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Expression of bacterial luminescence is stimulated by nalidixic acid in a nalidixic acid resistant mutant

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Abstract

Cells of Photobacterium phosphoreum (strain 496) grow equally well in a complex medium with 1% and 3% NaCl, but luminescence occurs with 3% but not 1% NaCl in the medium. However, log phase cells growing in 1% NaCl will develop luminescence within 30 to 45 min following a shift to 3% NaCl. Unlike the situation in certain other species of luminescent bacteria, this increase is not paralleled by increases in luciferase, the key enzyme in the luminescent reaction. In the present study it has been found that nalidixic acid and novobiocin, inhibitors of DNA gyrase, block this development of bioluminescence at concentrations where growth is not completely inhibited, but without concomitant changes in extractable luciferase activity. In a nalidixic acid-resistant mutant, growth was normal, but luminescence was greater than in the wild type. Addition of nalidixic acid stimulated luminescence even more, but again without concomitant changes in extractable luciferase activity. These results suggest that transcription of the certain genes affecting bioluminescence in bacteria is differentially sensitive to gyrase activity, and thus to DNA structure and/or conformation. However, the proteins and/or factors responsible for affecting bioluminescence under these conditions have not been identified.

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Abbreviations

nal:

nalidixic acid

References

  • Cozzarelli NR (1977) The mechanism of action of inhibitors of DNA synthesis. Annu Rev Biochem 46:641–668

    Google Scholar 

  • Cozzarelli NR (1980) DNA gyrase and the supercoiling of DNA. Science 207:953–960

    Google Scholar 

  • Drlica K (1984) Biology of bacterial deoxyribunucleic acid topoisomerases. Microbiol Rev 48:273–289

    Google Scholar 

  • Drlica K, Coughlin S (1989) Inhibitors of DNA gyrase. Pharmacol Ther 44:107–121

    Google Scholar 

  • Drlica K, Franco RJ (1988) Inhibitors of DNA topoisomerases. Biochemistry 27:2253–2259

    Google Scholar 

  • Drlica K, Snyder M (1978) Superhelical Escherichia coli DNA: relaxation by coumermycin. J Mol Biol 120:145–154

    Google Scholar 

  • Dunlap PV (1984) The ecology and physiology of the light organ symbiosis between Photobacterium leiognathi and pony fishes. PhD Thesis, University of California, Los Angeles

  • Dunlap PV, Greenberg EP (1985) Control of Vibrio fischeri luminescence gene expression in Escherichi coli by cyclic AMP and cyclic AMP receptor protein. J Bacteriol 164:45–50

    Google Scholar 

  • Franco RJ, Drlica K (1989) Gyrase inhibitors can increase gyr A expression and DNA supercoiling. J Bacteriol 171:6573–6579

    Google Scholar 

  • Gellert M (1981) DNA topoisomerases. Annu Rev Biochem 50: 879–910

    Google Scholar 

  • Gellert M, Mizuuchi K, O'Dea MH, Nash HA (1976a) DNA gyrase: An enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci USA 73:3872–3876

    Google Scholar 

  • Gellert M, O'Dea MH, Itoh T, Tomizawa J-I (1976b) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 73:4474–4478

    Google Scholar 

  • Gellert M, Mizuuchi K, O'Dea MH, Itoh T, Tomizawa J-I (1977) Nalidixic acid resistance: A second genetic character involved in DNA gyrase. Proc Natl Acad Sci USA 74:4772–4776

    Google Scholar 

  • Hastings JW, Baldwin TO, Nicoli MZ (1978) Bacterial luciferase: assay purification and properties. Methods Enzymol 57:136–152

    Google Scholar 

  • Hastings JW, Potrikus CJ, Gupta S, Kurfurst M, Makemson HC (1985) Biochemistry and physiology of bioluminescent bacteria. Adv Microbiol Physiol 26:235–291

    Google Scholar 

  • Hastings JW, Makemson JC, Dunlap PV (1987) How are growth and luminescence regulated independently in exosymbionts? Smybiosis 4:3–24

    Google Scholar 

  • Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:569–584

    Google Scholar 

  • Jovanoivch S, Lebowitz J (1987) Estimation of the effect of coumermycin A1 on Salmonella typhimurium promoters by using random operon fusions. J Bacteriol 169:4431–4435

    Google Scholar 

  • Long BH, Stringfellow DA (1988) Inhibitors of topoisomerase II. Adv Enzyme Regul 27:223–256

    Google Scholar 

  • Mancini JA, Boylan M, Soly RR, Graham AF, Meighen EA (1988) Cloning and expression of the Photobacterium phosphoreum luminescence system demonstrates a unique lux gene organization. J Biol Chem 263:14308–14314

    Google Scholar 

  • Manes SH, Pruss GJ, Drlica K (1983) Inhibition of RNA synthesis by oxolinic acid is unrelated to average DNA supercoiling. J Bacteriol 155:420–423

    Google Scholar 

  • Martin M, Showalter R, Silverman M (1989) Identification of a locus controlling expression of luminescence genes in Vibrio harveyi. J Bacteriol 171:2406–2414

    Google Scholar 

  • Meighen EA (1988) Enzymes and genes from the lux operons of bioluminescent bacteria. Annu Rev Microbiol 42:151–176

    Google Scholar 

  • Mizuuchi K, Nash HA (1976) Restriction assay for integrative recombination of balcteriophage DNA in vitro: Requirement for closed circular DNA substrate. Proc Natl Acad Sci USA 73:3524–3528

    Google Scholar 

  • Nealson KH, Platt J, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322

    Google Scholar 

  • Pruss GJ, Drlica K (1989) DNA supercoiling and procaryotic transcription. Cell 56:521–523

    Google Scholar 

  • Pruss GJ, Franco RJ, Chevalier SG, Manes SH, Drlica K (1986) Effects of DNA gyrase inhibitors in Escherichia coli topoisomerase I mutants. J Bacteriol 168:276–282

    Google Scholar 

  • Puga A, Tessman I (1973) Mechanism of transcription of bacteriophage S13. II. Inhibition of phase-specific transcription by nalidixic acid. J Mol Biol 75:99–108

    Google Scholar 

  • Reichelt JL, Baumann P (1973) Taxonomy of marine luminous bacteria. Arch Microbiol 94:283–330

    Google Scholar 

  • Sinclair K (1965) Hydroxyurea: Differential lethal effects on cultured mammalian cells druing the cell cycle. Science 150:1729–1731

    Google Scholar 

  • Sugino A, Peebles CL, Kreuzer KN, Cozzarelli NR (1977) Mechanism of action of nalidixic acid: purification of Escherichia coli nal A gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc Natl Acad Sci USA 74:4767–4771

    Google Scholar 

  • Ulitzur S (1989) The regulatory control of the bacterial luminescence system — a new view. J Biolum Chemilum 4:317–325

    Google Scholar 

  • Ulitzur S, Kuhn J (1988) The transcription of bacterial luminescence is regulated by Sigma 32. J Biolum Chemilum 2:81–93

    Google Scholar 

  • Young CW, Hodas S (1964) Hydroxyurea: Inhibitory effect on DNA metabolism. Science 146:1172–1174

    Google Scholar 

  • Watanabe H, Hastings JW (1986) Expression of luminescence in Photobacterium phosphoreum: Na+ regulation of in vivo luminescence appearance. Arch Microbiol 145:342–346

    Google Scholar 

  • Watanabe H, Mimura N, Takimoto A, Nakamura T (1975) Luminescence and respiratory activities of Photobacterium phosphoreum. Competition for cellular reducing power. J Biochem 77:1147–1155

    Google Scholar 

  • Weiser I, Ulitzur S, Yannai S (1981) DNA-damaging agents and DNA-synthesis inhibitors induce luminescence in dark variants of luminous bacteria. Mutat Res 91:443–450

    Google Scholar 

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Author notes

  1. Haruo Watanabe

    Present address: Research Institute of Electric and Magnetic Alloys, Inaba Biophoton Project, Research Development Corporation of Japan, 2-1-1 Yagiyama-minami, Taihaku-ku, 982, Sendai, Japan

Authors and Affiliations

  1. Laboratory of Applied Botany, Department of Agricultural Biology, Faculty of Agriculture, Kyoto University, 606, Kyoto, Japan

    Haruo Watanabe

  2. Department of Cellular and Developmental Biology, Harvard University, 16 Divinity Avenue, 02138, Cambridge, MA, USA

    J. W. Hastings

Authors
  1. Haruo Watanabe
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  2. J. W. Hastings
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Watanabe, H., Hastings, J.W. Expression of bacterial luminescence is stimulated by nalidixic acid in a nalidixic acid resistant mutant. Arch. Microbiol. 154, 239–243 (1990). https://doi.org/10.1007/BF00248961

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  • DOI: https://doi.org/10.1007/BF00248961

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