Abstract
Phototrophic growth of Rhodobacter capsulatus (formerly Rhodopseudomonas capsulata) under anaerobic conditions with either butyrate or propionate as carbonsource was dependent on the presence of either CO2 or an auxiliary oxidant. NO 3- , N2O, trimethylamine-N-oxide (TMAO) or dimethylsulphoxide (DMSO) were effective provided the appropriate anaerobic respiratory pathway was present. NO 3- was reduced extensively to NO 3- , TMAO to trimethylamine and DMSO to dimethylsulphide under these conditions. Analysis of culture fluids by nuclear magnetic resonance showed that two moles of TMAO or DMSO were reduced per mole of butyrate utilized and one mole of either oxidant was reduced per mole of propionate consumed. The growth rate of Rb. capsulatus on succinate or malate as carbon source was enhanced by TMAO in cultures at low light intensity but not at high light intensities. A new function for anaerobic respiration during photosynthesis is proposed: it permits reducing equivalents from reduced substrates to pass to auxiliary oxidants present in the medium. The use of CO2 or auxiliary oxidants under phototrophic conditions may be influence by the availability of energy from light. It is suggested that the nuclear magnetic resonance methodology developed could have further applications in studies of bacterial physiology.
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Abbreviations
- DMS:
-
dimethylsulphide
- DMSO:
-
dimethylsulphoxide
- TMA:
-
trimethylamine
- TMAO:
-
trimethylamine-N-oxide
- NMR:
-
nuclear magnetic resonance
References
Albers A, Gottschalk G (1976) Acetate metabolism in Rhodopseudomonas gelatinosa and several other Rhodospirillaceae. Arch Microbiol 111:45–49
Alef K, Jackson JB, McEwan AG, Ferguson SJ (1985) The activities of two pathways of nitrate reduction in Rhodopseudomonas capsulata. Arch Microbiol 142:403–408
Coleman JK, Cornish-Bowden A, Cole JA (1978) Purification and properties of nitrite reductase from Escherichia coli K12. Biochem J 175:483–493
Crofts AR, Wraight CA (1883) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185
Farrar TC, Becker ED (1971) Pulse and fourier transform NMR: introduction to theory and methods. Academic Press, New York
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 Revs 46:117:143
Kelly DJ, Richardson DJ, Ferguson SJ, Jackson JB (1988) Isolation of Tn5 insertion mutants of Rhodobacter capsulatus unable to reduce trimethylamine-N-oxide and dimethylsulphoxide. Arch Microbiol 150:138–144
King GF, Richardson DJ, Jackson JB, Ferguson SJ (1987) Dimethylsulphoxide and trimethylamine-N-oxide as electron transport acceptors: use of nuclear magnetic resonance to assay and characterise the reductase system in Rhodobacter capsulatus. Arch Microbiol 149:47–51
Kornberg HL, Lascelles J (1960) The formation of isocitratase by the Athiorhodaceae. J Gen Microbiol 23:511–517
Lascelles J (1960) The formation of ribulose-1,5-diphosphate carboxylase by growing cultures of Athiorhodaceae. J Gen Microbiol 23:499–510
McEwan AG, George CL, Ferguson SJ, Jackson JB (1982) A nitrate reductase activity in Rhodopseudomonas capsulata linked to electron transfer and generation of a membrane protential. FEBS Lett 150:277–280
McEwan, Ferguson SJ, Jackson JB (1983) Electron flow to dimethylamine-N-oxide generates a membrane potential in Rhodopseudomonas capsulata. Arch Microbiol 136:300–305
McEwan AG, Jackson JB, Ferguson SJ (1984) Rationalisation of properties of nitrate reductases in Rhodopseudomonas capsulata. Arch Microbiol 137:333–349
McEwan AG, Wetzstein HG, Ferguson SJ, Jackson JB (1985a) Periplasmic location of the terminal reductase in trimethylamine-N-oxide and dimethylsulphoxide respiration in the photosynthetic bacterium Rhodopseudomonas capsulata. Biochim Biophys Acta 806:810–417
McEwan AG, Greenfield AJ, Wetzstein HG, Jackson JB, Ferguson SJ (1985b), Nitrous oxide reduction by members of the family Rhodospirillaceae and the nitrous oxide reductase of Rhodopseudomonas capsulata. J Bacteriol 164:823–830
McEwan AG, Cotton NPJ, Ferguson SJ, Jackson JB (1985c) The role of auxiliary oxidents in the maintenance of a balanced redox poise for photosynthesis in bacteria. Biochim Biophys Acta 810:140–147
Metzler DE (1977) Biochemistry: the chemical reactions of living cells. Academic Press, New York, p 1129
Ormerod JG (1956) The use of radioactice carbon dioxide in the measurements of carbon dioxide fixation in Rhodospirillum rubrum. Biochem J 64:373–380
Richardson DJ, Kelly DJ, Jackson JB, Ferguson SJ, Alef K (1986) Inhibitory effects of myxothiazol and 2-n-heptyl-4-hydroxyquinone-N-oxide on the auxiliary electron transport pathways of Rhodobacter capsulatus. Arch Microbiol 146:159–165
Schultz JE, Weaver PF (1982) Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata. J Bacteriol 149:181–190
Van Niel CB (1944) The culture, general physiology, morphology and classification of the non-sulphur purple and non-bacteria. Bacteriol Rev 8:1–118
Weaver PF, Wall JD, Gest H (1975) Characterisation of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216
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Richardson, D.J., King, G.F., Kelly, D.J. et al. The role of auxiliary oxidants in maintaining redox balance during phototrophic growth of Rhodobacter capsulatus on propionate or butyrate. Arch. Microbiol. 150, 131–137 (1988). https://doi.org/10.1007/BF00425152
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DOI: https://doi.org/10.1007/BF00425152