Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The role ofc-type cytochromes in the terminal respiratory chain of the methylotrophic bacteriumMethylophilus methylotrophus

  • 14 Accesses

  • 13 Citations

Abstract

Whole cells of the methylotrophic bacteriumMethylophilus methylotrophus cultured under methanol-limited conditions contain approximately equal amounts of two majorc-type cytochromes,c H andc L. Virtually all of the cytochromec H, and over one-third of the cytochromec L, are loosely attached to the periplasmic surface of the respiratory membrane whence they can be released by sonication or by washing cells in ethylenediaminetetraacetate (EDTA). The latter causes inhibition of methanol oxidase activity and stimulation of ascorbate-N,N,N′,N′-tetramethyl-p-phenylenediamine (TMPD) oxidase activity, neither of which effects are reversible by divalent metal ions. Kinetic analyses indicate that ascorbate-TMPD is oxidised via two routes, viz. a slow low-affinity pathway involving loosely membrane-boundc-type cytochromes plus cytochrome oxidaseaa 3, and a faster higher-affinity pathway involving the firmly membrane-bound cytochrome oxidasec L o complex; the former route predominates in the presence of divalent metal ions, and the latter route after exposure to EDTA. These and other results are discussed in terms of the spatial organisation of the terminal respiratory chain, and of the role ofc-type cytochromes in the oxidation of methanol and ascorbate-TMPD.

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

Abbreviations

EDTA:

Enthylenediaminetetraacetate

PMS:

Phenazinemethosulphate

TMPD:

N,N,N′,N′-tetramethyl-p-phenylenediamine

SDS:

Sodium dodecylsulphate

I50 :

Concentration of inhibitor required to give 50% inhibition of enzyme activity

PQQ:

Pyrroloquinoline quinone

References

  1. Ackrell BAC, Jones CW (1971) The respiratory system ofAzotobacter vinelandii. 2. Oxygen effects. Europ J Biochem 20:29–35

  2. Anthony C, Zatman LJ (1964) The microbial oxidation of methanol: isolation and properties ofPseudomonas sp. M 27. Biochem J 92:609–614

  3. Beardsmore AJ, Aperghis PNG, Quayle JR (1982) Characterisation of the assimilatory and dissimilatory pathways of carbon metabolism during growth ofMethylophilus methylotrophus on methanol. J Gen Microbiol 128:1423–1439

  4. Beardmore-Gray M, O'Keefe DT, Anthony C (1982) The autoreducible cytochromesc of the methylotrophsMethylophilus methylotrophus andPseudomonas AM 1 Biochem J 207:161–165

  5. Beardmore-Gray M, O'Keefe DT, Anthony C (1983) The methanol: cytochromec oxidoreductase activity ofMethylophilus methylotrophus. J Gen Microbiol 129:923–933

  6. Burton SM, Byrom D, Carver MA, Jones GDD, Jones CW (1983) The oxidation of methylated amines by the methylotrophic bacteriumMethylophilus methylotrophus. FEMS Microbiol Letts 17:185–190

  7. Carver MA, Jones CW (1983) The terminal respiratory chain of the methylotrophic bacteriumMethylophilus methylotrophus. FEBS Letts 155:187–191

  8. Carver MA, Humphrey KM, Patchett RA, Jones CW (1983) The effect of EDTA and related chelating agents on the oxidation of methanol by the methylotrophic bacteriumMethylophilus methylotrophus. Europ J Biochem 138:611–615

  9. Cross AR, Anthony C (1980a) The purification and properties of the soluble cytochromesc of the obligate methylotrophMethylophilus methylotrophus. Biochem J 192:421–427

  10. Cross AR, Anthony C (1980b) The electron transport chains of the obligate methylotrophMethylophilus methylotrophus. Biochem J 192:429–439

  11. Dawson MJ, Jones CW (1981a) Respiration-linked proton translocation in the obligate methylotrophMethylophilus methylotrophus. Biochem J 194:915–924

  12. Dawson MJ, Jones CW (1981b) Energy conservation in the terminal region of the respiratory chain of the methylotrophic bacteriumMethylophilus methylotrophus. Europ J Biochem 118:113–118

  13. Duine JA, Frank J (1981) Methanol dehydrogenase: a quinoprotein. In: Dalton H (ed) Microbial growth on C1 compounds. Heyden, London, pp 31–41

  14. Duine JA, Frank J, De Ruiter LG (1979) Isolation of a methanol dehydrogenase with a functional coupling to cytochromec. Gen Microbiol 115:523–526

  15. Ferguson-Miller S, Brautigan DL, Margoliash E (1976) Correlation of the kinetics of electron-transfer activity of various eukaryotic cytochromesc with binding to mitochondrial cytochromec oxidase. J Biol Chem 251:1104–1115

  16. Ferguson-Miller S, Brautigan DL, Margoliash E (1978) Definition of cytochromec binding domains by chemical modification. J Biol Chem 253:149–159

  17. Hauska G, Trebst A, Melandri BA (1977) Artificial energy conservation in the respiratory chain; no native coupling between cytochromec and oxygen. FEBS Letts 73:385–391

  18. Jones CW (1973) The inhibition ofAzobacter vinelandii terminal oxidases by cyanide. FEBS Letts 36:347–350

  19. Jones CW, Kingsbury SA, Dawson MJ (1982) The partial resolution and dye-mediated reconstitution of methanol oxidase activity inMethylophilus methylotrophus. FEMS Microbiol Letts 13:195–200

  20. Meyer DJ (1972) Bacterial cytochrome oxidases. Ph. D. Thesis. University of Leicester

  21. Sorgato MC, Ferguson SJ, Kell DB, John P (1978) The protonmotive force in bovine heart submitochondrial particles. Biochem J 174:237–256

  22. Swank RT, Munkres KD (1971) Molecular weight analysis of oligopeptides by electrophoresis in polyacrylamide gel with sodium dodecyl sulphate. Anal Biochem 39:462–477

  23. Weber K, Osborne M (1969) The reliability of molecular weight determinations by dodecyl sulphate-polyacrylamide gel electrophoresis. J Biol Chem 244:4406–4412

  24. Wood PM (1980) Do photosynthetic bacteria contain cytochromec 1? Biochem J 189:385–391

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Carver, M.A., Jones, C.W. The role ofc-type cytochromes in the terminal respiratory chain of the methylotrophic bacteriumMethylophilus methylotrophus . Arch. Microbiol. 139, 76–82 (1984). https://doi.org/10.1007/BF00692716

Download citation

Key words

  • Bacterial respiration
  • Methylophilus methylotrophus
  • Cytochromes
  • Respiratory membrane