1887

Abstract

is a facultatively anaerobic bacterium that can perform respiration under aerobic conditions in the presence of haem, with vitamin K acting as a source of menaquinone. We investigated growth performance and oxidative stress resistance of WCFS1 cultures grown in de Man, Rogosa and Sharpe (MRS) medium without and with added manganese under fermentative, aerobic, aerobic with haem, and respiratory conditions. Previous studies showed that WCFS1 lacks a superoxide dismutase and requires high levels of manganese for optimum fermentative and aerobic growth. In this study, respiratory growth with added manganese resulted in significantly higher cell densities compared to the other growth conditions, while without manganese added, similar but lower cell densities were reached. Notably, cells derived from the respiratory cultures showed the highest hydrogen peroxide resistance in all conditions tested, although similar activity levels of haem-dependent catalase were detected in cells grown under aerobic conditions with haem. These results indicate that oxidative stress resistance of is affected by respiratory growth, growth phase, haem and manganese. As levels of haem and manganese can differ considerably in the raw materials used in fermentation processes, including those of milk, meat and vegetables, the insight gained here may provide tools to increase the performance and robustness of starter bacteria.

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2012-01-01
2019-10-22
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References

  1. Abriouel H., Herrmann A., Stärke J., Yousif N. M., Wijaya A., Tauscher B., Holzapfel W., Franz C. M.. ( 2004;). Cloning and heterologous expression of hematin-dependent catalase produced by Lactobacillus plantarum CNRZ 1228. . Appl Environ Microbiol 70:, 603–606. [CrossRef][PubMed]
    [Google Scholar]
  2. Archibald F. S., Duong M. N.. ( 1984;). Manganese acquisition by Lactobacillus plantarum. . J Bacteriol 158:, 1–8.[PubMed]
    [Google Scholar]
  3. Archibald F. S., Fridovich I.. ( 1981;). Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. . J Bacteriol 145:, 442–451.[PubMed]
    [Google Scholar]
  4. Brooijmans R., Smit B., Santos F., van Riel J., de Vos W. M., Hugenholtz J.. ( 2009a;). Heme and menaquinone induced electron transport in lactic acid bacteria. . Microb Cell Fact 8:, 28. [CrossRef][PubMed]
    [Google Scholar]
  5. Brooijmans R. J., de Vos W. M., Hugenholtz J.. ( 2009b;). Lactobacillus plantarum WCFS1 electron transport chains. . Appl Environ Microbiol 75:, 3580–3585. [CrossRef][PubMed]
    [Google Scholar]
  6. Chapman H. D.. ( 1966;). In Diagnostic Criteria for Plants and Soils, pp. 484–499. Edited by Chapman H. D... Riverside, CA:: Calfornia University Division of Agricultural Science;.
    [Google Scholar]
  7. Delwiche E. A.. ( 1961;). Catalase of Pedicoccus cerevisiae. . J Bacteriol 81:, 416–418.[PubMed]
    [Google Scholar]
  8. de Man J. C., Rogosa M., Sharpe M. E.. ( 1960;). A medium for the cultivation of lactobacilli. . J Appl Microbiol 23:, 130–135.
    [Google Scholar]
  9. den Besten H. M., Mols M., Moezelaar R., Zwietering M. H., Abee T.. ( 2009;). Phenotypic and transcriptomic analyses of mildly and severely salt-stressed Bacillus cereus ATCC 14579 cells. . Appl Environ Microbiol 75:, 4111–4119. [CrossRef][PubMed]
    [Google Scholar]
  10. 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. [CrossRef][PubMed]
    [Google Scholar]
  11. Elkins C. A., Mullis L. B.. ( 2004;). Bile-mediated aminoglycoside sensitivity in Lactobacillus species likely results from increased membrane permeability attributable to cholic acid. . Appl Environ Microbiol 70:, 7200–7209. [CrossRef][PubMed]
    [Google Scholar]
  12. FAO/WHO ( 2001;). Guidelines for the evaluation of probiotics in food. . http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf
  13. 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. [CrossRef][PubMed]
    [Google Scholar]
  14. Fuller R.. ( 1989;). Probiotics in man and animals. . J Appl Bacteriol 66:, 365–378. [CrossRef][PubMed]
    [Google Scholar]
  15. Gaudu P., Vido K., Cesselin B., Kulakauskas S., Tremblay J., Rezaïki L., Lamberet G., Sourice S., Duwat P., Gruss A.. ( 2002;). Respiration capacity and consequences in Lactococcus lactis. . Antonie van Leeuwenhoek 82:, 263–269. [CrossRef][PubMed]
    [Google Scholar]
  16. González-Flecha B., Demple B.. ( 1995;). Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. . J Biol Chem 270:, 13681–13687. [CrossRef][PubMed]
    [Google Scholar]
  17. Groot M. N., Klaassens E., de Vos W. M., Delcour J., Hols P., Kleerebezem M.. ( 2005;). Genome-based in silico detection of putative manganese transport systems in Lactobacillus plantarum and their genetic analysis. . Microbiology 151:, 1229–1238. [CrossRef][PubMed]
    [Google Scholar]
  18. Imlay J. A., Fridovich I.. ( 1991;). Superoxide production by respiring membranes of Escherichia coli. . Free Radic Res Commun 12:, 59–66. [CrossRef][PubMed]
    [Google Scholar]
  19. Imlay J. A., Linn S.. ( 1988;). DNA damage and oxygen radical toxicity. . Science 240:, 1302–1309. [CrossRef][PubMed]
    [Google Scholar]
  20. Ingham C. J., 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. [CrossRef][PubMed]
    [Google Scholar]
  21. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O. P., Leer R., Tarchini R., Peters S. A., Sandbrink H. M.. & other authors ( 2003;). Complete genome sequence of Lactobacillus plantarum WCFS1. . Proc Natl Acad Sci U S A 100:, 1990–1995. [CrossRef][PubMed]
    [Google Scholar]
  22. Knauf H. J., Vogel R. F., Hammes W. P.. ( 1992;). Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sake LTH677. . Appl Environ Microbiol 58:, 832–839.[PubMed]
    [Google Scholar]
  23. Kohanski M. A., Dwyer D. J., Hayete B., Lawrence C. A., Collins J. J.. ( 2007;). A common mechanism of cellular death induced by bactericidal antibiotics. . Cell 130:, 797–810. [CrossRef][PubMed]
    [Google Scholar]
  24. Kono Y., Fridovich I.. ( 1983a;). Functional significance of manganese catalase in Lactobacillus plantarum. . J Bacteriol 155:, 742–746.[PubMed]
    [Google Scholar]
  25. Kono Y., Fridovich I.. ( 1983b;). Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. . J Biol Chem 258:, 6015–6019.[PubMed]
    [Google Scholar]
  26. Labanauskas C. K.. ( 1966;). In Diagnostic Criteria for Plants and Soils, pp. 264–285. Edited by Chapman H. D... Riverside, CA:: Calfornia University Division of Agricultural Science;.
    [Google Scholar]
  27. Marco M. L., Bongers R. S., de Vos W. M., Kleerebezem M.. ( 2007;). Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. . Appl Environ Microbiol 73:, 124–132. [CrossRef][PubMed]
    [Google Scholar]
  28. Meijerink M., van Hemert S., Taverne N., Wels M., de Vos P., Bron P. A., Savelkoul H. F., van Bilsen J., Kleerebezem M., Wells J. M.. ( 2010;). Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. . PLoS ONE 5:, e10632. [CrossRef]
    [Google Scholar]
  29. Mille Y., Beney L., Gervais P.. ( 2005;). Compared tolerance to osmotic stress in various microorganisms: towards a survival prediction test. . Biotechnol Bioeng 92:, 479–484. [CrossRef][PubMed]
    [Google Scholar]
  30. Murphy M. G., Condon S.. ( 1984;). Correlation of oxygen utilization and hydrogen peroxide accumulation with oxygen induced enzymes in Lactobacillus plantarum cultures. . Arch Microbiol 138:, 44–48. [CrossRef][PubMed]
    [Google Scholar]
  31. Reuther W., Labanauskas C. K.. ( 1966;). In Diagnostic Criteria for Plants and Soils, pp. 157–175. Edited by Chapman H. D... Riverside, CA:: Calfornia University Division of Agricultural Science;.
    [Google Scholar]
  32. Rezaïki L., Cesselin B., Yamamoto Y., Vido K., van West E., Gaudu P., Gruss A.. ( 2004;). Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. . Mol Microbiol 53:, 1331–1342. [CrossRef]
    [Google Scholar]
  33. Serrano L. M., Molenaar D., Wels M., Teusink B., Bron P. A., de Vos W. M., Smid E. J.. ( 2007;). Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. . Microb Cell Fact 6:, 29. [CrossRef][PubMed]
    [Google Scholar]
  34. Stevens M. J., Molenaar D., de Jong A., de Vos W. M., Kleerebezem M.. ( 2010;). Involvement of the mannose phosphotransferase system of Lactobacillus plantarum WCFS1 in peroxide stress tolerance. . Appl Environ Microbiol 76:, 3748–3752. [CrossRef]
    [Google Scholar]
  35. van de Guchte M., Serror P., Chervaux C., Smokvina T., Ehrlich S. D., Maguin E.. ( 2002;). Stress responses in lactic acid bacteria. . Antonie van Leeuwenhoek 82:, 187–216. [CrossRef]
    [Google Scholar]
  36. Vaughan E. E., Heilig H. G., Ben-Amor K., de Vos W. M.. ( 2005;). Diversity, vitality and activities of intestinal lactic acid bacteria and bifidobacteria assessed by molecular approaches. . FEMS Microbiol Rev 29:, 477–490. [CrossRef][PubMed]
    [Google Scholar]
  37. 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. [CrossRef]
    [Google Scholar]
  38. Wang D., Du X., Zheng W.. ( 2008;). Alteration of saliva and serum concentrations of manganese, copper, zinc, cadmium and lead among career welders. . Toxicol Lett 176:, 40–47. [CrossRef]
    [Google Scholar]
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