Genome-wide transcriptomic responses of a human isolate of Lactobacillus plantarum exposed to p-coumaric acid stress

Molecular Nutrition and Food Research

Volumn 56, Issue 12, 2012, Pages 1848-1859

  Reverón, Inés ^a   de las Rivas, Blanca ^a   Muñoz, Rosario ^a   López de Felipe, Félix ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

Author keywords

Lactobacillus plantarum; Oxidative response; p Coumaric acid; Probiotics; Transcriptomics

Indexed keywords

4-COUMARIC ACID; BACTERIAL RNA; COUMARIC ACID; NITROGEN; PARA COUMARIC ACID; PROBIOTIC AGENT; TRANSCRIPTOME;

ADAPTATION; ARTICLE; BACTERIAL GENOME; DRUG EFFECT; GASTROINTESTINAL TRACT; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LACTOBACILLUS PLANTARUM; METABOLISM; MICROARRAY ANALYSIS; MICROBIOLOGY; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION;

ADAPTATION, PHYSIOLOGICAL; COUMARIC ACIDS; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; LACTOBACILLUS PLANTARUM; MICROARRAY ANALYSIS; NITROGEN; OXIDATIVE STRESS; PROBIOTICS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, BACTERIAL; TRANSCRIPTOME;

LACTOBACILLUS PLANTARUM;

EID: 84870689572     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200384     Document Type: Article

References (63)

1. Clifford, M. N., Chlorogenic acids and other cinnamates - nature, occurrence, dietary burden, absorption and metabolism. J. Sci. Food Agric. 2000, 80, 1033-1043.
2. Guglielmi, F., Luceri, C., Giovannelli, L., Dolara, P. et al., Effect of 4-coumaric and 3, 4-dihydroxybenzoic acid on oxidative DNA damage in rat colonic mucosa. Br. J. Nutr. 2003, 89, 581-587.
3. Luceri, C., Guglielmi, F., Lodovici, M., Giannini, L. et al., Plant phenolic 4-coumaric acid protects against intestinal inflammation in rats. Scand. J. Gastroenterol. 2004, 39, 1128-1133.
4. Ferguson, L. R., Shuo-Tun, Z., Harris, P. J., Antioxidant and antigenotoxic effects of plant cell wall hydroxycinnamic acids in cultured HT-29. Mol. Nutr. Food Res. 2005, 49, 585-693.
5. Rechner, A. R., Kuhnle, G., Bremner, P., Hubbard, G. P. et al., The metabolic fate of dietary polyphenols in humans. Free Rad. Biol. Med. 2002, 33, 220-235.
6. van Duynhovena, J., Vaughan, E. E., Jacobsa, D., Kempermana, R. et al., Metabolic fate of polyphenols in the human superorganism. Proc. Natl. Acad. Sci. USA 2011, 108, 4531-4538.
7. Dolara, P., Luceri, C., De Filippo, C., Femia, A. P. et al., Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats. Mutat. Res. 2005, 591, 237-246.
8. Lou, Z., Wang, H., Rao, S., Sun, J. et al., p-Coumaric acid kills bacteria through dual damage mechanisms. Food Control 2012, 25, 550-554.
9. Hervert-Hernandez, D., Goñi, I., Dietary polyphenols and human gut microbiota: a review. Food Rev. Int. 2011, 27, 154-169.
10. Ahrne, S., Nobaek, S., Jeppsson, B., Adlerberth, I. et al., The normal Lactobacillus flora of healthy human rectal and oral mucosa. J. Appl. Microbiol. 1998, 85, 88-94.
11. Johansson, M. L., Molin, G., Jeppsson, B., Nobaek, S. et al., Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Appl. Environ. Microbiol. 1993, 59, 15-20.
12. de Vries, M. C., Vaughan, E. E., Kleerebezem, M., deVos, W. M., Lactobacillus plantarum-survival, functional and potential probiotic properties in human intestinal tract. Int. Dairy J. 2006, 16, 1018-1028.
13. Licandro-Seraut, H., Gury, J., Phuong Tran, N., Barthelmebs, L. et al., Kinetics and intensity of the expression of genes involved in the stress response tightly induced by phenolic acids in Lactobacillus plantarum. J. Mol. Microb. Biotechnol. 2008, 14, 41-47.
14. Gury, J., Barthelmebs, L., Tran, N. P., Diviès, C. et al., Cloning, deletion, and characterization of PadR, the transcriptional repressor of the phenolic acid decarboxylase-encoding padA gene of Lactobacillus plantarum. Appl. Environ. Microbiol. 2004, 70, 2146-2153.
15. Nguyen, T., Tran, N., Cavin, J. F., Genetic and biochemical analysis of PadR-padC promoter interactions during the phenolic acid stress response in Bacillus subtilis 168. J. Bacteriol. 2011, 193, 4180-4191.
16. Meijerink, M., van Hemert, S., Taverne, N., Wels, M. et al., Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One 2010, 5, e10632.
17. Bron, P. A., Grangette, C., Mercenier, A., de Vos, W. M. et al., Identification of Lactobacillus plantarum genes that are induced in the gastrointestinal tract of mice. J. Bacteriol. 2004, 186, 5721-5729.
18. de Man, J., Rogosa, M., Sharpe, M., A medium for the cultivation of lactobacilli. J. Appl. Microbiol. 1960, 23, 130-135.
19. Vesa, T., Pochart, P., Marteau, P., Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract. Aliment. Pharmacol. Ther. 2003, 14, 823-828.
20. Pavan, S., Desreumaux, P., Mercenier, A., Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin. Diagn. Lab. Inmunol. 2003, 10, 696-701.
21. Marchesi, J. R., Sato, T., Weghtman, A. J., Martin, T. A. et al., Design and evaluation of useful bacterium-specific DNA primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 1998, 84, 117-123.
22. Pfaffl, M. W., Tichopad, A., Prgomet, C., Neuvians, T. P., Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol. Lett. 2004, 26, 509-515.
23. Smyth, G. K., Speed, T., Normalization of cDNA microarray data. Methods 2003, 31, 265-273.
24. Edgar, R., Domrachev, M., Lash, A. E., Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30, 207-210.
25. Münch, R., Hiller, K., Grote, A., Scheer, M. et al., Virtual footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 2005, 21, 4187-4189.
26. Beier, L., Nygaard, P., Jarmer, H., Saxild, H., Transcription analysis of the Bacillus subtilis PucR regulon and identification of a cis-acting sequence required for PucR-regulated expression of genes involved in purine catabolism. J. Bacteriol. 2002, 184, 3232-3241.
27. Miller, B., Franz, Ch., Cho, G., du Toit, M., Expression of the malolactic enzyme gene (mle) from Lactobacillus plantarum under winemaking conditions. Curr. Microbiol. 2011, 62, 682-1688.
28. Zhou, M., Boekhorst, J., Francke, Ch., Siezen, R., LocateP: genome-scale subcellular-location predictor for bacterial proteins. BMC Bioinformatics, 2008, 9, 173.
29. de Vries, M. C., Analyzing Global Gene Expression of Lactobacillus plantarum in the Human Gastrointestinal Tract. PhD Thesis, Wageningen University, Wageningen, The Netherlands 2006, 147 pp.
30. Deghorain, M., Goffin, P., Fontaine, L., Mainardi, J. L. et al., Selectivity for d-lactate incorporation into the peptidoglycan precursors of Lactobacillus plantarum: role of Aad, a VanX-like d-alanyl-d-alanine dipeptidase. J. Bacteriol. 2007, 189, 4332-4337.
31. Mainardi, J. L., Villet, R., Bugg, T. D., Mayer, C., Evolution of peptidoglycan biosynthesis under the selective pressure of antibiotics in gram-positive bacteria. FEMS Microbiol. Rev. 2008, 32, 386-408.
32. Kleerebezem, M. J., Boekhorst, J., van Kranenburg, R., Molenaar, D. et al., Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. USA 2003, 100, 1990-1995.
33. Wels, M., Kormelink, T., Kleerebezem, M., Siezen, R. An in silico analysis of T-box regulated genes and T-box evolution in prokaryotes, with emphasis on prediction of substrate specificity of transporters. BMC Genomics 2008, 9, 330-346.
34. Serrano, L. M., Molenaar, D., Wels, M., Teusink, B. et al., Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microb. Cell Fact. 2007, 6, 29.
35. van Bokhorst-van de Veen, H., Abee, T., Tempelaars, M., Bron, P. et al., Short- and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl. Environ. Microbiol. 2011, 77, 5247-5256.
36. + antiporter, ShaA, is required for initiation of sporulation in Bacillus subtilis. J. Bacteriol. 2000, 182, 898-904.
37. Boekhorst, J., Wels, M., Kleerebezem, M., Siezen, R. J., The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 2006, 152, 3175-3183.
38. Fiocco, D., Capozzi, V., Collins, M., Gallone, A. et al., Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J. Bacteriol. 2010, 192, 896-900.
39. Fiocco, D., Collins, M., Muscariello, L., Hols, P. et al., The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. J. Bacteriol. 2009, 191, 1688-1694.
40. Wels, M., Overmars, L., Francke, Ch., Kleerebezem, M. et al., Reconstruction of the regulatory network of Lactobacillus plantarum WCFS1 on basis of correlated gene expression and conserved regulatory motifs. Microbial. Biotech. 2011, 4, 333-344.
41. Wels, M., Francke, Ch., Kerkhoven, R., Kleerebezem, M. et al., Predicting cis-acting elements of Lactobacillus plantarum by comparative genomics with different taxonomic subgroups. Nucleic Acids Res. 2006, 34, 1947-1958.
42. Sonenshein, A., Control of key metabolic intersections in Bacillus subtilis. Nat. Rev., 2007, 5, 917-927.
43. Fiocco, D., Capozzi, V., Goffin, P., Hols, P. et al., Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 2007, 77, 909-915.
44. Frees, D., Savijoki, K., Varmanen, P., Ingmer, H., Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, gram-positive bacteria. Mol. Microbiol. 2007, 63, 1285-1295.
45. Winkler, J., Kao, K. C., Transcriptional analysis of Lactobacillus brevis to N-butanol and ferulic acid stress responses. PLoS One 2011, 6, e21438.
46. Kvint, K., Nachin, L., Diez, A., Nystrom, T., The bacterial universal stress protein: function and regulation. Curr. Opin. Microbiol. 2003, 6, 140-145.
47. Duong, T., Barrangou, R., Russell, W. M., Klaenhammer, T. R., Characterisation of the tre locus and analysis of trehalose cryoprotection in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 2006, 72, 1218-1225.
48. Thompson, J., Thomas, T., Phosphoenolpyruvate and 2-phosphoglycerate: endogenous energy source(s) for sugar accumulation by starved cells of Streptococcus lactis. J. Bacteriol. 1977, 130, 583-595.
49. Curiel, J., Rodríguez, H., de las Rivas, B., Anglade, P. et al., Response of a Lactobacillus plantarum human isolate to tannic acid challenge assessed by proteomic analyses. Mol. Nutr. Food Res. 2011, 55, 1454-1465.
50. ATP and maintenance energy as biologically interpretable phenomena. Annu. Rev. Microbiol. 1984, 38, 459-486.
51. Poolman, B., Molenaar, D., Smid, E. J., Ubbink, T. et al., Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J. Bacteriol. 1991, 173, 6030-6037.
52. Canales, J., Flores-Monterrosso, A., Rueda-López, M., Avila, C. et al., Identification of genes regulated by ammonium availability in the roots of maritime pine trees. Amino Acids, 2010, 39, 991-1001.
53. Kolling, R., Lother, H., AsnC an autogenously regulated activator of asparagine synthetase A transcription in Escherichia coli. J. Bacteriol. 1985, 164, 310-315.
54. Rozès, N., Peres, C., Effects of phenolic compounds on the growth and the fatty acid composition of Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 1998, 49, 108-111.
55. Simić, A., Manojlović, D., Segan, D., Todorović, M., Electrochemical behavior and antioxidant and prooxidant activity of natural phenolics. Molecules 2007, 12, 2327-2340.
56. Luo, S., Levine, R. L., Methionine in proteins defends against oxidative stress. FASEB J. 2009, 23, 464-72.
57. Huycke, M. M., Moore, D., Joyce, W., Wise, P. et al., Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol. 2001, 42, 729-740.
58. Soballe, B., Poole, R. K., Ubiquinone limits oxidative stress in Escherichia coli. Microbiology 2000, 146, 787-796.
59. Marco, M. L., Peters, T. H., Bongers, R. S., Molenaar, D. et al., Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ. Microbiol. 2009, 11, 2747-2757.
60. Walter, J., Chagnaud, P., Tannock, G. W., Loach, D. M. et al., A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl. Environ. Microbiol. 2005, 71, 979-986.
61. Monnet, V., Bacterial oligopeptide-binding proteins. Cell. Mol. Life Sci. 2003, 60, 2100-2114.
62. Espinosa-Urgel, M., Salido, A., Ramos, J. L., Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 2000, 182, 2363-2369.
63. Li, Z. H., Qiang Wang, Q., Ruan, X., De Pan, C. et al., Phenolics and plant allelopathy. Molecules 2010, 15, 8933-8952.