Abstract
Brochothrix thermosphacta, grown in batch culture in a yeast-dextrose broth, at temperatures from 30 °C to 10 °C, contained diverse membrane-bound respiratory cytochromes. Under conditions of moderate aeration, cytochromes of the a-, b- and d-type were detected at all growth temperatures, but the proportions changed as a function of temperature, with the spectra of cells grown at 10 or 15 °C being dominated by a-type cytochrome(s). Cytochrome a 3 was detected by its reactions with CO and cyanide in cells from all growth conditions. An additional cytochrome a, which was not cyanide-reactive, was also detected, suggesting the presence of an aa 3 oxidase complex. Cytochrome d was cyanide- and CO-reactive, but not detectable in photodissociation spectra, presumably because of the very rapid recombination of CO at the sub-zero temperatures used. Decreasing the oxygen transfer rates to batch cultures resulted in enhanced expression of cytochrome d and changed the proportion of the aa 3-type oxidase that could be attributed to ligand-binding cytochrome a 3; at the lowest oxygen transfer rates, no cytochrome a was detected, suggesting the presence of a cytochrome ba 3 terminal oxidase complex. Intact cells showed no evidence of a c-type cytochrome and no haem C was detected in membrane preparations. After growth at 10°C, the cytochrome composition of B. campestris was essentially identical to that of B. thermosphacta. The multiplicity of putative terminal oxidases in B. thermosphacta is discussed.
Similar content being viewed by others
References
Anemuller S, Schafer G (1990) Cytochrome aa 3 from Sulfolobus acidocaldarius. A single-subunit, quinol-oxidizing archaebacterial terminal oxidase. Eur J Biochem 191: 297–305
Anraku Y (1988) Bacterial electron transport chains. Annu Rev Biochem 57: 101–132
Chance B (1957) Techniques for the assay of the respiratory enzymes. Methods Enzymol 4: 272–329
Davidson CM, Hartree EF (1968) Cytochrome as a guide to classifying bacteria: taxonomy of Microbacterium thermosphactum. Nature 220: 502–504
Davidson CM, Mobbs P, Stubbs JM (1968) Some morphological and physiological properties of Microbacterium thermosphactum. J Appl Bacteriol 31: 551–559
Deibel RH, Evans JB (1960) Modified benzidine test for the detection of cytochrome-containing respiratory systems in microorganisms. J Bacteriol 79: 356–360
Feresu SB, Jones D (1988) Taxonomic studies on Brochothrix, Erysipelothrix, Listeria and atypical lactobacilli. J Gen Microbiol 134: 1165–1183
Gardner GA (1982) Brochothrix thermosphacta (Microbacterium thermosphactum) in the spoilage of meats: a review. In: Roberts TA, Hobbs GH, Christian JHB, Skovgaard N (ed) Psychrotrophic microorganisms in spoilage and pathogenicity. Academic Press, London, pp. 139–173
Hitchener BJ, Egan AF, Rogers PJ (1979) Energetics of Microbacterium thermosphactum in glucose-limited continuous culture. Appl Environ Microbiol 37: 1047–1052
Hubbard JA, Hughes MN, Poole RK (1989) Effects of copper concentration in continuous culture on the aa 3-type cytochrome oxidase and respiratory chains of Paracoccus denitrificans. Arch Microbiol 151: 300–306.
Jones CW, Poole RK (1985) The analysis of cytochromes. Methods Microbiol 18: 285–328
Keilin D (1966) The history of cell respiration and cytochrome. Cambridge University Press, Cambridge, UK
Kita K, Konishi K, Anraku Y (1986) Purification and properties of two terminal oxidase complexes of Escherichia coli aerobic respiration chain. Methods Enzymol 126: 94–113
Lauraeus M, Haltia T, Saraste M, Wikstrom M (1991) Bacillus subtilis expresses two kinds of haem-A-containing terminal oxidases. Eur J Biochem 197: 699–705
Lemma E, Unden G, Kroger A (1990) Menaquinone is an obligatory component of the chain catalyzing succinate respiration in Bacillus subtilis. Arch Microbiol 155: 62–67
Ludwig B, Schatz G (1980) A two-subunit cytochrome c oxidase (cytochrome aa 3) from Paracoccus denitrificans. Proc Natl Acad Sci USA 77: 196–200
Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87: 206–210
Matsushita K, Shinagawa E, Adachi O, Ameyama M (1990) Cytochrome a 1 of Acetobacter aceti is a cytochrome ba functioning as ubiquinol oxidase. Proc Natl Acad Sci USA 87: 9863–9867
Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell Scientific Publications, Oxford
Poole RK (1983) Bacterial cytochrome oxidases. A structurally and functionally diverse group of electron transfer proteins. Biochim Biophys Acta 726: 205–243
Pole RK (1988) Bacterial cytochrome oxidases. In: Anthony C (ed) Bacterial energy transduction. Academic Press, London, pp 231–291
Poole RK, Sivaram A, Salmon I, Chance B (1982) Photolysis at very low temperatures of CO-liganded cytochrome oxidase (cytochrome d) in oxygen-limited Escherichia coli. FEBS Lett 141: 237–241
Poole RK, Kumar C, Salmon I, Chance B (1983) The 650 nm chromophore in Escherichia coli is an “oxy” — or oxygenated compound, not the oxidized form of cytochrome oxidase d: a hypothesis. J Gen Microbiol 129: 1335–1344
Pudek MR, Bragg PD (1974) Inhibition by cyanide of the respiratory chain oxidases of Escherichia coli. Arch Biochem Biophys 164: 682–693
Saraste M, Holm L, Lemieux L, Lubben M, van derOost J (1991) The happy family of cytochrome oxidases. Biochem Soc Trans 19: 608–612
Sneath PHA, Jones D (1976) Brochothrix, a new genus tentatively placed in the family Lactobacillaceae. Int J Syst Bacteriol 26: 102–104
Talon R, Grimont PAD, Grimont F, Gasser F, Boeufgras JM (1988) Brochothrix campestris sp. nov. Int J Syst Bacteriol 38: 99–102
Wikstrom M, Krab K, Saraste M (1981) Cytochrome oxidase. A synthesis. Academic Press, London
Williams HD, Poole RK (1987) The cytochromes of Acetobacter pasteurianus NCIB 6428. Evidence of a role for a cytochrome a-like haemoprotein in electron transfer to cytochrome oxidase d. J Gen Microbiol 133: 2461–2472
Williams HD, Tan HB, Poole RK (1990) The occurrence and function of a-type cytochromes in the aerobic respiratory chain of Comamonas percolans NCTC 1937 grown under different conditions. J Gen Microbiol 136: 1167–1175
Zimmerman BH, Nitsche CI, Fee JA, Rusnak F, Munck E (1988) Properties of a copper-containing cytochrome ba 3: a second oxidase from the extreme thermophile Thermus thermophilus. Proc Natl Acad Sci USA 85: 5779–5783
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gil, A., Kroll, R.G. & Poole, R.K. The cytochrome composition of the meat spoilage bacterium Brochothrix thermosphacta: identification of cytochrome a 3- and d-type terminal oxidases under various conditions. Arch. Microbiol. 158, 226–233 (1992). https://doi.org/10.1007/BF00290819
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00290819