RY. [Breeding of high daptomycin producing strains and optimization of fermentation conditions] (in Chinese). Chin J Antibiot. 2020; 45(12): 1232–1237. https://doi.org/10.13461/j.cnki.cja.007055
Search in Google Scholar Back to article
Wu GY, Chen XS, Wang L, Mao ZG. [Screening of high-yield ε-poly-L-lysine producing strains through ribosome engineering] (in Chinese). Microbiol China. 2016;43(12):2744–2751. https://doi.org/10.13344/j.microbiol.china.160026
Search in Google Scholar Back to article
Xie Y, Yao S, Li W, Dan R, Wu G, Tong T, Chen Q. [Development and application of ribosome engineering in actinomycetes] (in Chinese). Chin J Biotech. 2022;38:546–564. https://doi.org/10.13345/j.cjb.210150
Search in Google Scholar Back to article
Xie ZP, Xu ZN, Zheng JM, Cen PL. [Determination of ammonium nitrogen in fermentation broth through indophenol blue reaction] (in Chinese). J Zhejiang Univ (Eng Sci). 2005;03:123–125. https://doi.org/10.3785/j.issn.1008-973X.2005.03.026
Search in Google Scholar Back to article
Yu G, Hu Y, Hui M, Chen L, Wang L, Liu N, Yin Y, Zhao J. Genome shuffling of Streptomyces roseosporus for improving daptomycin production. Appl Biochem Biotechnol. 2014 Mar;172(5): 2661–2669. https://doi.org/10.1007/s12010-013-0687-z
Search in Google Scholar Back to article
Zhang HY. [Optimization of fermentation medium and strain breeding for titer improvement of daptomycin by Streptomyces coelicolor] [MD Thesis] (in Chinese). Baoding (China): Hebei University, Department of Life Sciences; 2021. https://doi.org/10.27103/d.cnki.ghebu.2021.000755
Search in Google Scholar Back to article
Zhou J, Zhang Y. [Precursor resistance screening on mutation breeding and fed-batch fermentation for daptomycin production] (in Chinese). Chin J Antibiot 2018;43:817–823. https://doi.org/10.13461/j.cnki.cja.006300
Search in Google Scholar Back to article
Zuttion F, Colom A, Matile S, Farago D, Pompeo F, Kokavecz J, Galinier A, Sturgis J, Casuso I. High-speed atomic force microscopy highlights new molecular mechanism of daptomycin action. Nat Commun. 2020 Dec 9;11(1):6312. https://doi.org/10.1038/s41467-020-19710-z
Search in Google Scholar Back to article

Breeding of High Daptomycin-Producing Strain by Streptomycin Resistance Superposition

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