Abstract
Nuclear magnetic resonance is established as a sensitive and specific method for following the reduction of dimethylsulphoxide and trimethylamine-N-oxide by bacteria. Using this method it has been shown that cells of Rhodobacter capsulatus reduce both dimethylsulphoxide and trimethylamine-N-oxide at linear rates at all concentrations of these acceptors that can be conveniently detected during a continuous assay. The rate of reduction of trimethylamine-N-oxide was eightfold higher than the rate of dimethylsulphoxide reduction. An upper limit of approximately 0.1 mM may be placed upon the apparent K m value for each acceptor, but the value for dimethylsulphoxide is deduced to be lower than that for trimethylamine-N-oxide on the basis of the strong inhibitory effect of the former on the reduction of the latter. Reduction of trimethylamine-N-oxide by Rb. capsulatus was inhibited by illumination and by oxygen, but only the former effect was relieved following dissipation of the proton electrochemical gradient across the cytoplasmic membrane. Rotenone inhibited the reduction of trimethylamine-N-oxide whereas myxothiazol did not, consistent with a pathway of electrons to the reductase from NADH dehydrogenase that does not involve the cytochrome bc 1complex.
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Abbreviations
- DMS:
-
dimethyl sulphide
- DMSO:
-
dimethyl sulphoxide
- DSS:
-
3-(trimethylsilyl)-1-propane-sulphonic acid
- FCCP:
-
carbonyl cyanide p-trifluoromethoxyphenylhydrazone
- TMA:
-
trimethylamine
- TMAO:
-
trimethylamine-N-oxide
References
Anthony C (1982) The biochemistry of methylotrophs. Academic Press, London
Barrett EL, Kwan HS (1985) Bacterial reduction of trimethylamine oxide. Annu Rev Microbiol 39:131–149
Bilous PT, Weiner JH (1985) Dimethyl sulphoxide reductase activity by anaerobically grown Escherichia coli HB101. J Bacteriol 162:1151–1155
Bont JAM de, Dijken JP van, Harder W (1981) Dimethyl sulphoxide and dimethyl sulphide as a carbon, sulphur and energy source for growth of Hyphomicrobium S. J Gen Microbiol 127:315–323
Castell CH (1950) The influence of trimethylamine-N-oxide in the bacterial reduction of redox indicators. J Fish Res Board of Canada 7:567–575
Chang GW, Chan WL, Lew KK (1976) A trimethylamine-specific electrode for fish quality control. J Food Sci 41:723–724
Clayton RK (1963) Towards the isolation of a photochemical reaction centre in Rhodopseudomonas capsulata. Biochim Biophys Acta 73:312–323
Craske A, Ferguson SJ (1986) Respiratory nitrate reductase from Paracoccus denitrificans molecular characterisation and kinetic properties. Eur J Biochem 158:429–436
Dickenson CJ, Martin PA (1978) Comparison of flame ionisation and flame photometric detectors for the gas chromatographic analysis of dimethylsulphide. J Inst Brewing 84:143
Dyer WJ (1959) Report on trimethylamine in fish. J Anal Chem 42:292–294
Easter MC, Gibson DM, Ward FB (1982) A conductance method for the assay and study of bacterial trimethylamine oxide reduction. J Appl Bacteriol 52:357–365
Ferguson SJ, Jackson JB, McEwan AG (1987) Anaerobic respiration in the Rhodospirillaceae: characterisation of pathways and evaluation of roles in redox balancing during photosynthesis. FEMS Microbiol Rev 46:117–143
Fersht A (1985) Enzyme structure and mechanism (2nd edition). Freeman, New York
Kwan HS, Barrett EL (1983) Purification and properties of trimethylamine oxide reductase from Salmonella typhimurium. J Bacteriol 155:1455–1458
McEwan AG, Ferguson SJ, Jackson JB (1983) Electron flow to dimethylsulphoxide or trimethylamine-N-oxide generates a membrane potential in Rhodopseudomonas capsulata. Arch Microbiol 136:300–305
McEwan AG, Cotton NPJ, Ferguson SJ, Jackson JB (1984) The inhibition of nitrate reduction by light in Rhodopseudomonas capsulata is mediated by the membrane potential, but the inhibition by oxygen is not. Adv Photosynth Res 2:449–452
McEwan AG, Greenfield AJ, Wetzstein HG, Jackson JB, Ferguson SJ (1985a) Nitrous oxide reduction by Rhodospirillaceae and the nitrous oxide reductase of Rhodopseudomonas capsulata. J Bacteriol 164:823–830
McEwan AG, Wetzstein HG, Ferguson SJ, Jackson JB (1985b) Periplasmic location of the terminal reductase in trimethylamine-N-oxide and dimethyl sulphoxide respiration in the photosynthetic bacterium Rhodopseudomonas capsulata. Biochim Biophys Acta 806:410–417
McEwan AG, Wetzstein HG, Meyer O, Jackson JB, Ferguson SJ (1987) The periplasmic nitrate reductase of Rhodobacter capsulatus; purification, characterisation and distinction from a single reductase for trimethylamine-N-oxide, dimethylsulphoxide and chlorate. Arch Microbiol 147:340–345
Madigan MT, Gest H (1978) Growth of a photosynthetic bacterium anaerobically in darkness, supported by “oxidant dependent” sugar fermentation. Arch Microbiol 117:119–122
Morpeth FF, Boxer DH (1985) Kinetic analysis of respiratory nitrate reductase from Escherichia coli K12. Biochemistry 24:40–46
Owens JD, Miskin DR, Wacher-Viveros MC, Benge LCA (1985) Sources of conductance changes during bacterial reduction of trimethylamine oxide to trimethylammonium in phosphate buffer. J Gen Microbiol 131:1357–1361
Richardson DJ, Kelly DJ, Jackson JB, Ferguson SJ, Alef K (1986) Inhibitory effects of myxothiazol and 2-n-heptyl-4-hydroxyquinoline-N-oxide on the auxiliary electron transport pathways of Rhodobacter capsulatus. Arch Microbiol 146:159–165
Taylor DG, Trudgill PW, Cripps RE, Harris PR (1980) The microbial metabolism of acetone. J Gen Microbiol 118:159–170
Vandenberg JI, Kuchel PW, King GF (1986) Application of progress curve analysis to in situ enzyme kinetics monitored using 1H NMR spectroscopy. Anal Biochem 155:38–44
Weaver PF, Wall JD, Gest H (1975) Characterisation of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216
Wood P (1981) The redox potential for dimethylsulphoxide reduction to dimethylsulphide. FEBS Lett 124:11–14
Yamamoto I, Ishimoto M (1977) Anaerobic growth of Escherichia coli on formate by reduction of nitrate, fumarate and trimethylamine-N-oxide. Z Allg Mikrobiol 17:235–242
Yen H-C, Marrs BL (1977) Growth of Rhodopseudomonas capsulata under anaerobic dark conditions with dimethylsulfoxide. Arch Biochem Biophys 181:411–418
Zinder SH, Brock TD (1978) Dimethyl sulfoxide as an electron acceptor for anaerobic growth. Arch Microbiol 116:35–40
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King, G.F., Richardson, D.J., Jackson, J.B. et al. Dimethylsulphoxide and trimethylamine-N-oxide as bacterial electron transport acceptors: use of nuclear magnetic resonance to assay and characterise the reductase system in Rhodobacter capsulatus . Arch. Microbiol. 149, 47–51 (1987). https://doi.org/10.1007/BF00423135
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DOI: https://doi.org/10.1007/BF00423135