Modulation of Lactobacillus plantarum gastrointestinal robustness by fermentation conditions enables identification of bacterial robustness markers

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  van Bokhorst van de Veen, Hermien ^a,b,c   Lee, I Chiao ^a,b,c   Marco, Maria L ^a,b,f   Wels, Michiel ^a,b,d   Bron, Peter A ^a,b,e   Kleerebezem, Michiel ^a,b,c  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b NIZO FOOD RESEARCH   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARAC PROTEIN; PENICILLIN BINDING PROTEIN 2A; PROTEIN NAPA3; SODIUM PROTON EXCHANGE PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL SURVIVAL; BACTERIUM CULTURE; CONTROLLED STUDY; FERMENTATION MEDIUM; FERMENTATION TECHNIQUE; GASTROINTESTINAL TRACT; IN VITRO STUDY; LACTOBACILLUS PLANTARUM; NONHUMAN; PROTEIN FUNCTION; STOMACH PH; STRAIN DIFFERENCE;

BACTERIAL PROTEINS; BILE ACIDS AND SALTS; CULTURE MEDIA; FERMENTATION; GASTRIC ACID; GASTROINTESTINAL TRACT; HYDROGEN-ION CONCENTRATION; LACTOBACILLUS PLANTARUM; PENICILLIN-BINDING PROTEINS; PROBIOTICS; SODIUM-HYDROGEN ANTIPORTER;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS PLANTARUM;

EID: 84863607203     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039053     Document Type: Article

References (55)

1. FAO/WHO (2001) Evaluation of health and nutritional properties of powder milk with live lactic acid bacteria. Report of FAO/WHO expert consultation 1-4 October.
2. Marco ML, Pavan S, Kleerebezem M, (2006) Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17: 204-210.
3. Lebeer S, Vanderleyden J, De Keersmaecker SC, (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8: 171-184.
4. Bron PA, van Baarlen P, Kleerebezem M, (2012) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10: 66-78.
5. Ma D, Forsythe P, Bienenstock J, (2004) Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun 72: 5308-5314.
6. Gobbetti M, Cagno RD, De Angelis M, (2010) Functional microorganisms for functional food quality. Crit Rev Food Sci Nutr 50: 716-727.
7. Corcoran BM, Stanton C, Fitzgerald G, Ross RP, (2008) Life under stress: The probiotic stress response and how it may be manipulated. Current Pharmaceutical Design 14: 1382-1399.
8. van Bokhorst-van de Veen H, Bron PA, Wels M, Kleerebezem M, (2011) Engineering robust lactic acid bacteria. In: Tsakalidou E, Papadimitriou K, editors. pp. 369-394 editors. Stress Responses of Lactic Acid Bacteria: Springer US.
9. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, et al. (2002) Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82: 187-216.
10. Watson D, Sleator RD, Hill C, Gahan CG, (2008) Enhancing bile tolerance improves survival and persistence of Bifidobacterium and Lactococcus in the murine gastrointestinal tract. BMC Microbiol 8: 176.
11. Begley M, Gahan CG, Hill C, (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29: 625-651.
12. Weckx S, Van der Meulen R, Allemeersch J, Huys G, Vandamme P, et al. (2010) Community dynamics of bacteria in sourdough fermentations as revealed by their metatranscriptome. Appl Environ Microbiol 76: 5402-5408.
13. Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HT, et al. (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12: 758-773.
14. Ahrne S, Nobaek S, Jeppsson B, Adlerberth I, Wold AE, et al. (1998) The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 85: 88-94.
15. Vesa T, Pochart P, Marteau P, (2000) Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract. Aliment Pharmacol Ther 14: 823-828.
16. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100: 1990-1995.
17. Teusink B, Wiersma A, Molenaar D, Francke C, de Vos WM, et al. (2006) Analysis of growth of Lactobacillus plantarum WCFS1 on a complex medium using a genome-scale metabolic model. J Biol Chem 281: 40041-40048.
18. Teusink B, van Enckevort FH, Francke C, Wiersma A, Wegkamp A, et al. (2005) In silico reconstruction of the metabolic pathways of Lactobacillus plantarum: comparing predictions of nutrient requirements with those from growth experiments. Appl Environ Microbiol 71: 7253-7262.
19. Lambert JM, Bongers RS, Kleerebezem M, (2007) Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl Environ Microbiol 73: 1126-1135.
20. Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, et al. (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187: 6119-6127.
21. Pretzer G, Snel J, Molenaar D, Wiersma A, Bron PA, et al. (2005) Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J Bacteriol 187: 6128-6136.
22. Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, et al. (2010) Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS ONE 5: e10632.
23. van Hemert S, Meijerink M, Molenaar D, Bron PA, de Vos P, et al. (2010) Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol 10: 293.
24. Wegkamp A, de Vos WM, Smid EJ, (2009) Folate overproduction in Lactobacillus plantarum WCFS1 causes methotrexate resistance. FEMS Microbiol Lett 297: 261-265.
25. Wegkamp A, (2008) Modulation of folate production in lactic acid bacteria. Wageningen: Wageningen University, The Netherlands.
26. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C, (2004) Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J Appl Microbiol 96: 1024-1039.
27. Marteau P, Minekus M, Havenaar R, Veld J, (1997) Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: Validation and the effects of bile. Journal of Dairy Science 80: 1031-1037.
28. Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Moller PL, Michaelsen KF, et al. (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65: 4949-4956.
29. Matto J, Malinen E, Suihko ML, Alander M, Palva A, et al. (2004) Genetic heterogeneity and functional properties of intestinal bifidobacteria. J Appl Microbiol 97: 459-470.
30. Succi M, Tremonte P, Reale A, Sorrentino E, Grazia L, et al. (2005) Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS Microbiol Lett 244: 129-137.
31. Georgieva RN, Iliev IN, Chipeva VA, Dimitonova SP, Samelis J, et al. (2008) Identification and in vitro characterisation of Lactobacillus plantarum strains from artisanal Bulgarian white brined cheeses. J Basic Microbiol 48: 234-244.
32. 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.
33. 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.
34. Jordan S, Hutchings MI, Mascher T, (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32: 107-146.
35. Bron PA, Marco M, Hoffer SM, Van Mullekom E, de Vos WM, et al. (2004) 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.
36. Ingham CJ, Beerthuyzen M, van Hylckama Vlieg J, (2008) Population heterogeneity of Lactobacillus plantarum WCFS1 microcolonies in response to and recovery from acid stress. Appl Environ Microbiol 74: 7750-7758.
37. Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL, (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61: 393-410.
38. Lebeer S, Claes IJ, Verhoeven TL, Vanderleyden J, De Keersmaecker SC, (2011) Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb Biotechnol 4: 368-374.
39. Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR, Prouty AM, Brodsky IE, et al. (2007) Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J Bacteriol 189: 4624-4634.
40. Wall T, Bath K, Britton RA, Jonsson H, Versalovic J, et al. (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.
41. 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.
42. 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.
43. Govers MJ, Termont DS, Van Aken GA, Van der Meer R, (1994) Characterization of the adsorption of conjugated and unconjugated bile acids to insoluble, amorphous calcium phosphate. J Lipid Res 35: 741-748.
44. Sieuwerts S, de Bok FAM, Mols E, de Vos WM, Vlieg J, (2008) A simple and fast method for determining colony forming units. Letters in Applied Microbiology 47: 275-278.
45. Breiman L, (2001) Random forests. Machine Learning 45: 5-32.
46. van Bokhorst-van de Veen H, Abee T, Tempelaars M, Bron PA, Kleerebezem M, et al. (2011) Short- and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl Environ Microbiol 77: 5247-5256.
47. Horton RM, Cai ZL, Ho SN, Pease LR, (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
48. Sorvig E, Mathiesen G, Naterstad K, Eijsink VG, Axelsson L, (2005) High-level, inducible gene expression in Lactobacillus sakei and Lactobacillus plantarum using versatile expression vectors. Microbiology 151: 2439-2449.
49. 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.
50. Eijsink VG, Brurberg MB, Middelhoven PH, Nes IF, (1996) Induction of bacteriocin production in Lactobacillus sake by a secreted peptide. J Bacteriol 178: 2232-2237.
51. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
52. Maere S, Heymans K, Kuiper M, (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
53. Looijesteijn PJ, Hugenholtz J, (1999) Uncoupling of growth and exopolysaccharide production by Lactococcus lactis subsp. cremoris NIZO B40 and optimization of its synthesis. J Biosci Bioeng 88: 178-182.
54. Zhou M, Boekhorst J, Francke C, Siezen RJ, (2008) LocateP: genome-scale subcellular-location predictor for bacterial proteins. BMC Bioinformatics 9: 173.
55. Casadaban MJ, Cohen SN, (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179-207.