Annals of Microbiology

, Volume 68, Issue 5, pp 287–294 | Cite as

The response of LuxS/AI-2 quorum sensing in Lactobacillus fermentum 2-1 to changes in environmental growth conditions

  • Yue Gu
  • Bo Li
  • Jianjun Tian
  • Rong Wu
  • Yinfeng He
Original Article


Quorum sensing (QS) is a communication mechanism based on the production of autoinducers in order to regulate cooperative behavior and physiological traits among bacteria. Autoinducer-2 (AI-2) is mediated by luxS and pfs genes and is used for both intra- and interspecies communication. The effects of environmental stresses, such as pH, temperature, osmotic, and nutrient stresses, were investigated on the LuxS/AI-2 QS system in Lactobacillus fermentum 2-1. The AI-2 activity in L. fermentum 2-1 was induced by stress responses to acid shock, high temperature, and nutrient inadequacy while a decrease in activity was correlated with high pH, low temperature, and osmotic stress. Maximum transcription of luxS and pfs was achieved after L. fermentum 2-1 was exposed to acid shock, low temperature, high concentration of NaCl, and diluted MRS broth. The results indicate that various stresses affected the LuxS/AI-2 QS system, which may be involved in the resistance process of the L. fermentum 2-1.


Quorum sensing Lactobacillus fermentum 2-1 Autoinducer-2 Transcription Environmental stresses 


Funding information

This project was supported by the Program of National Natural Science Foundation of China (No. 31360396).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bonsaglia ECR, Silva NCC, Fernades Júnior A, Araújo Júnior JP, Tsunemi MH, Rall VLM (2014) Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control 35:386–391CrossRefGoogle Scholar
  2. Buck BL, Azcarate-Peril MA, Klaenhammer TR (2009) Role of autoinducer-2 on the adhesion ability of Lactobacillus acidophilus. J Appl Microbiol 107:269–279CrossRefPubMedGoogle Scholar
  3. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassier BL, Hughson FM (2002) Structural identification of a bacterial quorum sensing signal containing boron. Nature 415:545–549CrossRefPubMedGoogle Scholar
  4. Cotter PD, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453CrossRefPubMedPubMedCentralGoogle Scholar
  5. De Keersmaecker SCJ, Vanderleyden J (2003) Constraints on detection of autoinducer-2 (AI-2) signaling molecules using Vibrio harveyi as a reporter. Microbiol Comment 149:1953–1956CrossRefGoogle Scholar
  6. De Man JC, Rogosa M, Sharpe ME (1960) A medium for the cultivation of lactobacilli. J Appl Microbiol 23:130–135Google Scholar
  7. Delisa MP, Wu CF, Wang L, Valdes JJ, Bentley WE (2001) DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183:5239–5247CrossRefPubMedPubMedCentralGoogle Scholar
  8. Federle MJ, Bassler BL (2003) Interspecies communication in bacteria. J Clin Invest 112:1291–1299CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254–261CrossRefPubMedGoogle Scholar
  10. Greenberg EP, Hastings JW, Ulitzur S (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87–91CrossRefGoogle Scholar
  11. Guchte MVD, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82:187–216CrossRefPubMedGoogle Scholar
  12. Guo Y, Tian X, Huang R, Tao X, Shah NP, Wei H, Wan C (2017) A physiological comparative study of acid tolerance of Lactobacillus plantarum ZDY 2013 and L. plantarum ATCC 8014 at membrane and cytoplasm levels. Ann Microbiol 67:669–677CrossRefGoogle Scholar
  13. Heurlier K, Vendeville A, Halliday N, Green A, Winzer K, Tang CM, Hardie KR (2009) Growth deficiencies of Neisseria meningitidis pfs and luxS mutants are not due to inactivation of quorum sensing. J Bacteriol 191:1293–1302CrossRefPubMedGoogle Scholar
  14. Jutfelt F (2006) The intestinal epithelium of salmonids: transepithelial transport, barrier function and bacterial interactions. PhD Thesis, Department of Zoology, Göteborg UniversityGoogle Scholar
  15. Kaper JB, Sperandio V (2005) Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect Immun 73:3197–3209CrossRefPubMedPubMedCentralGoogle Scholar
  16. Klein G, Pack A, Bonaparte C, Reuter G (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103–125CrossRefPubMedGoogle Scholar
  17. Lebeer S, De Keersmaecker SCJ (2007) Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J Bacteriol 189:860–871CrossRefPubMedGoogle Scholar
  18. Lebeer S, Claes IJ, Verhoeven TL, Shen C, Lambrichts I, Ceuppens JL, Vanderleyden J, De Keersmaecker SC (2008) Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus GG. Appl Environ Microbiol 74:4711–4718CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li J, Chen J, Vidal JE, McClane BA (2011) The Agr-like quorum-sensing system regulates sporulation and production of enterotoxin and beta2 toxin by Clostridium perfringens type A non-food-borne human gastrointestinal disease strain F5603. Infect Immun 79:451–459Google Scholar
  20. Li B, Gu Y, Yan CL, Jia YB, He YF (2016) Screening and identification of AI-2 high-producing lactic acid bacteria. Food Sci Technol 37:185–188 (In Chinese with English Abstract)Google Scholar
  21. Lin L, Li T, Dai S, Yu JL, Chen XQ, Wang LY, Wang YG, Hua YJ, Tian B (2016) Autoinducer-2 signaling is involved in regulation of stress-related genes of Deinococcus radiodurans. Arch Microbiol 198:43–51CrossRefPubMedGoogle Scholar
  22. Liu C, Wang L, Li T, Lin L, Dai S, Tian B, Hua Y (2014) A PerR-like protein involved in response to oxidative stress in the extreme bacterium Deinococcus radiodurans. Biochem Biophys Res Commun 450:575–580CrossRefPubMedGoogle Scholar
  23. Marshall J (2013) Quorum sensing. Proc Natl Acad Sci U S A 110(8):2690CrossRefPubMedPubMedCentralGoogle Scholar
  24. Meng L, Du Y, Liu P, Li X, Liu Y (2017) Involvement of LuxS in Aeromonas salmonicida metabolism, virulence and infection in Atlantic salmon (salmo salar L). Fish Shellfish Immunol 64:260–269CrossRefPubMedGoogle Scholar
  25. Meurman JH, Stamatova I (2007) Probiotics: contributions to oral health. Oral Dis 13:443–451CrossRefPubMedGoogle Scholar
  26. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199CrossRefPubMedGoogle Scholar
  27. Moslehi-Jenabian S, Gori K, Jespersen L (2009) AI-2 signaling is induced by acidic shock in probiotic strain of Lactobacillus spp. Int J Food Microbiol 135:295–302CrossRefPubMedGoogle Scholar
  28. Park H, Shin H, Lee K, Holzapfel W (2016) Autoinducer-2 properties of kimchi are associated with lactic acid bacteria involved in its fermentation. Int J Food Microbiol 225:38–42CrossRefPubMedGoogle Scholar
  29. Parveen N, Cornell KA (2011) Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism. Mol Microbiol 2011:7–20CrossRefGoogle Scholar
  30. Parvez S, Malik KA, Ah Kang S, Kim HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100:1171–1185CrossRefPubMedGoogle Scholar
  31. Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christophersen C, Steinberg P, Kjelleber S, Givskov M (2000) How Delisea pulchrafuranones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146:3237–3244CrossRefPubMedGoogle Scholar
  32. Rogers PD, Liu TT, Barker KS, Hilliard GM, English BK, Thornton J, Swiatlo E, McDaniel LS (2007) Gene expression profiling of the response of Streptococcus pneumoniae to penicillin. J Antimicrob Chemother 59:616–626CrossRefPubMedGoogle Scholar
  33. Rosenquist H, Hansen D (1998) The antimicrobial effect of organic acids, sourdough and nisin against Bacillus subtilis and Bacillus licheniformis isolated from wheat bread. J Appl Microbiol 85:621–626CrossRefGoogle Scholar
  34. Sun SJ, Liu HJ, Weng CH, Lai CF, Ai LY, Liu YC, Zhu H (2016) The response of Serratia marcescens JG to environmental changes by quorum sensing system. Arch Microbiol 198:585–590CrossRefPubMedGoogle Scholar
  35. Surette MG, Bassler BL (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci USA 95:7046–7050CrossRefPubMedPubMedCentralGoogle Scholar
  36. Wen ZT, Burne RA (2004) LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. J Bacteriol 186:2682–2691CrossRefPubMedPubMedCentralGoogle Scholar
  37. Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MT, Linforth R, Cornell KA, Taylor AJ, Hill PJ, Williams P (2002) LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148:909–922CrossRefPubMedGoogle Scholar
  38. Wu C, Zhang J, Du G, Chen J (2013) Aspartate protects Lactobacillus casei against acid stress. Appl Microbiol Biotechnol 97:4083–4093CrossRefPubMedGoogle Scholar
  39. Yeo S, Park H, Ji Y, Park S, Yang J, Lee J, Mathara JM, Shin H, Holzapfel W (2015) Influence of gastrointestinal stress on autoinducer-2 activity of two lactobacillus species. FEMS Microbiol Ecol 91:1–9CrossRefGoogle Scholar
  40. Yu J, Madsen ML, Carruthers MD, Phillips GJ, Kavanaugh JS, Boyd JM, Horswill AR, Chris Minion F (2013) Analysis of autoinducer-2 quorum sensing in yersinia pestis. Infect Immun 81:4053–4062CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhu H, Liu HJ, Ning SJ, Gao YL (2011) A luxS-dependent transcript profile of cell-to-cell communication in Klebsiella pneumonia. Mol BioSyst 7:3164–3168CrossRefPubMedGoogle Scholar
  42. Zhu H, Liu HJ, Ning SJ, Gao YL (2012) The response of type 2 quorum sensing in Klebsiella pneumoniae to a fluctuating culture environment. DNA Cell Biol 31:455–459CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018

Authors and Affiliations

  • Yue Gu
    • 1
  • Bo Li
    • 1
  • Jianjun Tian
    • 1
  • Rong Wu
    • 1
  • Yinfeng He
    • 1
  1. 1.College of Food Science and EngineeringInner Mongolia Agricultural UniversityHohhotChina

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