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Comparative Genomic Analysis of Two-Component Signal Transduction Systems in Probiotic Lactobacillus casei

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Abstract

Lactobacillus casei has traditionally been recognized as a probiotic, thus needing to survive the industrial production processes and transit through the gastrointestinal tract before providing benefit to human health. The two-component signal transduction system (TCS) plays important roles in sensing and reacting to environmental changes, which consists of a histidine kinase (HK) and a response regulator (RR). In this study we identified HKs and RRs of six sequenced L. casei strains. Ortholog analysis revealed 15 TCS clusters (HK–RR pairs), one orphan HKs and three orphan RRs, of which 12 TCS clusters were common to all six strains, three were absent in one strain. Further classification of the predicted HKs and RRs revealed interesting aspects of their putative functions. Some TCS clusters are involved with the response under the stress of the bile salts, acid, or oxidative, which contribute to survive the difficult journey through the human gastrointestinal tract. Computational predictions of 15 TCSs were verified by PCR experiments. This genomic level study of TCSs should provide valuable insights into the conservation and divergence of TCS proteins in the L. casei strains.

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References

  1. Corcoran BM, Stanton C, Fitzgerald G, Ross RP (2008) Life under stress: the probiotic stress response and how it may be manipulated. Curr Pharm Des 14:1382–1399. doi:10.2174/138161208784480225

    Article  CAS  PubMed  Google Scholar 

  2. Santivarangkna C, Kulozik U, Foerst P (2008) Inactivation mechanisms of lactic acid starter cultures preserved by drying processes. J Appl Microbiol 105:1–13. doi:10.1111/j.1365-2672.2008.03744.x

    Article  CAS  PubMed  Google Scholar 

  3. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215. doi:10.1146/annurev.biochem.69.1.183

    Article  CAS  PubMed  Google Scholar 

  4. Karniol B, Vierstra RD (2004) The HWE histidine kinases, a new family of bacterial two-component sensor kinases with potentially diverse roles in environmental signaling. J Bacteriol 186:445–453. doi:10.1128/Jb.186.2.445-453.2004

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182. doi:10.1128/Jb.01887-05

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Marco ML, Pavan S, Kleerebezem M (2006) Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17:204–210. doi:10.1016/j.copbio.2006.02.005

    Article  CAS  PubMed  Google Scholar 

  7. de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Food Biotechnol 111:1–66. doi:10.1007/10_2008_097

    Article  Google Scholar 

  8. Zhu Y, Zhang YP, Li Y (2009) Understanding the industrial application potential of lactic acid bacteria through genomics. Appl Microbiol Biotechnol 83:597–610. doi:10.1007/s00253-009-2034-4

    Article  CAS  PubMed  Google Scholar 

  9. Landete JM, Garcia-Haro L, Blasco A, Manzanares P, Berbegal C, Monedero V, Zuniga M (2010) Requirement of the Lactobacillus casei MaeKR two-component system for l-malic acid utilization via a malic enzyme pathway. Appl Environ Microbiol 76:84–95. doi:10.1128/Aem.02145-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Alcantara C, Revilla-Guarinos A, Zuniga M (2011) Influence of two-component signal transduction systems of Lactobacillus casei BL23 on tolerance to stress conditions. Appl Environ Microbiol 77:1516–1519. doi:10.1128/Aem.02176-10

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. de Been M, Francke C, Moezelaar R, Abeel T, Siezen RJ (2006) Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis. Microbiology 152:3035–3048. doi:10.1099/mic.0.29137-0

    Article  PubMed  Google Scholar 

  12. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301. doi:10.1093/Nar/Gkr1065

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Fischer S, Brunk BP, Chen F, Gao X, Harb OS, Iodice JB, Shanmugam D, Roos DS, Stoeckert CJ Jr (2011) Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr Protoc Bioinformatics 12:11–19. doi:10.1002/0471250953.bi0612s35 Chap. 6: Unit 6

    Google Scholar 

  14. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34:D257–D260. doi:10.1093/Nar/Gkj079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. doi:10.1006/jmbi 2000.4315

    Article  CAS  PubMed  Google Scholar 

  16. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  PubMed  Google Scholar 

  17. Mascher T, Helmann JD, Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70:910–938. doi:10.1128/Mmbr.00020-06

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Zhulin IB, Taylor BL (1997) PAS domain S-boxes in Archaea, bacteria and sensors for oxygen and redox. Trends Biochem Sci 22:331–333. doi:10.1016/S0968-0004(97)01110-9

    Article  CAS  PubMed  Google Scholar 

  20. Aravind L, Ponting CP (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176:111–116. doi:10.1111/j.1574-6968.1999.tb13650.x

    Article  CAS  PubMed  Google Scholar 

  21. Hefti MH, Francoijs KJ, de Vries SC, Dixon R, Vervoort J (2004) The PAS fold: a redefinition of the PAS domain based upon structural prediction. Eur J Biochem 271:1198–1208. doi:10.1111/j.1432-1033.2004.04023.x

    Article  CAS  PubMed  Google Scholar 

  22. Bott M, Meyer M, Dimroth P (1995) Regulation of anaerobic citrate metabolism in Klebsiella pneumoniae. Mol Microbiol 18:533–546. doi:10.1111/j.1365-2958.1995.mmi_18030533.x

    Article  CAS  PubMed  Google Scholar 

  23. Yamamoto K, Matsumoto F, Oshima T, Fujita N, Ogasawara N, Ishihama A (2008) Anaerobic regulation of citrate fermentation by CitAB in Escherichia coli. Biosci Biotechnol Biochem 72:3011–3014. doi:10.1271/Bbb.80301

    Article  CAS  PubMed  Google Scholar 

  24. Ingmer H, Miller CA, Cohen SN (1998) Destabilized inheritance of pSC101 and other Escherichia coli plasmids by DpiA, a novel two-component system regulator. Mol Microbiol 29:49–59. doi:10.1046/j.1365-2958.1998.00895.x

    Article  CAS  PubMed  Google Scholar 

  25. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:1629–1631. doi:10.1126/science.1101630

    Article  CAS  PubMed  Google Scholar 

  26. Nikolskaya AN, Galperin MY (2002) A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res 30:2453–2459. doi:10.1093/nar/30.11.2453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Galperin MY (2008) Telling bacteria: do not LytTR. Structure 16:657–659. doi:10.1016/j.str.2008.04.003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. MartinezHackert E, Stock AM (1997) The DNA-binding domain of OmpR: crystal structure of a winged helix transcription factor. Structure 5:109–124. doi:10.1016/S0969-2126(97)00170-6

    Article  CAS  Google Scholar 

  29. Lavin JL, Kiil K, Resano O, Ussery DW, Oguiza JA (2007) Comparative genomic analysis of two-component regulatory proteins in Pseudomonas syringae. BMC Genomics 8:397. doi:10.1186/1471-2164-8-397

    Article  PubMed Central  PubMed  Google Scholar 

  30. Qian W, Han ZJ, He CZ (2008) Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol Plant Microbe Interact 21:151–161. doi:10.1094/Mpmi-21-2-0151

    Article  CAS  PubMed  Google Scholar 

  31. Zhao YF, Wang DP, Nakka S, Sundin GW, Korban SS (2009) Systems level analysis of two-component signal transduction systems in Erwinia amylovora: role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics 10:245. doi:10.1186/1471-2164-10-245

    Article  PubMed Central  PubMed  Google Scholar 

  32. Jordan S, Hutchings MI, Mascher T (2008) Cell envelope stress response in gram-positive bacteria. FEMS Microbiol Rev 32:107–146. doi:10.1111/j.1574-6976.2007.00091.x

    Article  CAS  PubMed  Google Scholar 

  33. Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S, Feeney M, Flynn S, Fitzgerald G, Daly C, Kiely B, O’Sullivan GC, Shanahan F, Collins JK (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386s–392s

    CAS  PubMed  Google Scholar 

  34. Wu R, Sun Z, Wu J, Meng H, Zhang H (2010) Effect of bile salts stress on protein synthesis of Lactobacillus casei Zhang revealed by 2-dimensional gel electrophoresis. J Dairy Sci 93:3858–3868. doi:10.3168/jds.2009-2967

    Article  CAS  PubMed  Google Scholar 

  35. Kobayashi K, Ogura M, Yamaguchi H, Yoshida KI, Ogasawara N, Tanaka T, Fujita Y (2001) Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J Bacteriol 183:7365–7370. doi:10.1128/Jb.183.24.7365- 7370.2001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Muller C, Sanguinetti M, Riboulet E, Hebert L, Posteraro B, Fadda G, Auffray Y, Rince A (2008) Characterization of two signal transduction systems involved in intracellular macrophage survival and environmental stress response in Enterococcus faecalis. J Mol Microbiol Biotechnol 14:59–66. doi:10.1159/000106083

    Article  CAS  PubMed  Google Scholar 

  37. Hobbs EC, Astarita JL, Storz G (2010) Small RNAs and small proteins involved in resistance to cell envelope stress and acid shock in Escherichia coli: analysis of a bar-coded mutant collection. J Bacteriol 192:59–67. doi:10.1128/Jb.00873-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Heermann R, Fuchs TM (2008) Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics 9:40. doi:10.1186/1471-2164-9-40

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Open Project Program of State Key Laboratory of Dairy Biotechnology, Bright Dairy & Food Co. Ltd., (No. SKLDB2012-007).

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Authors and Affiliations

  1. State Key Laboratory of Dairy Biotechnology, Bright Dairy & Food Co. Ltd, Shanghai, 200436, People’s Republic of China

    Shuijing Yu & Wanyi Chen

  2. Faculty of Resource and Environmental Engineering, Jiangxi University of Science and Technology, No. 86, Hongqi Ave., Ganzhou, 341000, Jiangxi, People’s Republic of China

    Shuijing Yu, Yanping Peng, Yangwu Deng & Yanhua Guo

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  1. Shuijing Yu
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Correspondence to Shuijing Yu.

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Yu, S., Peng, Y., Chen, W. et al. Comparative Genomic Analysis of Two-Component Signal Transduction Systems in Probiotic Lactobacillus casei . Indian J Microbiol 54, 293–301 (2014). https://doi.org/10.1007/s12088-014-0456-x

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