Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

N-Acyl-Homoserine Lactone Quorum Sensing Switch from Acidogenesis to Solventogenesis during the Fermentation Process in Serratia marcescens MG1

  • Jin, Wensong (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Lin, Hui (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Gao, Huifang (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Guo, Zewang (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Li, Jiahuan (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Xu, Quanming (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Sun, Shujing (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Hu, Kaihui (College of Life Sciences, Fujian Agriculture and Forestry University) ;
  • Lee, Jung-Kul (Department of Chemical Engineering, Konkuk University) ;
  • Zhang, Liaoyuan (College of Life Sciences, Fujian Agriculture and Forestry University)
  • Received : 2018.10.18
  • Accepted : 2019.02.20
  • Published : 2019.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

N-acyl-homoserine lactone quorum sensing (AHL-QS) has been shown to regulate many physiological behaviors in Serratia marcescens MG1. In the current study, the effects of AHL-QS on the biosynthesis of acid and neutral products by S. marcescens MG1 and its isogenic ${\Delta}swrI$ with or without supplementing exogenous N-hexanoyl-L-homoserine lactone ($C_6-HSL$) were systematically investigated. The results showed that swrI disruption resulted in rapid pH drops from 7.0 to 4.8, which could be restored to wild type by supplementing $C_6-HSL$. Furthermore, fermentation product analysis indicated that ${\Delta}swrI$ could lead to obvious accumulation for acidogenesis products such as lactic acid and succinic acid, especially excess acetic acid (2.27 g/l) produced at the early stage of fermentation, whereas solventogenesis products by ${\Delta}swrI$ appeared to noticeably decrease by an approximate 30% for acetoin during 32-48 h and by an approximate 20% for 2,3-butanediol during 24-40 h, when compared to those by wild type. Interestingly, the excess acetic acid produced could be removed in an AHL-QS-independent manner. Subsequently, quantitative real-time PCR was used to determine the mRNA expression levels of genes responsible for acidogenesis and solventogenesis and showed consistent results with those of product synthesis. Finally, by close examination of promoter regions of the analyzed genes, four putative luxI box-like motifs were found upstream of genes encoding acetyl-CoA synthase, lactate dehydrogenase, ${\alpha}$-acetolactate decarboxylase, and Lys-like regulator. The information from this study provides a novel insight into the roles played by AHL-QS in switching from acidogenesis to solventogenesis in S. marcescens MG1.

Keywords

References

  1. Papenfort K, Bassler BL. 2016. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14: 576-588. https://doi.org/10.1038/nrmicro.2016.89
  2. Whiteley M, Diggle SP, Greenberg EP. 2017. Progress in and promise of bacterial quorum sensing research. Nature 551: 313-320. https://doi.org/10.1038/nature24624
  3. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR. 2018. Bacterial quorum sensing and microbial community interactions. MBio 9.
  4. Zhou J, Lyu Y, Richlen M, Anderson DM, Cai Z. 2016. Quorum sensing is a language of chemical signals and plays an ecological role in algal-bacterial interactions. CRC Crit. Rev. Plant Sci. 35: 81-105. https://doi.org/10.1080/07352689.2016.1172461
  5. Mangwani N, Kumari S, Das S. 2016. Bacterial biofilms and quorum sensing: fidelity in bioremediation technology. Biotechnol. Genet. Eng. Rev. 32: 43-73. https://doi.org/10.1080/02648725.2016.1196554
  6. Givskov M, Olsen L , Molin S. 1988. Cloning and expression in Escherichia coli of the gene for extracellular phospholipase A1 from Serratia liquefaciens. J. Bacteriol. 170: 5855-5862. https://doi.org/10.1128/jb.170.12.5855-5862.1988
  7. Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S. 2005. Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J. Bacteriol. 187: 3477-3485. https://doi.org/10.1128/JB.187.10.3477-3485.2005
  8. Givskov M, Eberl L, Molin S. 1997. Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens. FEMS Microbiol. Lett. 148: 115-122. https://doi.org/10.1111/j.1574-6968.1997.tb10276.x
  9. Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M. 1998. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 6384-6388. https://doi.org/10.1128/JB.180.23.6384-6388.1998
  10. Zhang L, Singh R, Sivakumar D, Guo Z, Li J, Chen F, et al. 2017. An artificial synthetic pathway for acetoin, 2,3-butanediol, and 2-butanol production from ethanol using cell free multi-enzyme catalysis. Green Chem. 20:230-242. https://doi.org/10.1039/C7GC02898A
  11. Guo Z, Zhao X, He Y, Yang T, Gao H, Li G, et al. 2017. Efficient (3R)-acetoin production from meso-2,3-butanediol using a new whole-cell biocatalyst with co-expression of meso-2,3-butanediol dehydrogenase, NADH oxidase, and Vitreoscilla hemoglobin. J. Microbiol. Biotechnol. 27: 92-100. https://doi.org/10.4014/jmb.1608.08063
  12. Lopez-Contreras AM, Claassen PA, Mooibroek H, De Vos WM. 2000. Utilisation of saccharides in extruded domestic organic waste by Clostridium acetobutylicum ATCC 824 for production of acetone, butanol and ethanol. Appl. Microbiol. Biotechnol. 54: 162-167. https://doi.org/10.1007/s002530000374
  13. Biebl H, Zeng AP, Menzel K, Deckwer WD. 1998. Fermentation of glycerol to 1,3-propanediol and 2,3-butanediol by Klebsiella pneumoniae. Appl. Microbiol. Biotechnol. 50: 24-29. https://doi.org/10.1007/s002530051251
  14. Rao B, Zhang LY, Sun J, Su G, Wei D, Chu J, et al. 2012. Characterization and regulation of the 2,3-butanediol pathway in Serratia marcescens. Appl. Microbiol. Biotechnol. 93: 2147-2159. https://doi.org/10.1007/s00253-011-3608-5
  15. Celinska E, Grajek W. 2009. Biotechnological production of 2,3-butanediol--current state and prospects. Biotechnol. Adv. 27: 715-725. https://doi.org/10.1016/j.biotechadv.2009.05.002
  16. Stormer FC. 1968. Evidence for induction of the 2,3-butanediolforming enzymes in Aerobacter aerogenes. FEBS Lett. 2: 36-38. https://doi.org/10.1016/0014-5793(68)80094-8
  17. Gao S, Guo W, Shi L, Yu Y, Zhang C, Yang H. 2014. Characterization of acetoin production in a budC gene disrupted mutant of Serratia marcescens G12. J. Ind. Microbiol. Biotechnol. 41: 1267-1274. https://doi.org/10.1007/s10295-014-1464-x
  18. Van Houdt R, Moons P, Hueso Buj M, Michiels CW. 2006. N-acyl-L-homoserine lactone quorum sensing controls butanediol fermentation in Serratia plymuthica RVH1 and Serratia marcescens MG1. J. Bacteriol. 188: 4570-4572. https://doi.org/10.1128/JB.00144-06
  19. Givskov M, Ostling J, Eberl L, Lindum PW, Christensen AB, Christiansen G, et al. 1998. Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 742-745. https://doi.org/10.1128/JB.180.3.742-745.1998
  20. Riedel K, Ohnesorg T, Krogfelt KA, Hansen TS, Omori K, Givskov M, et al. 2001. N-acyl-L-homoserine lactone-mediated regulation of the lip secretion system in Serratia liquefaciens MG1. J. Bacteriol. 183: 1805-1809. https://doi.org/10.1128/JB.183.5.1805-1809.2001
  21. Labbate M, Queck SY, Koh KS, Rice SA, Givskov M, Kjelleberg S. 2004. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J. Bacteriol. 186: 692-698. https://doi.org/10.1128/JB.186.3.692-698.2004
  22. Zhang L, Shuang C, Xie H, Tian Y, Hu K. 2012. Efficient acetoin production by optimization of medium components and oxygen supply control using a newly isolated Paenibacillus polymyxa CS107. J. Chem. Technol. Biotechnol. 87: 1551-1557. https://doi.org/10.1002/jctb.3791
  23. Van Houdt R, Aertsen A, Michiels CW. 2007. Quorum-sensing-dependent switch to butanediol fermentation prevents lethal medium acidification in Aeromonas hydrophila AH-1N. Res. Microbiol. 158: 379-385. https://doi.org/10.1016/j.resmic.2006.11.015
  24. Studer SV, Mandel MJ, Ruby EG. 2008. AinS quorum sensing regulates the Vibrio fischeri acetate switch. J. Bacteriol. 190: 5915-5923. https://doi.org/10.1128/JB.00148-08
  25. Xiao Z, Xu P. 2007. Acetoin metabolism in bacteria. Crit. Rev. Microbiol. 33: 127-140. https://doi.org/10.1080/10408410701364604
  26. Byers JT, Lucas C, Salmond GP, Welch M. 2002. Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule. J. Bacteriol. 184: 1163-1171. https://doi.org/10.1128/jb.184.4.1163-1171.2002
  27. Blomqvist K, Nikkola M, Lehtovaara P, Suihko ML, Airaksinen U, Straby KB, et al. 1993. Characterization of the genes of the 2,3-butanediol operons from Klebsiella terrigena and Enterobacter aerogenes. J. Bacteriol. 175: 1392-1404. https://doi.org/10.1128/jb.175.5.1392-1404.1993
  28. Kovacikova G, Lin W, Skorupski K. 2005. Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetateresponsive LysR-type regulator AlsR in Vibrio cholerae. Mol. Microbiol. 57: 420-433. https://doi.org/10.1111/j.1365-2958.2005.04700.x
  29. Moons P, Van Houdt R, Vivijs B, Michiels CW, Aertsen A. 2011. Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1. Appl. Environ. Microbiol. 77: 3422-3427. https://doi.org/10.1128/AEM.02763-10
  30. Horng YT, Deng SC, Daykin M, Soo PC, Wei JR, Luh KT, et al. 2002. The LuxR family protein SpnR functions as a negative regulator of N-acyl homoserine lactone-dependent quorum sensing in Serratia marcescens. Mol. Microbiol. 45: 1655-1671. https://doi.org/10.1046/j.1365-2958.2002.03117.x
  31. Hao Y, Winans SC, Glick BR, Charles TC. 2010. Identification and characterization of new LuxR/LuxI-type quorum sensing systems from metagenomic libraries. Environ. Microbiol. 12: 105-117. https://doi.org/10.1111/j.1462-2920.2009.02049.x
  32. Zhang L, Sun J, Hao Y, Z hu J, Chu J, Wei D, et al. 2010. Microbial production of 2,3-butanediol by a surfactant (serrawettin)-deficient mutant of Serratia marcescens H30. J. Ind. Microbiol. Biotechnol. 37: 857-862. https://doi.org/10.1007/s10295-010-0733-6
  33. Zhang LY, Zhan SR, Chen LZ, Guan X, Hu KH. 2013. Screening of traditional Chinese edible fungi for quorum sensing inhibitors activity. Res. J. Biotechnol. 8: 79-83.

Cited by

  1. Bioelectrochemical Detoxification of Phenolic Compounds during Enzymatic Pre-Treatment of Rice Straw vol.29, pp.11, 2019, https://doi.org/10.4014/jmb.1909.09042
  2. Quorum Sensing System Affects the Plant Growth Promotion Traits of Serratia fonticola GS2 vol.11, 2020, https://doi.org/10.3389/fmicb.2020.536865
  3. Inhibition of Microbial Quorum Sensing Mediated Virulence Factors by Pestalotiopsis sydowiana vol.30, pp.4, 2019, https://doi.org/10.4014/jmb.1907.07030