Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1981 Jun;146(3):928–936. doi: 10.1128/jb.146.3.928-936.1981

Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria.

F S Archibald, I Fridovich
PMCID: PMC216946  PMID: 6263860

Abstract

A previous study of the aerotolerant bacterium Lactobacillus plantarum, which lacks superoxide dismutase (SOD), demonstrated that it possesses a novel substitute for this defensive enzyme. Thus, L. plantarum contains 20 to 25 mM Mn(II),m in a dialyzable form, which is able to scavenge O2- apparently as effectively as do the micromolar levels of SOD present in most other organisms. This report describes a survey of the lactic acid bacteria. The substitution of millimolar levels of Mn(II) for micromolar levels of SOD is a common occurrence in this group of microorganisms, which contained either SOD or high levels of Mn(II), but not both. Two strains were found which had neither high levels of Mn(II) nor SOD, and they were, as was expected, very oxygen intolerant. Lactic acid bacteria containing SOD grew better aerobically than anaerobically, whereas the organisms containing Mn(II) in place of SOD showed aerobic growth which was best, at best, equal to anaerobic growth. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) increases the rate of O2- production in these organisms. Lactobacillus strains containing high intracellular Mn(II) were more resistant to the oxygen-dependent toxicity of plumbagin than were strains containing lower levels of Mn(II). The results support the conclusion that a high internal level of Mn(II) provides these organisms with an important defence against endogenous O2-.

Full text

PDF
931

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Archibald F. S., Fridovich I. Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J Bacteriol. 1981 Jan;145(1):442–451. doi: 10.1128/jb.145.1.442-451.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beauchamp C., Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971 Nov;44(1):276–287. doi: 10.1016/0003-2697(71)90370-8. [DOI] [PubMed] [Google Scholar]
  3. Brawn K., Fridovich I. DNA strand scission by enzymically generated oxygen radicals. Arch Biochem Biophys. 1981 Feb;206(2):414–419. doi: 10.1016/0003-9861(81)90108-9. [DOI] [PubMed] [Google Scholar]
  4. Britton L., Malinowski D. P., Fridovich I. Superoxide dismutase and oxygen metabolism in Streptococcus faecalis and comparisons with other organisms. J Bacteriol. 1978 Apr;134(1):229–236. doi: 10.1128/jb.134.1.229-236.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bryan-Jones D. G., Whittenbury R. Haematin-dependent oxidative phosphorylation in Streptococcus faecalis. J Gen Microbiol. 1969 Oct;58(2):247–260. doi: 10.1099/00221287-58-2-247. [DOI] [PubMed] [Google Scholar]
  6. Cone R., Hasan S. K., Lown J. W., Morgan A. R. The mechanism of the degradation of DNA by streptonigrin. Can J Biochem. 1976 Mar;54(3):219–223. doi: 10.1139/o76-034. [DOI] [PubMed] [Google Scholar]
  7. Curnutte J. T., Karnovsky M. L., Babior B. M. Manganese-dependent NADPH oxidation by granulocyte particles. The role of superoxide and the nonphysiological nature of the manganese requirement. J Clin Invest. 1976 Apr;57(4):1059–1067. doi: 10.1172/JCI108348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. EVANS J. B., NIVEN C. F., Jr Nutrition of the heterofermentative Lactobacilli that cause greening of cured meat products. J Bacteriol. 1951 Nov;62(5):599–603. doi: 10.1128/jb.62.5.599-603.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. FRIDOVICH I., HANDLER P. Xanthine oxidase. V. Differential inhibition of the reduction of various electron acceptors. J Biol Chem. 1962 Mar;237:916–921. [PubMed] [Google Scholar]
  10. Fox G. E., Stackebrandt E., Hespell R. B., Gibson J., Maniloff J., Dyer T. A., Wolfe R. S., Balch W. E., Tanner R. S., Magrum L. J. The phylogeny of prokaryotes. Science. 1980 Jul 25;209(4455):457–463. doi: 10.1126/science.6771870. [DOI] [PubMed] [Google Scholar]
  11. Greenstock C. L., Miller R. W. The oxidation of tiron by superoxide anion. Kinetics of the reaction in aqueous solution in chloroplasts. Biochim Biophys Acta. 1975 Jul 8;396(1):11–16. doi: 10.1016/0005-2728(75)90184-x. [DOI] [PubMed] [Google Scholar]
  12. Gregory E. M., Fridovich I. Induction of superoxide dismutase by molecular oxygen. J Bacteriol. 1973 May;114(2):543–548. doi: 10.1128/jb.114.2.543-548.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gregory E. M., Fridovich I. Oxygen metabolism in Lactobacillus plantarum. J Bacteriol. 1974 Jan;117(1):166–169. doi: 10.1128/jb.117.1.166-169.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hassan H. M., Fridovich I. Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys. 1979 Sep;196(2):385–395. doi: 10.1016/0003-9861(79)90289-3. [DOI] [PubMed] [Google Scholar]
  15. Kirby T., Blum J., Kahane I., Fridovich I. Distinguishing between Mn-containing and Fe-containing superoxide dismutases in crude extracts of cells. Arch Biochem Biophys. 1980 May;201(2):551–555. doi: 10.1016/0003-9861(80)90544-5. [DOI] [PubMed] [Google Scholar]
  16. Kono Y., Takahashi M. A., Asada K. Oxidation of manganous pyrophosphate by superoxide radicals and illuminated spinach chloroplasts. Arch Biochem Biophys. 1976 Jun;174(2):454–462. doi: 10.1016/0003-9861(76)90373-8. [DOI] [PubMed] [Google Scholar]
  17. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  18. Lesko S. A., Lorentzen R. J., Ts'o P. O. Role of superoxide in deoxyribonucleic acid strand scission. Biochemistry. 1980 Jun 24;19(13):3023–3028. doi: 10.1021/bi00554a029. [DOI] [PubMed] [Google Scholar]
  19. Lown J. W., Weir G. Studies related to antitumor antibiotics. Part XIV. Reactions of mitomycin B with DNA. Can J Biochem. 1978 May;56(5):269–304. [PubMed] [Google Scholar]
  20. Lynch R. E., Cole B. C. Mycoplasma pneumoniae: a prokaryote which consumes oxygen and generates superoxide but which lacks superoxide dismutase. Biochem Biophys Res Commun. 1980 Sep 16;96(1):98–105. doi: 10.1016/0006-291x(80)91186-9. [DOI] [PubMed] [Google Scholar]
  21. McCord J. M., Keele B. B., Jr, Fridovich I. An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc Natl Acad Sci U S A. 1971 May;68(5):1024–1027. doi: 10.1073/pnas.68.5.1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McPhail L. C., DeChatelet L. R., Shirley P. S. Further characterization of NADPH oxidase activity of human polymorphonuclear leukocytes. J Clin Invest. 1976 Oct;58(4):774–780. doi: 10.1172/JCI108528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morgan A. R., Cone R. L., Elgert T. M. The mechanism of DNA strand breakage by vitamin C and superoxide and the protective roles of catalase and superoxide dismutase. Nucleic Acids Res. 1976 May;3(5):1139–1149. doi: 10.1093/nar/3.5.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Norrod P., Morse S. A. Absence of superoxide dismutase in some strains of Neisseria gonorrhoeae. Biochem Biophys Res Commun. 1979 Oct 29;90(4):1287–1294. doi: 10.1016/0006-291x(79)91176-8. [DOI] [PubMed] [Google Scholar]
  25. Smalley A. J., Jahrling P., Van Demark P. J. Molar growth yields as evidence for oxidative phosphorylation in Streptococcus faecalis strain 10Cl. J Bacteriol. 1968 Nov;96(5):1595–1600. doi: 10.1128/jb.96.5.1595-1600.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Van Hemmen J. J., Meuling W. J. Inactivation of biologically active DNA by gamma-ray-induced superoxide radicals and their dismutation products singlet molecular oxygen and hydrogen peroxide. Biochim Biophys Acta. 1975 Aug 21;402(2):133–141. doi: 10.1016/0005-2787(75)90031-3. [DOI] [PubMed] [Google Scholar]
  27. Waud W. R., Brady F. O., Wiley R. D., Rajagopalan K. V. A new purification procedure for bovine milk xanthine oxidase: effect of proteolysis on the subunit structure. Arch Biochem Biophys. 1975 Aug;169(2):695–701. doi: 10.1016/0003-9861(75)90214-3. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES