1887

Abstract

Lactic acid bacteria have a variety of mechanisms for tolerance to oxygen and reactive oxygen species, and these mechanisms differ among species. Lactobacillus casei strain Shirota grows well under aerobic conditions, indicating that the various systems involved in oxidative stress resistance function in this strain. To elucidate the mechanism of oxidative stress resistance in L. casei strain Shirota, we examined the transcriptome response to oxygen or hydrogen peroxide exposure. We then focused on an uncharacterized gene that was found to be up-regulated by both oxygen and hydrogen peroxide stress; we named the gene hprA1 (hydrogen peroxide resistance gene). This gene is widely distributed among lactobacilli. We investigated the involvement of this gene in oxidative stress resistance, as well as the mechanism of tolerance to hydrogen peroxide. Growth of L. casei MS105, an hprA1-disrupted mutant, was not affected by oxygen stress, whereas the survival rate of MS105 after hydrogen peroxide treatment was markedly reduced compared to that of the wild-type. However, the activity of MS105 in eliminating hydrogen peroxide was similar to that of the wild-type. We cloned hprA1 from L. caseiShirota and purified recombinant HprA1 protein from Escherichia coli. We demonstrated that the recombinant HprA1 protein bound to iron and prevented the formation of a hydroxyl radical in vitro. Thus, HprA1 protein probably contributes to hydrogen peroxide tolerance in L. casei strain Shirota by binding to iron in the cells and preventing the formation of a hydroxyl radical.

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2016-11-23
2019-10-23
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References

  1. Ai L., Chen C., Zhou F., Wang L., Zhang H., Chen W., Guo B..( 2011;). Complete genome sequence of the probiotic strain Lactobacillus casei BD-II. . J Bacteriol 193: 3160–3161. [CrossRef] [PubMed]
    [Google Scholar]
  2. Asahara T., Nomoto K., Watanuki M., Yokokura T..( 2001;). Antimicrobial activity of intraurethrally administered probiotic Lactobacillus casei in a murine model of Escherichia coli urinary tract infection. . Antimicrob Agents Chemother 45: 1751–1760. [CrossRef] [PubMed]
    [Google Scholar]
  3. Broadbent J. R., Neeno-Eckwall E. C., Stahl B., Tandee K., Cai H., Morovic W., Horvath P., Heidenreich J., Perna N. T. et al.( 2012;). Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. . BMC Genomics 13: 533. [CrossRef] [PubMed]
    [Google Scholar]
  4. Cai H., Thompson R., Budinich M. F., Broadbent J. R., Steele J. L..( 2009;). Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. . Genome Biol Evol 1: 239–257. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chang S. K., Hassan H. M..( 1997;). Characterization of superoxide dismutase in Streptococcus thermophilus. . Appl Environ Microbiol 63: 3732–3735.[PubMed]
    [Google Scholar]
  6. Chen C., Ai L., Zhou F., Wang L., Zhang H., Chen W., Guo B..( 2011;). Complete genome sequence of the probiotic bacterium Lactobacillus casei LC2W. . J Bacteriol 193: 3419–3420. [CrossRef] [PubMed]
    [Google Scholar]
  7. Ding H., Clark R. J., Ding B..( 2004;). IscA mediates iron delivery for assembly of iron-sulfur clusters in IscU under the limited accessible free iron conditions. . J Biol Chem 279: 37499–37504. [CrossRef] [PubMed]
    [Google Scholar]
  8. Halliwell B., Gutteridge J. M..( 1981;). Formation of thiobarbituric-acid-reactive substance from deoxyribose in the presence of iron salts: the role of superoxide and hydroxyl radicals. . FEBS Lett 128: 347–352.[PubMed] [CrossRef]
    [Google Scholar]
  9. Higuchi M., Shimada M., Yamamoto Y., Hayashi T., Koga T., Kamio Y..( 1993;). Identification of two distinct NADH oxidases corresponding to H2O2-forming oxidase and H2O-forming oxidase induced in Streptococcus mutans. . J Gen Microbiol 139: 2343–2351. [CrossRef] [PubMed]
    [Google Scholar]
  10. Higuchi M., Yamamoto Y., Poole L. B., Shimada M., Sato Y., Takahashi N., Kamio Y..( 1999;). Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. . J Bacteriol 181: 5940–5947.[PubMed]
    [Google Scholar]
  11. Hochwind K., Weinmaier T., Schmid M., van Hemert S., Hartmann A., Rattei T., Rothballer M..( 2012;). Draft genome sequence of Lactobacillus casei W56. . J Bacteriol 194: 6638. [CrossRef] [PubMed]
    [Google Scholar]
  12. Horinouchi S., Weisblum B..( 1982;). Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. . J Bacteriol 150: 815–825.[PubMed]
    [Google Scholar]
  13. Huang T. C., Lin R. F., Chu M. K., Chen H. M..( 1999;). Organization and expression of nitrogen-fixation genes in the aerobic nitrogen-fixing unicellular cyanobacterium Synechococcus sp. strain RF-1. . Microbiology 145: 743–753. [CrossRef] [PubMed]
    [Google Scholar]
  14. Kaga C., Takagi A., Kano M., Kado S., Kato I., Sakai M., Miyazaki K., Nanno M., Ishikawa F. et al.( 2013;). Lactobacillus casei Shirota enhances the preventive efficacy of soymilk in chemically induced breast cancer. . Cancer Sci 104: 1508–1514. [CrossRef] [PubMed]
    [Google Scholar]
  15. Kono Y., Fridovich I..( 1983;). Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. . J Biol Chem 258: 6015–6019.[PubMed]
    [Google Scholar]
  16. Koryszewska-Baginska A., Aleksandrzak-Piekarczyk T., Bardowski J..( 2013;). Complete genome sequence of the probiotic strain Lactobacillus casei (formerly Lactobacillus paracasei) LOCK919. . Genome Announc 1: e00758-13. [CrossRef] [PubMed]
    [Google Scholar]
  17. Makarova K., Slesarev A., Wolf Y., Sorokin A., Mirkin B., Koonin E., Pavlov A., Pavlova N., Karamychev V. et al.( 2006;). Comparative genomics of the lactic acid bacteria. . Proc Natl Acad Sci USA 103: 15611–15616. [CrossRef] [PubMed]
    [Google Scholar]
  18. Matsumoto S., Hara T., Hori T., Mitsuyama K., Nagaoka M., Tomiyasu N., Suzuki A., Sata M..( 2005;). Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. . Clin Exp Immunol 140: 417–426. [CrossRef] [PubMed]
    [Google Scholar]
  19. Matsuzaki T., Takagi A., Ikemura H., Matsuguchi T., Yokokura T..( 2004;). Antitumor activity and action mechanisms of Lactobacillus casei through the regulation of immune responses. . Biofactors 22: 63–66. [CrossRef] [PubMed]
    [Google Scholar]
  20. Mazé A., Boël G., Zúñiga M., Bourand A., Loux V., Yebra M. J., Monedero V., Correia K., Jacques N. et al.( 2010;). Complete genome sequence of the probiotic Lactobacillus casei strain BL23. . J Bacteriol 192: 2647–2648. [CrossRef] [PubMed]
    [Google Scholar]
  21. Miyoshi A., Rochat T., Gratadoux J. J., Le Loir Y., Oliveira S. C., Langella P., Azevedo V..( 2003;). Oxidative stress in Lactococcus lactis. . Genet Mol Res 2: 348–359.[PubMed]
    [Google Scholar]
  22. Nakamura M., Saeki K., Takahashi Y..( 1999;). Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hs cA-fdx-ORF3 gene cluster. . J Biochem 126: 10–18. [CrossRef] [PubMed]
    [Google Scholar]
  23. Reott M. A., Parker A. C., Rocha E. R., Smith C. J..( 2009;). Thioredoxins in redox maintenance and survival during oxidative stress of Bacteroides fragilis. . J Bacteriol 191: 3384–3391. [CrossRef] [PubMed]
    [Google Scholar]
  24. Rocha E. R., Tzianabos A. O., Smith C. J..( 2007;). Thioredoxin reductase is essential for thiol/disulfide redox control and oxidative stress survival of the anaerobe Bacteroides fragilis. . J Bacteriol 189: 8015–8023. [CrossRef] [PubMed]
    [Google Scholar]
  25. Saitou N., Nei M..( 1987;). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol 4: 406–425.[PubMed]
    [Google Scholar]
  26. Sambrook J. W., Russell D. W..( 2001;). Molecular Cloning: a Laboratory Manual , , 3rd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  27. Sanders J. W., Leenhouts K. J., Haandrikman A. J., Venema G., Kok J..( 1995;). Stress response in Lactococcus lactis: cloning, expression analysis, and mutation of the lactococcal superoxide dismutase gene. . J Bacteriol 177: 5254–5260.[PubMed] [CrossRef]
    [Google Scholar]
  28. Serata M., Iino T., Yasuda E., Sako T..( 2012;). Roles of thioredoxin and thioredoxin reductase in the resistance to oxidative stress in Lactobacillus casei. . Microbiology 158: 953–962. [CrossRef] [PubMed]
    [Google Scholar]
  29. Shi H., Bencze K. Z., Stemmler T. L., Philpott C. C..( 2008;). A cytosolic iron chaperone that delivers iron to ferritin. . Science 320: 1207–1210. [CrossRef] [PubMed]
    [Google Scholar]
  30. Shida K., Kiyoshima-Shibata J., Nagaoka M., Watanabe K., Nanno M..( 2006;). Induction of interleukin-12 by Lactobacillus strains having a rigid cell wall resistant to intracellular digestion. . J Dairy Sci 89: 3306–3317. [CrossRef] [PubMed]
    [Google Scholar]
  31. Takahashi Y., Nakamura M..( 1999;). Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters in Escherichia coli. . J Biochem 126: 917–926. [CrossRef] [PubMed]
    [Google Scholar]
  32. Wang S., Zhu H., He F., Luo Y., Kang Z., Lu C., Feng L., Lu X., Xue Y., Wang H..( 2014;). Whole genome sequence of the probiotic strain Lactobacillus paracasei N1115, isolated from traditional Chinese fermented milk. . Genome Announc 2: e00059-14. [CrossRef] [PubMed]
    [Google Scholar]
  33. Wang W., Huang H., Tan G., Si F., Liu M., Landry A. P., Lu J., Ding H..( 2010;). In vivo evidence for the iron-binding activity of an iron-sulfur cluster assembly protein IscA in Escherichia coli. . Biochem J 432: 429–436. [CrossRef] [PubMed]
    [Google Scholar]
  34. Yamamoto Y., Poole L. B., Hantgan R. R., Kamio Y..( 2002;). An iron-binding protein, Dpr, from Streptococcus mutans prevents iron-dependent hydroxyl radical formation in vitro. . J Bacteriol 184: 2931–2939. [CrossRef] [PubMed]
    [Google Scholar]
  35. Yasuda E., Serata M., Sako T..( 2008;). Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. . Appl Environ Microbiol 74: 4746–4755. [CrossRef] [PubMed]
    [Google Scholar]
  36. Zhang W., Yu D., Sun Z., Wu R., Chen X., Chen W., Meng H., Hu S., Zhang H..( 2010;). Complete genome sequence of Lactobacillus casei Zhang, a new probiotic strain isolated from traditional homemade koumiss in Inner Mongolia, China. . J Bacteriol 192: 5268–5269. [CrossRef] [PubMed]
    [Google Scholar]
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