DOI: 10.1128/jb.138.2.377-382.1979. Role of Heme in Synthesis and Membrane Binding of Succinic Dehydrogenase in <i>Bacillus subtilis</i>

Role of Heme in Synthesis and Membrane Binding of Succinic Dehydrogenase in Bacillus subtilis

10.1128/jb.138.2.377-382.1979

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

A 5-aminolevulinic acid-requiring mutant of Bacillus subtilis was isolated. When the mutant is shifted from medium containing 5-aminolevulinic acid to medium lacking this growth factor, the bacteria continued to grow at undiminished rate for about three generations. The membranes from these bacteria contained severely reduced amounts of cytochrome. The mutant was used to study the role of heme synthesis on synthesis and membrane binding of succinic dehydrogenase (SDH). The amount of SDH in whole-cell lysates in the soluble cytoplasmic fraction and in membranes was determined by one-dimensional (rocket) immunoelectrophoresis with an SDH-specific antiserum. After heme synthesis was blocked, the relative amount of SDH in the membrane decreased, whereas increasing amounts of SDH antigen were found in the cytoplasm. When heme synthesis was resumed on readdition of 5-aminolevulinic acid, the amount of membrane-bound SDH antigen increased at a much faster rate than net synthesis. During a 3-h growth period without 5-aminolevulinic acid, there was little change in the pattern of membrane proteins as determined by sodium dodecyl sulfate–polyacrylamide gel electrophoresis of radioactively labeled membranes, as compared to membranes from control cultures. However, both the 65,000-dalton and the 28,000-dalton polypeptides of the SDH complex (L. Hederstedt, E. Holmgren, and L. Rutberg, J. Bacteriol. 138: 370–376, 1979) were present in decreasing amounts in membranes from 5-aminolevulinic acid-starved bacteria. From these results we suggest that SDH in B. subtilis is synthesized as a soluble protein and becomes membrane bound only when it attaches to a site in the membrane, (part of) which is a cytochrome of b type.

Bibliography

Holmgren, E., Hederstedt, L., & Rutberg, L. (1979). Role of Heme in Synthesis and Membrane Binding of Succinic Dehydrogenase in Bacillus subtilis. Journal of Bacteriology, 138(2), 377â382.

Authors 3

Erik Holmgren (first)
Lars Hederstedt (additional)
Lars Rutberg (additional)

References 16 Referenced 34

Anderson , T. J. , and G. Ivanovics . 1967 . Isolation and some characteristics of haemin dependent mutants of Bacillus subtilis . J. Gen. Microbiol. 49 : 31 - 40 . (10.1099/00221287-49-1-31) / J. Gen. Microbiol. / Isolation and some characteristics of haemin dependent mutants of Bacillus subtilis by Anderson T. J. (1967)
Bjerrum , 0. J. 1977 . Immunochemical investigation of membrane proteins. A methodological survey with emphasis placed on immunoprecipitation in gels . Biochim. Biophys. Acta 472 : 135 - 195 . (10.1016/0304-4157(77)90016-8) / Biochim. Biophys. Acta / Immunochemical investigation of membrane proteins. A methodological survey with emphasis placed on immunoprecipitation in gels by Bjerrum 0. (1977)
Davis , K. A. , and Y. Hatefi . 1971 . Succinate dehydrogenase. I Purification, molecular properties and substructure . Biochemistry 10 : 2509 - 2516 . (10.1021/bi00789a014) / Biochemistry / Succinate dehydrogenase. I Purification, molecular properties and substructure by Davis K. A. (1971)
Davis , K. A. , Y. Hatefi , I. P. Crawford , and H. Baltscheffsky . 1977 . Purification, Molecular properties and amino acid composition of Rhodospirillum rubrum succinate dehydrogenase . Arch. Biochem. Biophys. 180 : 459 - 464 . (10.1016/0003-9861(77)90060-1) / Arch. Biochem. Biophys. / Purification, Molecular properties and amino acid composition of Rhodospirillum rubrum succinate dehydrogenase by Davis K. A. (1977)
Farrand , S. K. , and H. W. Taber . 1973 . Physiological effects of menaquinone deficiency in Bacillus subtilis . J. Bacteriol. 115 : 1035 - 1044 . (10.1128/jb.115.3.1035-1044.1973) / J. Bacteriol. / Physiological effects of menaquinone deficiency in Bacillus subtilis by Farrand S. K. (1973)
Gelman , N. S. , M. A. Lukoyanova , and D. N. Ostrovskii . 1975 . Bacterial membranes and the respiratory chain . Biomembranes 6 : 129 - 253 . / Biomembranes / Bacterial membranes and the respiratory chain by Gelman N. S. (1975)
Haddock , B. A. , and H. V. Schairer . 1973 . Electrontransport chains of Escherichia coli. Reconstitution of respiration in a 5-aminolevulinic acid-requiring mutant . Eur. J. Biochem. 35 : 3445 . (10.1111/j.1432-1033.1973.tb02806.x) / Eur. J. Biochem. / Electrontransport chains of Escherichia coli. Reconstitution of respiration in a 5-aminolevulinic acid-requiring mutant by Haddock B. A. (1973)
Hanstein , W. G. , K. A. Davis , M. A. Ghalambor , and Y. Hateff . 1971 . Succinate dehydrogenase. II. Enzymatic properties . Biochemistry 10 : 2517 - 2524 . (10.1021/bi00789a015) / Biochemistry / Succinate dehydrogenase. II. Enzymatic properties by Hanstein W. G. (1971)
Hederstedt , L , E. Holmgren , and L Rutberg . 1979 . Characterization of a succinate dehydrogenase complex solubilized from the cytoplasmic membrane of Bacillus subtilis with the nonionic detergent Triton X-100 . J. Bacteriol. 138 : 370 - 376 . (10.1128/jb.138.2.370-376.1979) / J. Bacteriol. / Characterization of a succinate dehydrogenase complex solubilized from the cytoplasmic membrane of Bacillus subtilis with the nonionic detergent Triton X-100 by Hederstedt L (1979)
Kiss , I. , I. Berek , and G. Ivanovics . 1971 . Mapping the A-aminolevulinic acid synthetase locus in Bacillus subtilis . J. Gen. Microbiol. 66 : 153 - 159 . (10.1099/00221287-66-2-153) / J. Gen. Microbiol. / Mapping the A-aminolevulinic acid synthetase locus in Bacillus subtilis by Kiss I. (1971)
MacGregor , C. H. 1975 . Anaerobic cytochrome b, in Escherichia coli: association with and regulation of nitrate reductase . J. Bacteriol. 121 : 1111 - 1116 . (10.1128/jb.121.3.1111-1116.1975) / J. Bacteriol. / Anaerobic cytochrome b, in Escherichia coli: association with and regulation of nitrate reductase by MacGregor C. H. (1975)
Miki , K. , I. Sekuzu , and K. Okunuki . 1967 . Cytochromes of Bacillus subtilis. I. Cytochrome system in the particulate fraction . Ann. Rep. Biol. Works Fac. Sci. Osaka Univ. 15 : 33 - 58 . / Ann. Rep. Biol. Works Fac. Sci. Osaka Univ. / Cytochromes of Bacillus subtilis. I. Cytochrome system in the particulate fraction by Miki K. (1967)
Ohne , M. 1975 . Regulation of the dicarboxylic acid part of the citric acid cycle in BaciUus subtilis . J. Bacteriol. 122 : 224 - 234 . (10.1128/jb.122.1.224-234.1975) / J. Bacteriol. / Regulation of the dicarboxylic acid part of the citric acid cycle in BaciUus subtilis by Ohne M. (1975)
Ross , E. , and G. Schatz . 1976 . Cytochrome cl of Baker's yeast. II. Synthesis on cytoplasmic ribosomes and influence of oxygen and heme on accumulation of apoprotein . J. Biol. Chem. 251 : 1997 - 2004 . (10.1016/S0021-9258(17)33646-3) / J. Biol. Chem. / Cytochrome cl of Baker's yeast. II. Synthesis on cytoplasmic ribosomes and influence of oxygen and heme on accumulation of apoprotein by Ross E. (1976)
Rutberg , B. , L Hederstedt , E. Holmgren , and L. Rutberg . 1978 . Characterization of succinic dehydrogenase mutants of Bacillus subtilis with crossed immunoelectrophoresis . J. Bacteriol. 136 : 304 - 311 . (10.1128/jb.136.1.304-311.1978) / J. Bacteriol. / Characterization of succinic dehydrogenase mutants of Bacillus subtilis with crossed immunoelectrophoresis by Rutberg B. (1978)
Saltzgaber-Miiller , J. , and G. Schatz . 1978 . Heme is necessary for the accumulation and assembly of cytochrome c oxidase subunits in Saccharomyces cerevisiae . J. Biol. Chem. 253 : 305 - 310 . (10.1016/S0021-9258(17)38304-7) / J. Biol. Chem. / Heme is necessary for the accumulation and assembly of cytochrome c oxidase subunits in Saccharomyces cerevisiae by Saltzgaber-Miiller J. (1978)

Dates

Type	When
Created	5 years, 7 months ago (Jan. 3, 2020, 11:32 a.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:33 p.m.)
Indexed	1 year, 7 months ago (Jan. 14, 2024, 5:42 p.m.)
Issued	46 years, 3 months ago (May 1, 1979)
Published	46 years, 3 months ago (May 1, 1979)
Published Print	46 years, 3 months ago (May 1, 1979)

Funders 0

None

BibTeX

@article{Holmgren_1979, title={Role of Heme in Synthesis and Membrane Binding of Succinic Dehydrogenase in Bacillus subtilis}, volume={138}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.138.2.377-382.1979}, DOI={10.1128/jb.138.2.377-382.1979}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Holmgren, Erik and Hederstedt, Lars and Rutberg, Lars}, year={1979}, month=may, pages={377–382} }

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