Skip to main content
SpringerLink
Log in

Anti-stress activity of Propionibacterium freudenreichii: identification of a reactivative protein

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Propionibacterium freudenreichii subsp. shermanii is known to prevent mutations caused by various agents such as N-methyl-N′-nitro-N-nitrosoguanidine, 9-aminoacridine, 4-nitro-quinoline-1-oxide and by UV radiation in both prokaryotic and eukaryotic cells. It was also shown to prevent or repair damage caused by H2O2 or UV radiation in Salmonella typhimurium and Escherichia coli, a characteristic previously designated as reactivative effect. In order to characterise this effect at the molecular level, we have purified the active component from a P. freudenreichii cell-free extract using a combination of ammonium sulfate precipitation, anion-exchange and size-exclusion chromatography. The isolated 35 kDa protein was then identified using both N-terminal and internal peptide sequencing as a cysteine synthase. The latter was localised in the P. freudenreichii proteomic map. It is constitutively expressed but also clearly induced during adaptation to detergent and heat, but not acid, stresses. The biological meaning of cysteine synthase in the context of adaptation to oxidative and non-oxidative stresses is discussed.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agerholm-Larsen L., Raben A., Haulrik N., Hansen A.S., Manders M. and Astrup A. 2000a. Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur. J. Clin. Nutr. 54: 288-297.

    Google Scholar 

  • Agerholm-Larsen L., Bell M.L., Grunwald G.K. and Astrup A. 2000b. The effect of a probiotic milk product on plasma choles-terol: a meta-analysis of short-term intervention studies. Eur. J. Clin. Nutr. 54: 856-860.

    Google Scholar 

  • Antelmann H., Bernhardt J., Schmid R., Mach H., Volker U. and Hecker M. 1997. First steps from a two-dimensional protein index towards a response-regulation map for Bacillus subtilis. Electrophoresis 18: 1451-1463.

    Google Scholar 

  • Benov L., Kredich N.M. and Fridovich I. 1996. The mechanism of the auxotrophy for sulfur-containing amino acids imposed upon Escherichia coli by superoxide. J. Biol. Chem. 271: 21037-21040.

    Google Scholar 

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

    Google Scholar 

  • Bougle D., Roland N., Lebeurrier F. and Arhan P. 1999. Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects. Scand. J. Gastroenterol. 34: 144-148.

    Google Scholar 

  • Coulter E.D. and Kurtz D.M.J. 2001. A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reduc-tase. Arch. Biochem. Biophys. 394: 76-86.

    Google Scholar 

  • Das A., Coulter E.D., Kurtz D.M.J. and Ljungdahl L.G. 2001. Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidoreductase-rub-redoxin and rubrerythrin-type A flavoprotein-high-molecular-weight rubredoxin. J. Bacteriol. 183: 1560-1567.

    Google Scholar 

  • Duche O., Tremoulet F., Glaser P. and Labadie J. 2002. Salt stress proteins induced in Listeria monocytogenes. Appl. Environ. Microbiol. 68: 1491-1498.

    Google Scholar 

  • Gent-Ruijters M.L., Meijere F.A., Vries W. and Stouthamer A.H. 1976. Lactate metabolism in Propionibacterium pentosaceum growing with nitrate or oxygen as hydrogen acceptor. Antonie van Leeuwenhoek. 42: 217-228.

    Google Scholar 

  • Grant C.M., MacIver F.H. and Dawes I.W. 1996. Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 29: 511-515.

    Google Scholar 

  • Graumann P., Schroder K., Schmid R. and Marahiel M.A. 1996. Cold shock stress-induced proteins in Bacillus subtilis. J. Bac-teriol. 178: 4611-4619.

    Google Scholar 

  • Guandalini S., Pensabene L., Zikri M.A., Dias J.A., Casali L.G., Hoekstra H., Kolacek S., Massar K., Micetic-Turk D., Papadopoulou A., de Sousa J.S., Sandhu B., Szajewska H. and Weizman Z. 2000. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J. Pediatr. Gastroenterol. Nutr. 30: 54-60.

    Google Scholar 

  • Hartke A., Frere J., Boutibonnes P. and 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.

    Google Scholar 

  • Henzel W.J., Billeci T.M., Stults J.T., Wong S.C., Grimley C. and Watanabe C. 1993. Identifying proteins from two-dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. Proc. Natl. Acad. Sci. USA 90: 5011-5015.

    Google Scholar 

  • Isenberg J., Stoffel B., Wolters U., Beuth J., Stutzer H., Ko H.L. and Pichlmaier H. 1995. Immunostimulation by propionibacteria: effects on immune status and antineoplastic treatment. Anti-cancer Res. 15: 2363-2368.

    Google Scholar 

  • Jan G., Belzacq A.S., Haouzi D., Rouault A., Metivier D., Kroemer G. and Brenner C. 2002. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ. 9: 179-188.

    Google Scholar 

  • Jan G., Leverrier P. and Roland N. 2001a. Survival and beneficial effects of propionibacteria in the human gut: in vivo and in vitro investigations. Lait 82: 131-144.

    Google Scholar 

  • Jan G., Leverrier P., Pichereau V. and Boyaval P. 2001b. Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii. Appl. Environ. Microbiol. 67: 2029-2036.

    Google Scholar 

  • Kellam P., Dallas W.S., Ballantine S.P. and Delves C.J. 1995. Functional cloning of the dihydropteroate synthase gene of Staphylococcus haemolyticus. FEMS Microbiol. Lett. 134: 165-169.

    Google Scholar 

  • Ketterer B. 1988. Protective role of glutathione and glutathione transferases in mutagenesis and carcinogenesis. Mutat. Res. 202: 343-361.

    Google Scholar 

  • Kim J.A., Sha Z. and Mayfield J.E. 2000. Regulation of Brucella abortus catalase. Infect. Immun. 68: 3861-3866.

    Google Scholar 

  • Krapp A.R., Rodriguez R.E., Poli H.O., Paladini D.H., Palatnik J.F. and Carrillo N. 2002. The flavoenzyme ferredoxin (flavodoxin)-NADP(H) reductase modulates NADP(H) homeostasis during the soxRS response of Escherichia coli. J. Bacteriol. 184: 1474-1480.

    Google Scholar 

  • Kullisaar T., Zilmer M., Mikelsaar M., Vihalemm T., Annuk H., Kairane C. and Kilk A. 2002. Two antioxidative lactobacilli strains as promising probiotics. Int. J. Food Microbiol. 72: 215-224.

    Google Scholar 

  • Kurth J. and Stoffel W. 1990. A facile method for the isolation and preparation of proteins and peptides for sequence analysis in the picomolar range. Biol. Chem. Hoppe Seyler 371: 675-685.

    Google Scholar 

  • Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.

    Google Scholar 

  • Lee S., Reth A., Meletzus D., Sevilla M. and Kennedy C. 2000. Characterization of a major cluster of nif, fix, and associated genes in a sugarcane endophyte, Acetobacter diazotrophicus. J. Bacteriol. 182: 7088-7091.

    Google Scholar 

  • Lombard M., Houee-Levin C., Touati D., Fontecave M. and Niviere V. 2001. Superoxide reductase from Desulfoarculus baarsii: reaction mechanism and role of glutamate 47 and lysine 48 in catalysis. Biochemistry 40: 5032-5040.

    Google Scholar 

  • Lyon W.J. and Glatz B.A. 1993. Isolation and purification of propionicin PLG-1, a bacteriocin produced by a strain of Prop-ionibacterium thoenii. Appl. Environ. Microbiol. 59: 83-88.

    Google Scholar 

  • Mori H., Sato Y., Taketomo N., Kamiyama T., Yoshiyama Y., Meguro S., Sato H. and Kaneko T. 1997. Isolation and structural identification of bifidogenic growth stimulator produced by Propionibacterium freudenreichii. J. Dairy Sci. 80: 1959-1964.

    Google Scholar 

  • Nielsen P.A. 1983. Role of reduced sulfur compounds in nutrition of Propionibacterium acnes. J. Clin. Microbiol. 17: 276-279.

    Google Scholar 

  • Noji M., Saito M., Nakamura M., Aono M., Saji H. and Saito K. 2001. Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol. 126: 973-980.

    Google Scholar 

  • Nystrom T. 1999. Starvation, cessation of growth and bacterial aging. Curr. Opin. Microbiol. 2: 214-219.

    Google Scholar 

  • Ogasawara N., Nakai S. and Yoshikawa H. 1994. Systematic sequencing of the 180 kilobase region of the Bacillus subtilis chromosome containing the replication origin. DNA Res. 1: 1-14.

    Google Scholar 

  • PearsonW.R. and Lipman D.J. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85: 2444-2448.

    Google Scholar 

  • Pool-Zobel B.L., Munzner R. and Holzapfel W.H. 1993. An-tigenotoxic properties of lactic acid bacteria in the Salmonella Protectyphimurium mutagenicity assay. Nutr. Cancer 20: 261-270.

    Google Scholar 

  • Rhee C.H. and Park H.D. 2001. Three glycoproteins with an-timutagenic activity identified in Lactobacillus plantarum KLAB21. Appl. Environ. Microbiol. 67: 3445-3449.

    Google Scholar 

  • Rizkalla S.W., Luo J., Kabir M., Chevalier A., Pacher N. and Slama G. 2000. Chronic consumption of fresh but not heated yogurt improves breath-hydrogen status and short-chain fatty acid profiles: a controlled study in healthy men with or without lactose maldigestion. Am. J. Clin. Nutr. 72: 1474-1479.

    Google Scholar 

  • Schwab C.E., Huber W.W., Parzefall W., Hietsch G., Kassie F., Schulte-Hermann R. and Knasmuller S. 2000. Search for com-pounds that inhibit the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Crit. Rev. Toxicol. 30: 1-69.

    Google Scholar 

  • Sheih Y.H., Chiang B.L., Wang L.H., Liao C.K. and Gill H.S. 2001. Systemic immunity-enhancing effects in healthy subjects fol lowing dietary consumption of the lactic acid bacterium Lac-tobacillus rhamnosus HN001. J. Am. Coll. Nutr. 20: 149-156.

    Google Scholar 

  • Thompson D.K., Beliaev A.S., Giometti C.S., Tollaksen S.L., Khare T., Lies D.P., Nealson K.H., Lim H., Yates J., Brandt C.C., Tiedje J.M. and Zhou J. 2002. Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl. Environ. Microbiol. 68: 881-892.

    Google Scholar 

  • Vorobjeva L. 2000. Physiological peculiarities of propionibacteria-present facts and prospective applications. Sci. Prog. 83: 277-301.

    Google Scholar 

  • Vorobjeva L.I., Cherdinceva T.A., Abilev S.K. and Vorobjeva N.V. 1991. Antimutagenicity of propionic acid bacteria. Mutat. Res. 251: 233-239.

    Google Scholar 

  • Vorobjeva L.I., Iljasova O.V., Khodjaev E., Ponomareva G.M. and Varioukhina S. 2001. Inhibition of induced mutagenesis in Salmonella typhimurium by the protein of Propionibacterium freudenreichii subsp. shermanii. Anaerobe 7: 37-44.

    Google Scholar 

  • Vorobjeva L.I., Khodjaev E. and Cherdinceva T.A. 1996. The study of induced antimutagenisis of propionic acid bacteria. J. Microbiol. Meth. 24: 249-258.

    Google Scholar 

  • Vorobjeva L.I., Nikitenko G.V., Khodzhaev E.I. and Ponomareva G.M. 1993. Reactivation of Escherichia coli inactivated by ultraviolet light by cell extracts of propionic acid bacteria. Mikrobiologiia 62: 1135-1143.

    Google Scholar 

  • Vuilleumier S. and Pagni M. 2002. The elusive roles of bacterial glutathione S-transferases: new lessons from genomes. Appl. Microbiol. Biotechnol. 58: 138-146.

    Google Scholar 

  • Wiencke J.K., Pemble S., Ketterer B. and Kelsey K.T. 1995. Gene deletion of glutathione S-transferase theta: correlation with induced genetic damage and potential role in endogenous muta-genesis. Cancer Epidemiol. Biomarkers 4: 253-259.

    Google Scholar 

  • Wollowski I., Rechkemmer G. and Pool-Zobel B.L. 2001. Protec tive role of probiotics and prebiotics in colon cancer. Am. J. Clin. Nutr. 73: 451S-455S.

    Google Scholar 

  • Zarate G., Chaia A.P., Gonzalez S. and Oliver G. 2000. Viability and beta-galactosidase activity of dairy propionibacteria subject-ed to digestion by artificial gastric and intestinal fluids. J. Food Prot. 63: 1214-1221.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Moscow State University, 119899, Moscow, Russia

    Lena Vorobjeva, Evgeni Khodjaev, Svetlana Varioukhina & Galina Ponomareva

  2. Laboratoire de Recherches de Technologie Laitière, Institut National de la Recherche Agronomique, 65 rue de St Brieuc, 35042, Rennes Cedex, France

    Pauline Leverrier, Patrick Boyaval & Gwénaël Jan

  3. Standa Industrie, 68 rue R. Kaskoreff, 14050, Caen Cedex 4, France

    Pauline Leverrier

  4. Institute of Bioorganic Chemistry, 117997 GSP, Moscow V-437, Russia

    Aleksei Zinchenko & Elena Gordeeva

Authors
  1. Lena Vorobjeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pauline Leverrier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aleksei Zinchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick Boyaval
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Evgeni Khodjaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Svetlana Varioukhina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Galina Ponomareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elena Gordeeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gwénaël Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vorobjeva, L., Leverrier, P., Zinchenko, A. et al. Anti-stress activity of Propionibacterium freudenreichii: identification of a reactivative protein. Antonie Van Leeuwenhoek 85, 53–62 (2004). https://doi.org/10.1023/B:ANTO.0000020276.18127.99

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:ANTO.0000020276.18127.99

Search

Navigation