Combination of heterogeneous catalase and superoxide dismutase protects Bifidobacterium longum strain NCC2705 from oxidative stress

Applied Microbiology and Biotechnology

Volumn 98, Issue 17, 2014, Pages 7523-7534

  Zuo, Fanglei ^a   Yu, Rui ^a   Feng, Xiujuan ^b   Khaskheli, Gul Bahar ^a   Chen, Lili ^a   Ma, Huiqin ^a   Chen, Shangwu ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b CHINA UNIVERSITY OF PETROLEUM   (China)

Author keywords

Bifidobacteria; Catalase; Oxidative stress; Reactive oxygen species; Superoxide dismutase

Indexed keywords

BACTERIA; ENZYMES; GENES; PORPHYRINS; REACTIVE OXYGEN SPECIES; STRAIN RATE;

BIFIDOBACTERIA; BIFIDOBACTERIUM LONGUM; CATALASE; HETEROGENEOUS EXPRESSIONS; LACTOBACILLUS PLANTARUM; OXIDATIVE STRESS RESPONSE; STREPTOCOCCUS THERMOPHILUS; SUPER OXIDE DISMUTASE;

OXIDATIVE STRESS;

CATALASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; BACTERIAL DNA; PEROXIDE; RECOMBINANT PROTEIN;

DNA; ENZYME ACTIVITY; GENE EXPRESSION; MICROBIAL ACTIVITY; OXIDATION; SYNERGISM;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BIFIDOBACTERIUM LONGUM; CELL VIABILITY; CISTRON; CONTROLLED STUDY; ESCHERICHIA COLI; LACTOBACILLUS PLANTARUM; LPKATL GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PLASMID; PROTEIN EXPRESSION; STREPTOCOCCUS THERMOPHILUS; STSODA GENE; BIFIDOBACTERIUM; CHEMISTRY; DNA SEQUENCE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; PHYSIOLOGY;

BIFIDOBACTERIUM LONGUM; LACTOBACILLUS PLANTARUM; STREPTOCOCCUS THERMOPHILUS;

BIFIDOBACTERIUM; CATALASE; DNA, BACTERIAL; GENE EXPRESSION; LACTOBACILLUS PLANTARUM; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PEROXIDES; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; STREPTOCOCCUS THERMOPHILUS; SUPEROXIDE DISMUTASE;

EID: 84906948249     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5851-z     Document Type: Article

References (38)

1. Abriouel H, Herrmann A, Stärke J, Yousif NMK, Wijaya A, Tauscher B, Holzapfel W, Franz CMAP (2004) Cloning and heterologous expression of hematin-dependent catalase produced by Lactobacillus plantarum CNRZ 1228. Appl Environ Microbiol 70:603-606 (Pubitemid 38090255)
2. Achuthan AA, Duary RK, Madathil A, Panwar H, Kumar H, Batish VK, Grover S (2012) Antioxidative potential of lactobacilli isolated from the gut of Indian people. Mol Biol Rep 39:7887-7897
3. An HR, Zhai ZY, Yin S, Luo YB, Han BZ, Hao YL (2011) Coexpression of the superoxide dismutase and the catalase provides remarkable oxidative stress resistance in Lactobacillus rhamnosus. J Agric Food Chem 59:3851-3856
4. Andrus JM, Bowen SW, Klaenhammer TR, Hassan HM (2003) Molecular characterization and functional analysis of the manganese-containing superoxide dismutase gene (sodA) from Streptococcus thermophilus AO54. Arch Biochem Biophys 420:103-113 (Pubitemid 37393379)
5. Archibald FS, Fridovich I (1981) Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J Bacteriol 145:442-451 (Pubitemid 11140325)
6. Boylston TD, Vinderola CG, Ghoddusi HB, Reinheimer JA (2004) Incorporation of bifidobacteria into cheeses: challenges and rewards. Int Dairy J 14:375-387 (Pubitemid 38345661)
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgramquantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
8. Bruno-Bárcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM (2004) Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol 70:4702-4710 (Pubitemid 39095495)
9. Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025-1035 (Pubitemid 46183877)
10. Halliwell B, Gutteridge JMC (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501-514 (Pubitemid 16072574)
11. Hayashi K, Maekawa I, Tanaka K, Ijyuin S, Shiwa Y, Suzuki I, Niimura Y, Kawasaki S (2013) Purification and characterization of oxygen-inducible haem catalase from oxygen-tolerant Bifidobacterium asteroides. Microbiology 159:89-95
12. He JL, Sakaguchi K, Suzuki T (2012) Acquired tolerance to oxidative stress in Bifidobacterium longum 105-A via the expression of a catalase gene. Appl Environ Microbiol 78:2988-2990
13. Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y (2006) Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl Environ Microbiol 72:6854-6858 (Pubitemid 44582936)
14. Khokhlova EV, Efimov BA, Kafarskaia LI, Shkoporov AN (2010) Heterologous expression of secreted biologically active human interleukin-10 in Bifidobacterium breve. Arch Microbiol 192:769 -774
15. Klijn A, Moine D, Delley M, Mercenier A, Arigoni F, Pridmore RD (2006) Construction of a reporter vector for the analysis of Bifidobacterium longum promoters. Appl Environ Microbiol 72:7401-7405 (Pubitemid 44748466)
16. Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751-5754
17. Korshunov S, Imlay JA (2010) Two sources of endogenous hydrogen peroxide in Escherichia coli. Mol Microbiol 75:1389-1401
18. Lee J, Hwang KT, Chung MY, Cho DH, Park CS (2005) Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. J Food Sci 70:388-391
19. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469-474
20. Messner KR, Imlay JA (1999) The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J Biol Chem 274:10119-10128
21. Oberg TS, Ward RE, Steele JL, Broadbent JR (2013) Genetic and physiological responses of Bifidobacterium animalis subsp. lactis to hydrogen peroxide stress. J Bacteriol 195:3743-3751
22. Ruiz L, Ruas-Madiedo P, Gueimonde M, de Los Reyes-Gavilán CG, Margolles A, Sánchez B (2011) How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences. Genes Nutr 6:307-318
23. Ruiz L, Gueimonde M, Ruas-Madiedo P, Ribbera A, de los Reyes-Gavilán CG, Ventura M, Margolles A, Sánchez B (2012) Molecular clues to understand the aerotolerance phenotype of Bifidobacterium animalis subsp. lactis. Appl Environ Microbiol 78:644-650
24. Samson G, Herbert SK, Fork DC, Laudenbach DE (1994) Acclimation of the photosynthetic apparatus to growth irradiance in a mutant strain of Synechococcus lacking iron superoxide dismutase. Plant Physiol 105:287-294
25. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore RD, Arigoni F (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99:14422-14427 (Pubitemid 35257687)
26. Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173-7181 (Pubitemid 33121851)
27. Seaver LC, Imlay JA (2004) Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem 279:48742-48750 (Pubitemid 39625751)
28. Shea RJ, Mulks MH (2002) Ohr, encoding an organic hydroperoxide reductase, is an in vivo-induced gene in Actinobacillus pleuropneumoniae. Infect Immun 70:794-802 (Pubitemid 34083842)
29. Shimizu N, Kobayashi K, Hayashi K (1984) The reaction of superoxide radical with catalase: mechanism of the inhibition of catalase by superoxide radical. J Biol Chem 259:4414-4418 (Pubitemid 14126890)
30. Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389-394
31. Steele KH, Baumgartner JE, Valderas MW, Martin Roop R II (2010) Comparative study of the roles of AhpC and KatE as respiratory antioxidants in Brucella abortus 2308. J Bacteriol 192:4912-4922
32. Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2:188-194 (Pubitemid 29176944)
33. Sun ZK, Baur A, Zhurina D, Yuan J, Riedel CU (2012) Accessing the inaccessible: molecular tools for bifidobacteria. Appl Environ Microbiol 78:5035-5042
34. Whittenbury R (1964) Hydrogen peroxide formation and catalase activity in the lactic acid bacteria. J Gen Mirobiol 35:13-26
35. Wolff SP (1994) Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. In: Sies H (ed) Methods in enzymology: oxygen radicals in biological systems part C, Vol. 233. Academic Press, London, pp 182-189
36. Wood NJ, Sørensen J (2001) Catalase and superoxide dismutase activity in ammonia-oxidising bacteria. FEMS Microbiol Ecol 38:53-58 (Pubitemid 34033720)
37. Xiao M, Xu P, Zhao JY, Wang Z, Zuo FL, Zhang JW, Ren FZ, Li PL, Chen SW, Ma HQ (2011) Oxidative stress-related responses of Bifidobacterium longum subsp. longum BBMN68 at the proteomic level after exposure to oxygen. Microbiology 157:1573-1588
38. Zuo FL, Feng XJ, Sun XF, Du C, Chen SW (2013) Characterization of plasmid pML21 of Enterococcus faecalis ML21 from koumiss. Curr Microbiol 66:103-105