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Understanding high ε-poly-l-lysine production by Streptomyces albulus using pH shock strategy in the level of transcriptomics

  • Genetics and Molecular Biology of Industrial Organisms - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

ε-Poly-l-lysine (ε-PL) is a natural food preservative, which exhibits antimicrobial activity against a wide spectra of microorganisms. The production of ε-PL was significantly enhanced by pH shock in our previous study, but the underlying mechanism is poorly understood. According to transcriptional and physiological analyses in this study, the mprA/B and pepD signal transduction system was first proved to be presented and activated in Streptomyces albulus M-Z18 by pH shock, which positively regulated the transcription of ε-PL synthetase (Pls) gene and enhanced the Pls activity during fermentation. Furthermore, pH shock changed the ratio of unsaturation to saturation fatty acid in the membrane through up-regulating the transcription of fatty acid desaturase genes (SAZ_RS14940, SAZ_RS14945). In addition, pH shock also enhanced the transcription of cytochrome c oxidase (SAZ_RS15070, SAZ_RS15075), ferredoxin reductase (SAZ_RS34975) and iron sulfur protein (SAZ_RS31410) genes, and finally resulted in the improvement of cell respiratory activity. As a result, pH shock was considered to influence a wide range of proteins including regulators, fatty acid desaturase, respiratory chain component, and ATP-binding cassette transporter during fermentation. These combined influences might contribute to enhanced ε-PL productivity with pH shock.

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References

  1. Bankar SB, Singhal RS (2013) Panorama of poly-ε-lysine. Rsc Adv 3:8586–8603

    Article  CAS  Google Scholar 

  2. Beney L, Gervais P (2001) Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl Microbiol Biotechnol 57:34–42

    Article  CAS  Google Scholar 

  3. Borst P, Zelcer N, Helvoort AV (2000) ABC transporters in lipid transport. Biochim Biophys Acta 1486:128–144

    Article  CAS  Google Scholar 

  4. Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445–2458

    Article  CAS  Google Scholar 

  5. Chen X-S, Li S, Liao L-J, Ren X-D, Li F, Tang L, Zhang J-H, Mao Z-G (2011) Production of ε-poly-l-lysine using a novel two-stage pH control strategy by Streptomyces sp. M-Z18 from glycerol. Bioprocess Biosyst Eng 34:561–567

    Article  CAS  Google Scholar 

  6. Chen X-S, Mao Z-G (2013) Comparison of glucose and glycerol as carbon sources for ε-poly-l-lysine production by Streptomyces sp. M-Z18. Appl Biochem Biotechnol 170:185–197

    Article  CAS  Google Scholar 

  7. Chen X-S, Ren X-D, Zeng X, Zhao F-L, Tang L, Zhang H-J, Zhang J-H, Mao Z-G (2013) Enhancement of ε-poly-l-lysine production coupled with precursor l-lysine feeding in glucose–glycerol co-fermentation by Streptomyces sp. M-Z18. Bioprocess Biosyst Eng 36:1843–1849

    Article  CAS  Google Scholar 

  8. Chen X, Tang L, Li S, Liao L, Zhang J, Mao Z (2011) Optimization of medium for enhancement of ε-poly-l-lysine production by Streptomyces sp. M-Z18 with glycerol as carbon source. Bioresour Technol 102:1727–1732

    Article  CAS  Google Scholar 

  9. Foster JW (1991) Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol 173:6896–6902

    Article  CAS  Google Scholar 

  10. Hayes A, Hobbs G, Smith CP, Oliver SG, Butler PR (1997) Environmental signals triggering methylenomycin production by Streptomyces coelicolor A3(2). J Bacteriol 179:5511–5515

    Article  CAS  Google Scholar 

  11. He H, Hovey R, Kane J, Singh V, Zahrt TC (2006) MprAB is a stress-responsive two-component system that directly regulates expression of sigma factors SigB and SigE in Mycobacterium tuberculosis. J Bacteriol 188:2134

    Article  CAS  Google Scholar 

  12. Hiraki J, Ichikawa T, Ninomiya S, Seki H, Uohama K, Seki H, Kimura S, Yanagimoto Y, Barnett JW Jr (2003) Use of ADME studies to confirm the safety of epsilon-polylysine as a preservative in food. Regul Toxicol Pharm 37:328–340

    Article  CAS  Google Scholar 

  13. Huang R, Pan M, Wan C, Shah NP, Tao X, Wei H (2016) Physiological and transcriptional responses and cross protection of Lactobacillus plantarum ZDY2013 under acid stress. J Dairy Sci 99:1002–1010

    Article  CAS  Google Scholar 

  14. Jiang J, Sun YF, Tang X, He CN, Shao YL, Tang YJ, Zhou WW (2017) Alkaline pH shock enhanced production of validamycin A in fermentation of Streptomyces hygroscopicus. Bioresour Technol 249:234

    Article  Google Scholar 

  15. Kahar P, Iwata T, Hiraki J, Park EY, Okabe M (2001) Enhancement of ε-polylysine production by Streptomyces albulus strain 410 using pH control. J Biosci Bioeng 91:190–194

    Article  CAS  Google Scholar 

  16. Kim YJ, Moon AN, Song JY, Kim ES, Kim CJ, Chang YK (2009) Gene-expression analysis of acidic pH shock effects on two-component systems in Streptomyces coelicolor. Biotechnol Bioprocess Eng 14:584

    Article  CAS  Google Scholar 

  17. Kolbeck S, Behr J, Vogel RF, Ludwig C, Ehrmann MA (2019) Acid stress response of Staphylococcus xylosus elicits changes in the proteome and cellular membrane. J Appl Microbiol 126:1480–1495

    Article  CAS  Google Scholar 

  18. Köster W (2001) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 152:291–301

    Article  Google Scholar 

  19. Overbergh L, Giulietti A, Valckx D, Decallonne B, Bouillon R, Mathieu C (2003) The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression. J Biomol Tech 14:33–43

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Lara AR, Leal L, Flores N, Gosset G, Bolívar F, Ramírez OT (2010) Transcriptional and metabolic response of recombinant Escherichia coli to spatial dissolved oxygen tension gradients simulated in a scale-down system. Biotechnol Bioeng 93:372–385

    Article  Google Scholar 

  21. Li S, Li F, Chen X-S, Wang L, Xu J, Tang L, Mao Z-G (2012) Genome shuffling enhanced ε-poly-l-lysine production by improving glucose tolerance of Streptomyces graminearus. Appl Biochem Biotechnol 166:414–423

    Article  CAS  Google Scholar 

  22. Liu S, Wu Q, Zhang J, Mo S (2011) Production of ε-poly-l-lysine by Streptomyces sp. using resin-based, in situ product removal. Biotechnol Lett 33:1581–1585

    Article  CAS  Google Scholar 

  23. Michener JK, Jens N, Smolke CD (2012) Identification and treatment of heme depletion attributed to overexpression of a lineage of evolved P450 monooxygenases. Proc Natl Acad Sci USA 109:19504–19509

    Article  CAS  Google Scholar 

  24. Mishra NK, Chang J, Zhao PX (2014) Prediction of membrane transport proteins and their substrate specificities using primary sequence information. PLoS One 9:e100278

    Article  Google Scholar 

  25. Pan L, Chen X-S, Liu M-M, Liu Y-J, Mao Z-G (2017) Efficient production of ε-poly-l-lysine from glucose by two-stage fermentation using pH shock strategy. Process Biochem 63:8–15

    Article  CAS  Google Scholar 

  26. Pang X, Vu P, Byrd TF, Ghanny S, Soteropoulos P, Mukamolova GV, Wu S, Samten B, Howard ST (2007) Evidence for complex interactions of stress-associated regulons in an mprAB deletion mutant of Mycobacterium tuberculosis. Microbiol 153:1229–1242

    Article  CAS  Google Scholar 

  27. Ren X-D, Chen X-S, Tang L, Zeng X, Wang L, Mao Z-G (2015) Physiological mechanism of the overproduction of ε-poly-l-lysine by acidic pH shock in fed-batch fermentation. Bioprocess Biosyst Eng 38:2085–2094

    Article  CAS  Google Scholar 

  28. Ren X-D, Chen X-S, Zeng X, Wang L, Tang L, Mao Z-G (2015) Acidic pH shock induced overproduction of ε-poly-l-lysine in fed-batch fermentation by Streptomyces sp. M-Z18 from agro-industrial by-products. Bioprocess Biosyst Eng 38:1113–1125

    Article  CAS  Google Scholar 

  29. Riccardo M, Roberta P, Sebastien R, Jocelyn B, Luc G, Issar S, Roberta P (2004) Sigma factors and global gene regulation in Mycobacterium tuberculosis. J Bacteriol 186:895–902

    Article  Google Scholar 

  30. Shih IL, Shen MH, Van YT (2006) Microbial synthesis of poly(epsilon-lysine) and its various applications. Bioresour Technol 97:1148–1159

    Article  CAS  Google Scholar 

  31. Wang D, Yang C, Long D, Zhu J, Wang J, Zhang S (2015) Comparative transcriptome analyses of drought-resistant and—susceptible Brassica napus L. and development of EST-SSR markers by RNA-Seq. J Plant Biol 58:259–269

    Article  CAS  Google Scholar 

  32. Wei ZH, Bai L, Deng Z, Zhong JJ (2012) Impact of nitrogen concentration on validamycin A production and related gene transcription in fermentation of Streptomyces hygroscopicus 5008. Bioprocess Biosyst Eng 35:1201–1208

    Article  CAS  Google Scholar 

  33. White MJ, He H, Penoske RM, Twining SS, Zahrt TC (2010) PepD participates in the Mycobacterial stress response mediated through MprAB and SigE. J Bacteriol 192:1498

    Article  CAS  Google Scholar 

  34. Xu D, Yao H, Xu Z, Wang R, Xu Z, Li S, Feng X, Liu Y, Xu H (2017) Production of ε-poly-lysine by Streptomyces albulus PD-1 via solid-state fermentation. Bioresour Technol 223:149–156

    Article  CAS  Google Scholar 

  35. Xu Z, Feng X, Sun Z, Cao C, Li S, Xu Z, Xu Z, Bo F, Xu H (2015) Economic process to co-produce poly (ε-l-lysine) and poly (l-diaminopropionic acid) by a pH and dissolved oxygen control strategy. Bioresour Technol 187:70–76

    Article  CAS  Google Scholar 

  36. Yamanaka K, Kito N, Imokawa Y, Maruyama C, Utagawa T, Hamano Y (2010) Mechanism of ε-poly-l-lysine production and accumulation revealed by identification and analysis of an ε-poly-l-lysine-degrading enzyme. Appl Environ Microbiol 76:5669–5675

    Article  CAS  Google Scholar 

  37. Yoshida T, Nagasawa T (2003) ε-Poly-l-lysine: microbial production, biodegradation and application potential. Appl Microbiol Biotechnol 62:21–26

    Article  CAS  Google Scholar 

  38. Zhang Y, Feng X, Xu H, Yao Z, Ouyang P (2010) ε-Poly-l-lysine production by immobilized cells of Kitasatospora sp. MY 5-36 in repeated fed-batch cultures. Bioresour Technol 101:5523–5527

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Program of the National Natural Science Foundation of China (31671846, 31301556), and the National First-Class Discipline Program of Light Industry Technology and Engineering (LITE2018-27), the Cooperation Project of Jiangsu Province among Industries, Universities and Institutes (BY2016022-25).

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  1. The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, 1800 Lihu Road, Wuxi, 214122, China

    Long Pan, Xusheng Chen, Kaifang Wang & Zhonggui Mao

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  1. Long Pan
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  2. Xusheng Chen
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Correspondence to Xusheng Chen or Zhonggui Mao.

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Pan, L., Chen, X., Wang, K. et al. Understanding high ε-poly-l-lysine production by Streptomyces albulus using pH shock strategy in the level of transcriptomics. J Ind Microbiol Biotechnol 46, 1781–1792 (2019). https://doi.org/10.1007/s10295-019-02240-z

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