Skip to main content
SpringerLink
Log in
Book cover

Stress Responses of Lactic Acid Bacteria pp 369–394Cite as

Engineering Robust Lactic Acid Bacteria

  • Chapter
  • First Online:

Part of the book series: Food Microbiology and Food Safety ((FMFS))

Abstract

For centuries, lactic acid bacteria (LAB) have been industrially exploited as starter cultures in the fermentation of foods and feeds for their spoilage-preventing and flavor-enhancing characteristics. More recently, the health-promoting effects of LAB on the consumer have been widely acknowledged, which has led to the introduction of many products containing these probiotic strains. Within this rapidly growing market for the food industry, there is increasing interest in unraveling the molecular mechanisms involved in the stress resistance and robustness of these starter and probiotic strains. This chapter reviews the tools available in the postgenomics era to reveal these molecular mechanisms and the current strategies employed to utilize the information obtained for the rational design of more robust industrial LAB strains.

PAB and HvB-vdV contributed equally to this chapter.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Altermann E, Buck LB, Cano R, Klaenhammer TR (2004) Identification and phenotypic characterization of the cell-division protein CdpA. Gene 342:189–197

    Article  CAS  Google Scholar 

  • Altermann E, Russell WM, Azcarate-Peril MA, Barrangou R, Buck BL, McAuliffe O, Souther N, Dobson A, Duong T, Callanan M, Lick S, Hamrick A, Cano R, Klaenhammer TR (2005) Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci USA 102:3906–3912

    Article  CAS  Google Scholar 

  • Bachmann H, Kleerebezem M, van Hylckama Vlieg JE (2008) High-throughput identification and validation of in situ-expressed genes of Lactococcus lactis. Appl Environ Microbiol 74:4727–4736

    Article  CAS  Google Scholar 

  • Bachmann H, Kruijswijk Z, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE (2009a) A high-throughput cheese manufacturing model for effective cheese starter culture screening. J Dairy Sci 92:5868–5882

    Article  CAS  Google Scholar 

  • Bachmann H, Starrenburg MJC, Dijkstra A, Molenaar D, Kleerebezem M, Rademaker JLW, van Hylckama Vlieg JET (2009b) Regulatory phenotyping reveals important diversity within the species Lactococcus lactis. Appl Environ Microbiol 75:5687–5694

    Article  CAS  Google Scholar 

  • Bachmann H, de Wilt L, Kleerebezem M, van Hylckama Vlieg JE (2010) Timeresolved genetic responses of Lactococcus lactis to a dairy environment. Environ Microbiol 12:1260–1270

    Google Scholar 

  • Boekhorst J, Siezen RJ, Zwahlen MC, Vilanova D, Pridmore RD, Mercenier A, Kleerebezem M, de Vos WM, Brüssow H, Desiere F (2004) The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. Microbiology 150:3601–3611

    Article  CAS  Google Scholar 

  • Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11:731–753

    Article  CAS  Google Scholar 

  • Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek R, Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau S, Boutry M, Delcour J, Goffeau A, Hols P (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22:1554–1558

    Article  CAS  Google Scholar 

  • Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L (2006) A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin Gastroenterol Hepatol 4:754–759

    Article  CAS  Google Scholar 

  • Breiman L (2001) Random forests. Mach Learn 45:5–32

    Article  Google Scholar 

  • Bron PA, Grangette C, Mercenier A, de Vos WM, Kleerebezem M (2004a) Identification of Lactobacillus plantarum genes that are induced in the gastrointestinal tract of mice. J Bacteriol 186:5721–5729

    Article  CAS  Google Scholar 

  • Bron PA, Marco M, Hoffer SM, Van Mullekom E, de Vos WM, Kleerebezem M (2004b) Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J Bacteriol 186:7829–7835

    Article  CAS  Google Scholar 

  • Bron PA, Molenaar D, de Vos WM, Kleerebezem M (2006) DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. J Appl Microbiol 100:728–738

    Article  CAS  Google Scholar 

  • Bron PA, Meijer M, Bongers RS, de Vos WM, Kleerebezem M (2007) Dynamics of competitive population abundance of Lactobacillus plantarum ivi gene mutants in faecal samples after passage through the gastrointestinal tract of mice. J Appl Microbiol 103:1424–1434

    Article  CAS  Google Scholar 

  • Brooijmans R, Smit B, Santos F, van Riel J, de Vos WM, Hugenholtz J (2009) Heme and menaquinone induced electron transport in lactic acid bacteria. Microb Cell Fact 8:28

    Article  Google Scholar 

  • Bruno-Barcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM (2004) Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol 70:4702–4710

    Article  CAS  Google Scholar 

  • Bruno-Barcena JM, Azcarate-Peril MA, Klaenhammer TR, Hassan HM (2005) Marker-free ­chromosomal integration of the manganese superoxide dismutase gene (sodA) from Streptococcus thermophilus into Lactobacillus gasseri. FEMS Microbiol Lett 246:91–101

    Article  CAS  Google Scholar 

  • Coconnier MH, Lievin V, Hemery E, Servin AL (1998) Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl Environ Microbiol 64:4573–4580

    Google Scholar 

  • Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2005) Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71:3060–3067

    Article  CAS  Google Scholar 

  • Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2007) Growth of probiotic lactobacilli in the presence of oleic acid enhances subsequent survival in gastric juice. Microbiology 153:291–299

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • De Angelis M, Gobbetti M (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4:106–122

    Article  Google Scholar 

  • De Angelis M, Bini L, Pallini V, Cocconcelli PS, Gobbetti M (2001) The acid-stress response in Lactobacillus sanfranciscensis CB1. Microbiology 147:1863–1873

    Google Scholar 

  • De Angelis M, Di Cagno R, Huet C, Crecchio C, Fox PF, Gobbetti M (2004) Heat shock response in Lactobacillus plantarum. Appl Environ Microbiol 70:1336–1346

    Article  Google Scholar 

  • De Vries MC (2006) Analyzing global gene expression of Lactobacillus plantarum in the human gastrointestinal tract. PhD thesis. Wageningen University, The Netherlands

    Google Scholar 

  • de Vos WM, Bron PA, Kleerebezem M (2004) Post-genomics of lactic acid bacteria and other food-grade bacteria to discover gut functionality. Curr Opin Biotechnol 15:86–93

    Google Scholar 

  • Denou E, Berger B, Barretto C, Panoff JM, Arigoni F, Brussow H (2007) Gene expression of ­commensal Lactobacillus johnsonii strain NCC533 during in vitro growth and in the murine gut. J Bacteriol 189:8109–8119

    Article  CAS  Google Scholar 

  • Desmond C, Ross RP, O’Callaghan E, Fitzgerald G, Stanton C (2002) Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia. J Appl Microbiol 93:1003–1011

    Article  CAS  Google Scholar 

  • Desmond C, Fitzgerald GF, Stanton C, Ross RP (2004) Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl Environ Microbiol 70:5929–5936

    Article  CAS  Google Scholar 

  • Duwat P, Sourice S, Cesselin B, Lamberet G, Vido K, Gaudu P, Le Loir Y, Violet F, Loubière P, Gruss A (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 183:4509–4516

    Article  CAS  Google Scholar 

  • FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. London, Ontario, Canada

    Google Scholar 

  • Fiocco D, Capozzi V, Goffin P, Hols P, Spano G (2007) Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum. Appl Microbiol Biotechnol 77:909–915

    Article  CAS  Google Scholar 

  • Fiocco D, Capozzi V, Collins M, Gallone A, Hols P, Guzzo J, Weidmann S, Rieu A, Msadek T, Spano G (2010) Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J Bacteriol 192:896–900

    Article  CAS  Google Scholar 

  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512

    Article  CAS  Google Scholar 

  • Frees D, Ingmer H (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol Microbiol 31:79–87

    Article  CAS  Google Scholar 

  • Gotteland M, Cruchet S (2003) Suppressive effect of frequent ingestion of Lactobacillus johnsonii La1 on Helicobacter pylori colonization in asymptomatic volunteers. J Antimicrob Chemother 51:1317–1319

    Google Scholar 

  • Gresham D, Kruglyak L (2008) Rise of the machines. PLoS Genet 4:e1000134

    Article  Google Scholar 

  • Gross G, van der Meulen J, Snel J, van der Meer R, Kleerebezem M, Niewold TA, Hulst MM, Smits MA (2008) Mannose-specific interaction of Lactobacillus plantarum with porcine ­jejunal epithelium. FEMS Immunol Med Microbiol 54:215–223

    Article  CAS  Google Scholar 

  • Gross G, Snel J, Boekhorst J, Smits MA, Kleerebezem M (2010) Biodiversity of mannose-specific adhesion in Lactobacillus plantarum revisited: strain-specific domain composition of the ­mannose-adhesin. Beneficial Microbes 1:61–66

    Article  CAS  Google Scholar 

  • Guzzo J, Jobin M-P, Delmas F, Fortier L-C, Garmyn D, Tourdot-Maréchal R, Lee B, Diviès C (2000) Regulation of stress response in Oenococcus oeni as a function of environmental changes and growth phase. Int J Food Microbiol 55:27–31

    Article  CAS  Google Scholar 

  • Hartke A, Bouche S, Giard JC, Benachour A, Boutibonnes P, Auffray Y (1996) The lactic acid stress response of Lactococcus lactis subsp. lactis. Curr Microbiol 33:194–199

    Article  CAS  Google Scholar 

  • Hartke A, Frere J, Boutibonnes P, Auffray Y (1997) Differential induction of the chaperonin GroEL and the Co-chaperonin GroES by heat, acid, and UV-irradiation in Lactococcus lactis subsp. lactis. Curr Microbiol 34:23–26

    Article  CAS  Google Scholar 

  • Herve-Jimenez L, Guillouard I, Guedon E, Gautier C, Boudebbouze S, Hols P, Monnet V, Rul F, Maguin E (2008) Physiology of Streptococcus thermophilus during the late stage of milk fermentation with special regard to sulfur amino-acid metabolism. Proteomics 8:4273–4286

    Article  CAS  Google Scholar 

  • Herve-Jimenez L, Guillouard I, Guedon E, Boudebbouze S, Hols P, Monnet V, Maguin E, Rul F (2009) Postgenomic analysis of Streptococcus thermophilus cocultivated in milk with Lactobacillus delbrueckii subsp. bulgaricus: involvement of nitrogen, purine, and iron metabolism. Appl Environ Microbiol 75:2062–2073

    Article  CAS  Google Scholar 

  • Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guédon E, Monnet V, Renault P, Kleerebezem M (2005) New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 29:435–463

    CAS  Google Scholar 

  • Hufner E, Markieton T, Chaillou S, Crutz-Le Coq AM, Zagorec M, Hertel C (2007) Identification of Lactobacillus sakei genes induced during meat fermentation and their role in survival and growth. Appl Environ Microbiol 73:2522–2531

    Article  Google Scholar 

  • Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx AP, Lebeer S, De Keersmaecker SC, Vanderleyden J, Hämäläinen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjärvi T, Auvinen P, de Vos WM (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci USA 106:17193–17198

    Article  CAS  Google Scholar 

  • Kets E, Teunissen P, de Bont J (1996) Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Appl Environ Microbiol 62:259–261

    CAS  Google Scholar 

  • Kilstrup M, Jacobsen S, Hammer K, Vogensen FK (1997) Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl Environ Microbiol 63:1826–1837

    CAS  Google Scholar 

  • Kim WS, Perl L, Park JH, Tandianus JE, Dunn NW (2001) Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr Microbiol 43:346–350

    Article  CAS  Google Scholar 

  • Klaenhammer TR, Barrangou R, Buck BL, Azcarate-Peril MA, Altermann E (2005) Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29:393–409

    Article  CAS  Google Scholar 

  • Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 100:1990–1995

    Article  CAS  Google Scholar 

  • Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, Bron PA (2010) The extracellular biology of the lactobacilli. FEMS Microbiol Rev 34:199–230

    Article  CAS  Google Scholar 

  • Kleerebezem M, Vaughan EE (2009) Probiotic and Gut Lactobacilli and Bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63:269–290

    Google Scholar 

  • Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764, table of contents

    Google Scholar 

  • Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrêne Y, Vanderleyden J, De Keersmaecker SC (2009) Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol 75:3554–3563

    Article  CAS  Google Scholar 

  • Leverrier P, Dimova D, Pichereau V, Auffray Y, Boyaval P, Jan G (2003) Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl Environ Microbiol 69:3809–3818

    Article  CAS  Google Scholar 

  • Lorca GL, Font de Valdez G, Ljungh A (2002) Characterization of the protein-synthesis dependent adaptive acid tolerance response in Lactobacillus acidophilus. J Mol Microbiol Biotechnol 4:525–532

    CAS  Google Scholar 

  • Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Díaz-Muñiz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103:15611–15616

    Article  Google Scholar 

  • Marco ML, Peters TH, Bongers RS, Molenaar D, van Hemert S, Sonnenburg JL, Gordon JI, Kleerebezem M (2009) Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ Microbiol 11:2747–2757

    Article  CAS  Google Scholar 

  • Macro ML, Wels M, de vos WM, Vaughan EE, Kleerebezem M (2010) Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J 11:1481–1484

    Article  CAS  Google Scholar 

  • Martini MC, Lerebours EC, Lin WJ, Harlander SK, Berrada NM, Antoine JM, Savaiano DA (1991) Strains and species of lactic acid bacteria in fermented milks (yogurts): effect on in vivo lactose digestion. Am J Clin Nutr 54:1041–1046

    CAS  Google Scholar 

  • McLeod A, Nyquist OL, Snipen L, Naterstad K, Axelsson L (2008) Diversity of Lactobacillus sakei strains investigated by phenotypic and genotypic methods. Syst Appl Microbiol 31:393–403

    Article  CAS  Google Scholar 

  • Meijerink M, van Hemert S, Taverne N, Wels M, de vos P, Bron PA, Savelkoul HF, Van Bilsen J, Kleerebezem M, Wells JM (2010) Identification of generic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLos One 5:e10632

    Article  CAS  Google Scholar 

  • Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, Kleerebezem M (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187:6119–6127

    Article  CAS  Google Scholar 

  • Noonpakdee W, Sitthimonchai S, Panyim S, Lertsiri S (2004) Expression of the catalase gene katA in starter culture Lactobacillus plantarum TISTR850 tolerates oxidative stress and reduces lipid oxidation in fermented meat product. Int J Food Microbiol 95:127–135

    Article  CAS  Google Scholar 

  • O’Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, O’Sullivan GC, Kiely B, Collins JK, Shanahan F, Quigley EM (2005) Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128:541–551

    Article  Google Scholar 

  • O’Sullivan E, Condon S (1997) Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis. Appl Environ Microbiol 63:4210–4215

    Google Scholar 

  • Perea Velez M, Verhoeven TL, Draing C, Von Aulock S, Pfitzenmaier M, Geyer A, Lambrichts I, Grangette C, Pot B, Vanderleyden J, De Keersmaecker SC (2007) Functional analysis of D-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73:3595–3604

    Article  Google Scholar 

  • Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR (2007) Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J Bacteriol 189:4624–4634

    Article  CAS  Google Scholar 

  • Pieterse B (2006) Transcriptome analysis of the lactic acid and NaCI-stress response of Lactobacillus plantarum. PhD thesis. Wageningen University, The Netherlands

    Google Scholar 

  • Pieterse B, Leer RJ, Schuren FH, van der Werf MJ (2005) Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151:3881–3894

    Article  CAS  Google Scholar 

  • Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917–925

    Article  CAS  Google Scholar 

  • Pretzer G, Snel J, Molenaar D, Wiersma A, Bron PA, Lambert J, de Vos WM, van der Meer R, Smits MA, Kleerebezem M (2005) Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J Bacteriol 187:6128–6136

    Article  CAS  Google Scholar 

  • Pridmore RD, Berger B, Desiere F, Vilanova D, Barretto C, Pittet AC, Zwahlen MC, Rouvet M, Altermann E, Barrangou R, Mollet B, Mercenier A, Klaenhammer T, Arigoni F, Schell MA (2004) The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci USA 101:2512–2517

    Article  CAS  Google Scholar 

  • Rainey PB, Preston GM (2000) In vivo expression technology strategies: valuable tools for ­biotechnology. Curr Opin Biotechnol 11:440–444

    Article  CAS  Google Scholar 

  • Rauch PJ, De Vos WM (1992) Characterization of the novel nisin-sucrose conjugative transposon Tn5276 and its insertion in Lactococcus lactis. J Bacteriol 174:1280–1287

    CAS  Google Scholar 

  • Rediers H, Rainey PB, Vanderleyden J, De Mot R (2005) Unraveling the secret lives of bacteria: use of in vivo expression technology and differential fluorescence induction promoter traps as tools for exploring niche-specific gene expression. Microbiol Mol Biol Rev 69:217–261

    Article  CAS  Google Scholar 

  • Rochat T, Gratadoux JJ, Corthier G, Coqueran B, Nader-Macias ME, Gruss A, Langella P (2005a) Lactococcus lactis SpOx spontaneous mutants: a family of oxidative-stress-resistant dairy strains. Appl Environ Microbiol 71:2782–2788

    Article  CAS  Google Scholar 

  • Rochat T, Miyoshi A, Gratadoux JJ, Duwat P, Sourice S, Azevedo V, Langella P (2005b) High-level resistance to oxidative stress in Lactococcus lactis conferred by Bacillus subtilis catalase KatE. Microbiology 151:3011–3018

    Article  CAS  Google Scholar 

  • Salotra P, Singh DK, Seal KP, Krishna N, Jaffe H, Bhatnagar R (1995) Expression of DnaK and GroEL homologs in Leuconostoc esenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol Lett 131:57–62

    Article  CAS  Google Scholar 

  • Serrano LM, Molenaar D, Wels M, Teusink B, Bron PA, de Vos WM, Smid EJ (2007) Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microb Cell Fact 6:29

    Article  Google Scholar 

  • Sheehan VM, Sleator RD, Fitzgerald GF, Hill C (2006) Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:2170–2177

    Article  CAS  Google Scholar 

  • Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145

    Article  CAS  Google Scholar 

  • Siezen RJ, Wilson G (2010) Probiotic genomics. Microbial Biotechnology 3:1–9

    Article  CAS  Google Scholar 

  • Siezen RJ, Renckens B, van Swam I, Peters S, van Kranenburg R, Kleerebezem M, de Vos WM (2005) Complete sequences of four plasmids of Lactococcus lactis subsp. cremoris SK11 reveal extensive adaptation to the dairy environment. Appl Environ Microbiol 71:8371–8382

    Article  CAS  Google Scholar 

  • Siezen R, Boekhorst J, Muscariello L, Molenaar D, Renckens B, Kleerebezem M (2006) Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific Gram-positive bacteria. BMC Genom 7:126

    Article  Google Scholar 

  • Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HT, Rademaker JL, Starrenburg MJ, Kleerebezem M, Molenaar D, van Hylckama Vlieg JE (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12:758–773

    Article  CAS  Google Scholar 

  • Sleator RD, Hill C (2006) Patho-biotechnology: using bad bugs to do good things. Curr Opin Biotechnol 17:211–216

    Article  CAS  Google Scholar 

  • Smiddy M, Sleator RD, Patterson MF, Hill C, Kelly AL (2004) Role for compatible solutes glycine betaine and L-carnitine in listerial barotolerance. Appl Environ Microbiol 70:7555–7557

    Article  CAS  Google Scholar 

  • Smit G, Smit BA, Engels WJ (2005) Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev 29:591–610

    Article  CAS  Google Scholar 

  • Spano G, Massa S (2006) Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Crit Rev Microbiol 32:77–86

    Article  CAS  Google Scholar 

  • Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermeire A, Goddeeris B, Cox E, Remon JP, Remaut E (2003) Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol 21:785–789

    Article  CAS  Google Scholar 

  • van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82:187–216

    Article  Google Scholar 

  • van Hemert S, Meijerink M, Molenaar D, Bron PA, de Vos P, Kleerebezem M, Wells JM, Marco ML (2010) Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol 10:293

    Article  Google Scholar 

  • van Kranenburg R, Golic N, Bongers R, Leer RJ, de Vos WM, Siezen RJ, Kleerebezem M (2005) Functional analysis of three plasmids from Lactobacillus plantarum. Appl Environ Microbiol 71:1223–1230

    Article  Google Scholar 

  • Veening JW, Smits WK, Kuipers OP (2008a) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62:193–210

    Article  CAS  Google Scholar 

  • Veening JW, Stewart EJ, Berngruber TW, Taddei F, Kuipers OP, Hamoen LW (2008b) Bet-hedging and epigenetic inheritance in bacterial cell development. Proc Natl Acad Sci USA 105:4393–4398

    Article  CAS  Google Scholar 

  • Vogel RF, Pavlovic M, Hormann S, Ehrmann MA (2005) High pressure-sensitive gene expression in Lactobacillus sanfranciscensis. Braz J Med Biol Res 38:1247–1252

    Article  CAS  Google Scholar 

  • Wall T, Bath K, Britton RA, Jonsson H, Versalovic J, Roos S (2007) The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl Environ Microbiol 73:3924–3935

    Article  CAS  Google Scholar 

  • Walter J, Heng NC, Hammes WP, Loach DM, Tannock GW, Hertel C (2003) Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl Environ Microbiol 69:2044–2051

    Article  CAS  Google Scholar 

  • Walter J, Loach DM, Alqumber M, Rockel C, Hermann C, Pfitzenmaier M, Tannock GW (2007) D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100–23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 9:1750–1760

    Article  CAS  Google Scholar 

  • Wels M (2008) Unraveling the regulatory network of Lactobacillus plantarum WCFS1 (Thesis), pp. 1–192, Wageningen University, The Netherlands

    Google Scholar 

  • Wels M, Francke C, Kerkhoven R, Kleerebezem M, Siezen RJ (2006) Predicting cis-acting ­elements of Lactobacillus plantarum by comparative genomics with different taxonomic ­subgroups. Nucleic Acids Res 34:1947–1958

    Article  CAS  Google Scholar 

  • Whitehead K, Versalovic J, Roos S, Britton RA (2008) Genomic and genetic characterization of the bile stress response of probiotic Lactobacillus reuteri ATCC 55730. Appl Environ Microbiol 74:1812–1819

    Article  CAS  Google Scholar 

  • Xie Y, Chou LS, Cutler A, Weimer B (2004) DNA Macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl Environ Microbiol 70:6738–6747

    Article  CAS  Google Scholar 

  • Zoetendal EG, Booijink CCGM, Klaassens ES, Heilig HGHJ, Kleerebezem M, Smidt H, de Vos WM (2006) Isolation of RNA from bacterial samples of the human gastrointestinal tract. Nat Protoc 1:954–959

    Article  CAS  Google Scholar 

  • Zomer A, Fernandez M, Kearney B, Fitzgerald GF, Ventura M, van Sinderen D (2009) An interactive regulatory network controls stress response in Bifidobacterium breve UCC2003. J Bacteriol 191:7039–7049

    Article  CAS  Google Scholar 

  • Zotta T, Asterinou K, Rossano R, Ricciardi A, Varcamonti M, Parente E (2009) Effect of inactivation of stress response regulators on the growth and survival of Streptococcus thermophilus Sfi39. Int J Food Microbiol 129:211–220

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. TI Food and Nutrition, Nieuwe Kanaal 9A, 6709 PA, Wageningen, The Netherlands

    Peter A. Bron, Hermien van Bokhorst-van de Veen, Michiel Wels & Michiel Kleerebezem

  2. NIZO Food Research, 20, 6710 BA, Ede, The Netherlands

    Peter A. Bron, Hermien van Bokhorst-van de Veen, Michiel Wels & Michiel Kleerebezem

  3. Kluyver Centre for Genomics of Industrial Fermentation, Julianalaan 67, 2628 BC, Delft, The Netherlands

    Peter A. Bron

  4. Laboratory for Microbiology, Wageningen University, Dreijeplein 10, 6703 HB, Wageningen, The Netherlands

    Hermien van Bokhorst-van de Veen & Michiel Kleerebezem

  5. Center for Molecular and Biomolecular Informatics, Radboud University Nijmegen Medical Center, 9101, 6500 HB, Nijmegen, The Netherlands

    Michiel Wels

Authors
  1. Peter A. Bron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hermien van Bokhorst-van de Veen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michiel Wels
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michiel Kleerebezem
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michiel Kleerebezem .

Editor information

Editors and Affiliations

  1. Laboratory of Dairy Research, Department of Food Science and Technolog, Agricultural University of Athens, Iera Odos 75, Athens, 118 55, Greece

    Effie Tsakalidou

  2. Laboratory of Dairy Research, Department of Food Science and Technolog, Agricultural University of Athens, Iera Odos 75, Athens, 188 55, Greece

    Konstantinos Papadimitriou

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Bron, P.A., van Bokhorst-van de Veen, H., Wels, M., Kleerebezem, M. (2011). Engineering Robust Lactic Acid Bacteria. In: Tsakalidou, E., Papadimitriou, K. (eds) Stress Responses of Lactic Acid Bacteria. Food Microbiology and Food Safety. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-92771-8_16

Download citation

Publish with us

Policies and ethics

Search

Navigation