Summary
The bioenergetics of Ca2+ transport in bacteria are discussed with special emphasis on the interrelationship between transport and other cellular functions such as substrate oxidation by the respiratory chain and oxidative phosphorylation. The unusual polarity of Ca2+ movement provides an exceptional tool to compare active transport and other ATP requiring or generating processes since this ion is actively taken up by everted vesicles in which the coupling-factor ATPase is exposed to the external medium. As inferred from studies with everted vesicles, the active extrusion of Ca2+ by whole cells can be accomplished by substrate driven respiration, hydrolysis of ATP or as in the case ofStreptococcus faecalis by a nonhydrolytic unknown process which involves ATP directly. Substrate oxidation and the hydrolysis of ATP result in the generation of a pH gradient which can energize the Ca2+ uptake directly (Ca2+/H+ antiport) or via a secondary Na+ gradient (Ca2+/Na+ antiport). In contrast to exponentially growing cells sporulating Bacilli accumulate Ca2+ during the synthesis of dipicolinic acid. Studies involving Ca2+ transport provided evidence in support of the hypothesis that the Mg2+ ATPase fromEscherichia coli not only provides the driving force for various cellular functions but exerts a regulatory role by controlling the permeability of the membrane to protons. The different specificity requirements of various naphthoquinone analogs in the restoration of transport or oxidative phosphorylation, after the natural menaquinone has been destroyed by irradiation, has indicated that a protonmotive force is sufficient to drive active transport. However, in addition to the driving force (protonmotive force) necessary to establish oxidative phosphorylation, a specific spatial orientation of the respiratory components, such as the naphthoquinones, is essential for the utilization of the proton gradient or membrane potential or both. Finally evidence suggesting that intracellular Ca2+ levels might play a fundamental role in bacterial homeostasis is discussed, in particular the role of Ca2+ in the process of chemiotaxis and in conferring bacteria heat stability. A vitamin K-dependent carboxylation reaction has been found inEscherichia coli which is similar to that reported in mammalian systems which results in γ carboxylation of glutamate residues. Although all of the proteins containing γ-carboxyglutamate described so far are involved in Ca2+ metabolism, the role of these proteins inEscherichia coli is unknown and remains to be elucidated.
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Abbreviations
- FCCP:
-
carbonylcyanide p-trifluoromethoxyphenylhydrazone
- DCCD:
-
N′N′ dicyclohexylcarbodiimide
- CCCP:
-
carbonylcyanide m-chlorophenylhydrazone
- PMS:
-
phenazine methosulfate
- D-LDH:
-
D-lactate dehydrogenase
- TPD, N,N,N′N′:
-
tetramethyl-p-phenylenediamine
- pCMPS:
-
p-chloromercuriphenylsulfonate
- HQNO:
-
2n-heptyl-4-hydroxyquinoline-N-oxide
- EGTA:
-
ethyleneglycolbis(amino-ethyl-ether)-N,N′-tetraacetic acid
- TCS:
-
tetrachlorosalicylanilide
- pCMBS:
-
p-chloromercuribenzene sulfonic acid
- pCMB:
-
p-chloromercuribenzoate, ΔμH+, protonmotive force
- Δϕ:
-
membrane potential
- ΔpH:
-
transmembrane proton gradient
References
Silver, S., 1977, in Microorganisms and Minerals (Weinberg, E. D., ed.) pp. 49–103. Marcel Dekker, New York.
Silver, S., 1978, in Bacterial Transport (Rosen, B. P., ed.) pp. 221–324, Marcel Dekker, New York.
Crosby, W. H., Greene, R. A. and Slepecky, R. A., 1971, in Spore Research (Barker, A. M., Gould, G. W. and Wolf, J., eds.) pp. 143–160, Academic Press, New York.
Vinter, V., 1969, in The Bacterial Spore (Gould, G. W. and Hurst, A., eds.) pp. 73–123, Academic Press, New York.
Stahl, S. and Ljunger, C., 1976, FEBS Lett. 63, 184–187.
Kobayashi, H., Van Brunt, J. and Harold, F. M., 1978, J. Biol. Chem. 253, 2085–2092.
Tsuchiya, T. and Rosen, B. P., 1976, J. Biol. Chem. 251, 962–967.
Bhattacharyya, P. and Barnes, E. M., 1976. J. Biol. Chem. 251, 5614–5619.
Barnes, E. M., Roberts, R. R. and Bhattacharyya, P., 1978. Membr. Biochem. 1, 73–88.
Kumar, G., Devés, R. and Brodie, A. F. 1979, Eur. J. Biochem. 100, 365–375.
Belliveau J. W. and Lanyi, J. K. 1978, Arch. Biochem. Biophys. 186, 98–105.
Ordal, G. W. and Fields, R. B., 1977, J. Theor. Biol. 68, 491–500.
Jackson, C. M., 1979, in Vitamin K Metabolism and Vitamin K-dependent Proteins (Suttie, J. W., ed.) pp. 16–29, University Park Press, Baltimore.
Van Buskirk, J. J., Low, M. and Kirsh, W. M., 1979, in Vitamin K Metabolism and Vitamin K-dependent Proteins (Suttie, J. W., ed.) pp. 274–278, University Park Press, Baltimore.
Brodie, A. F. and Gray, C. T., 1956. J. Biol. Chem. 219, 853–862.
Lee, S. H., Sutherland, T. O., Devés, R. and Brodie, A. F., 1980, Proc. Natl. Acad. Sci. USA 77, 102–106.
Hersey, D. F. and Ajl, S. J., 1951, J. Gen. Physiol. 34, 295–304.
Pinchot, G. B. and Racker, E., 1951, in Phosphorus Metabolism (McElroy, W. D. and Glass, B., eds.) Vol. 1, pp. 366–369, John Hopkins Univ. Press, Baltimore.
Pinchot, G. B., 1953. J. Biol. Chem. 205, 65–74.
Brodie, A. F. and Gray, C. T., 1955, Biochim. Biophys. Acta 17, 146–147.
Pinchot, G. B., 1965. Persp. Biol. and Med. 8, 180–195.
Brodie, A. F., Lee, S. H. and Kalra, V. K., 1979, in Microbiology (Schlessinger, D., ed.) pp. 46–53, American Society for Microbiology, Washington, D.C.).
Lee, S. H., Kalra, V. K. and Brodie, A. F., 1979, J. Biol. Chem. 254, 6861–6864.
Higashi, T., Bogin, E. and Brodie, A. F., 1969, J. Biol. Chem. 244, 500–502.
Brodie, A. F., Weber, M. M. and Gray, C. T., 1957. Biochim. Biophys. Acta 25, 448–449.
Brey, R. N. and Rosen, B. P., 1979. J. Biol. Chem. 254, 1957–1963.
Silver, S. and Kralovic, M. L., 1969. Biochem. Biophys. Res. Commun. 34, 640–645.
Silver, S., Toth, K. and Scribner, H. (1975). J. Bacteriol. 122, 880–885.
Bronner, F., Nash, W. C. and Golub, E. E., 1975, in Spores VI (Gerhardt, P., Costilow, R. N. and Sadoff, H. L., eds.) pp. 356–361, American Society for Microbiology, Washington, D.C.
Jasper, P. and Silver, S. 1978. J. Bacteriol. 133, 1323–1328.
Rosen, B. P. and McClees, J. S. 1974. Proc. Natl. Acad. Sci. USA 71, 5042–5046.
Tsuchiya, T. and Rosen, B. P., 1975. J. Biol. Chem. 250, 7687–7692.
Reeves, J. P., 1973. Biochem. Biophys. Res. Commun. 45, 931–936.
Hertzberg, E. L. and Hinkle, P. C., 1974. Biochem. Biophys. Res. Commun. 58, 178–184.
West, I. C. and Mitchell, P., 1974. FEBS Lett. 40, 1.
Hasan, S. M. and Rosen, B. P., 1977. Biochim. Biophys. Acta 459, 225–240.
Tsuchiya, T. and Takeda, K., 1979. J. Biochem. 85, 943–951.
Lee, C. P., 1971. Biochemistry 10, 4375–4381.
Schuldiner, S., Rottenberg, H. and Avron, M. 1972. Eur. J. Biochem. 25, 64–70.
Lee, S. H. and Brodie, A. F., 1978. Biochem. Biophys. Res. Commun. 85, 788–794.
Brey, R. N., Beck, J. C., and Rosen, B. P., 1978. Biochim. Biophys. Res. Commun. 83, 1588–1594.
Adler, L. W. and Rosen, B. P., 1977. J. Bacteriol. 129, 959–966.
Adler, L. W., Ichikawa, T., Hasan, S. M., Tsuchiya, T. and Rosen, B. P., 1977. J. Supramol. Struct. 7, 15–27.
Kaback, H. R., 1974. Science 186, 882–892.
Futai, M., 1974. J. Membr. Biol. 15, 15–28.
Wickner, W., 1976. J. Bacteriol. 127, 162–167.
Hare, J. E., Olden, K. and Kennedy, E. P., 1974. Proc. Natl. Acad. Sci. USA 71, 4843–4846.
Short, S. A., Kaback, H. R. and Kohn, L. D., 1975. J. Biol. Chem. 250, 4291–4296.
Kashket, E. R. and Brodie, A. F., 1963. J. Biol. Chem. 238, 2564–2570.
Barnes, E. M., Jr. and Kaback, H. R., 1971. J. Biol. Chem. 246, 5518–5522.
Tsuchiya, T. and Rosen, B. P., 1975. Biochem. Biophys. Res. Commun. 63, 832–838.
Hasan, S. M., Tsuchiya, T. and Rosen, B. P., 1978. J. Bacteriol 133, 108–113.
Kumar, G., Kalra, V. K. and Brodie, A. F., 1979. Arch. Biochem. Biophys. 198, 22–30.
Brodie, A. F. and Gray, C. T., 1956. Biochim. Biophys. Acta 19, 384–386.
Brodie, A. F., 1959. J. Biol. Chem. 234, 398–404.
Lee, S. H., Kalra, V. K., Ritz, C. J. and Brodie A. F., 1977. J. Biol. Chem. 252, 1084–1091.
Ritz, C. J. and Brodie, A. F., 1977. Biochem. Biophys. Res. Commun. 75, 933–939.
Ritz-Gold, C. J., Gold, C. M. and Brodie, A. F., 1979, Biochim. Biophys. Acta 547, 1–17.
Ritz-Gold, C. J. and Brodie, A. F., 1979. Biochim. Biophys. Acta 547, 18–26.
Carreira, J., Muñoz, E., Andrew, J. M., and Nieto, M., 1976. Biochim. Biophys. Acta 436, 183–189.
Bragg, P. D. and Hou, C., 1975. Arch. Biochem. Biophys. 176, 311–321.
Schnebli, H. P. and Abrams, A. J., 1970. J. Biol. Chem. 245, 1115–1121.
Kumar, G., Kalra, V. K. and Brodie, A. F., 1979. J. Biol. Chem. 254, 1964–1971.
Jacobus, W. E., Tiozzo, R., Lungle, G., Lehninger, A. L. and Carafoli, E., 1975. J. Biol. Chem. 250, 7863–7870.
Vercesi, A., Reynafarje, B. and Lehninger, A. L., 1978. J. Biol. Chem. 253, 6379–6385.
Barnes, E. M. and Bhattacharryya, P., 1977. J Supramol. Struct. 6, 333–344.
Lanyi, J. K., Renthal, R. and McDonald, R. E., 1976. Biochemistry 15, 1603–1610.
Lanyi, J. K. and MacDonald, R. E., 1976. Biochemistry 15, 4608–4615.
Eisenbach, M., Sprung, S., Garty, H., Johnstone, R., Rottenburg, H. and Caplan, S. R., 1977. Biochim. Biophys. Acta 173, 370–376.
Harold, F. M. and Spitz, E., 1975. J. Bacteriol 122, 266–277.
Golub, E. E. and Bronner, F., 1974. J. Bacteriol. 119, 840–843.
Tsuchiya, T. and Rosen, B. P., 1975. J. Biol. Chem. 250, 8409–8415.
Suryanarayana, M. and Brodie, A. F., 1964. J. Biol. Chem. 239, 4292–4297.
Futai, M., Sternweis, P. C. and Heppel, L. A., 1974. Proc. Natl. Acad. Sci. USA 71, 2725–2729.
Bragg, P. D., Davies, P. L. and Hou, C., 1973. Arch. Biochem. Biophys. 159, 664–670.
Larsen, S. H., Adler, J., Gargus, J. J. and Hogg, R. W., 1974. Proc. Natl. Acad. Sci. USA 71, 1239–1243.
Butlin, J. D., Cox, G. B. and Gibson, F., 1971. Biochem. J. 124, 75–81.
Butlin, J. D., Cox, G. B. and Gibson, F., 1973. Biochem. Biophys. Acta 292, 366–375.
Fillingame, R. H., 1975. J. Bacteriol. 124, 870–883.
Brodie, A. F. and Ballantine, J., 1960. J. Biol. Chem. 235, 232–237.
Brodie, A. F., Doris, B. R. and Fieser, L. F., 1958. J. Am. Chem. Soc. 80, 6454.
Gale, P. H., Arison, B. H., Trenner, N. R., Page, A. C., Jr., Folkers, K. and Brodie, A. F., 1963. Biochemistry 2, 200–203.
Hirata, H., Asano, A. and Brodie, A. F., 1971. Biochem. Biophys. Res. Commun. 44, 368–374.
Brodie, A. F. and Ballantine, J., 1960. J. Biol. Chem. 235, 226–231.
Brodie, A. F. and Watanabe, T. 1966. in Vitamins and Hormones (Harris, R. S. ed.) Vol. 24, pp. 447–464, Academic Press, N. Y., London.
Asano, A. and Brodie, A. F., 1965. J. Biol. Chem. 240, 4002–4010.
Brodie, A. F., 1965, in: Biochemistry of Quinones (Morton, R. A., ed.) pp. 355–404. Academic Press, London, N.Y.
Dunphy, P. J. and Brodie, A. F., 1971. in Methods in Enzymology (McCormick, D. B. and Wright, L. D.) Vol 18, pp. 407–460.
Boyer, P. D., 1977. Ann. Rev. Biochem. 46, 957–966.
Williams, R. J. P., 1975. FEBS Lett. 53, 123–125.
Lee, S. H., Cohen, N. S., Jacobs, A. J. and Brodie, A. F., 1979. Biochemistry 18, 2232–2239.
Eisenstadt, E. and Silver, S., 1972. in Spores V, (Halvorson, H. O., Hanson, R., and Campbell, L. L., eds.) pp. 180–186, American Society for Microbiology, Washington, D. C.
Hogarth, C. and Ellat, D. J., 1978. Biochem. J. 176, 197–203.
Hogarth, C. and Ellar, D. J., 1979. Biochem. J. 178, 627–632.
Ordal, G. W., 1977. Nature 270, 66–67.
Berg, H. C. and Brown, D. A. 1972. Nature 239, 500–504.
Macnab, R. M. and Koshland, D. E., Jr., 1972. Proc. Natl. Acad. Sci. USA 69, 2509–2512.
Mato, J. M., 1979. FEBS Lett. 102, 241–243.
Springer, M. S., Kort, E. N., Larsen, S. H., Ordal, G. W., Reader, R. W. and Adler, J., 1975. Proc. Natl. Acad. Sci. USA 72, 4640–4644.
Aswad, D. and Koshland, D. E. Jr., 1974. J. Bacteriol, 118, 640–645.
Koshland, D. E. Jr., 1977. Science 196, 1055–1063.
Ljunger, C. 1970. Physiol. Plant. 23, 351–364.
Stahl, S., 1978. Arch. Microbiol. 119, 17–24.
Stahl, S., 1978. FEMS. Microbiol. Lett. 4, 77–81.
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Dr. A. F. Brodie deceased on January 24, 1981.
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Devés, R., Brodie, A.F. Active transport of Ca2+ in bacteria: Bioenergetics and function. Mol Cell Biochem 36, 65–84 (1981). https://doi.org/10.1007/BF02354906
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DOI: https://doi.org/10.1007/BF02354906