1887

Abstract

Summary: The marine luminous bacterium , the species-specific light-organ symbiont of monocentrid (pinecone) fish, grew on 3′:5′-cyclic adenosine monophosphate (cAMP) as a sole source of carbon and energy, a capability not previously described in bacteria. In a minimal, chemically defined medium containing cAMP as the sole source of carbon and energy, cells grew more slowly than on glucose or ribose, but as quickly as on 5′-AMP. Expression of luminescence, which is dependent on cAMP in , was stimulated in cells grown on cAMP compared to cells grown on glucose or ribose. All strains of tested (MJ-1, B-61, ATCC 7744, MJ-A1, CG-A1) grew on cAMP, as did strains of two other marine luminous bacteria, and , and strains of the terrestrial enteric bacterium . Other tested species of marine luminous bacteria ( [] ) and terrestrial enteric bacteria (), which grew on 5′-AMP or ribose, did not grow on cAMP. Assays on intact cells and periplasmic extracts revealed that MJ-1 produced a periplasmic 3′:5′-cAMP phosphodiesterase (cAMP phosphodiesterase) of very high specific activity [9·0 μmol phosphate released (mg protein) min] and narrow substrate specificity (3′:5′-cAMP and 3′:5′-cGMP were attacked). The novel periplasmic location and unusually high activity of cAMP phosphodiesterase appear to account for the ability of this species to grow on cAMP. The periplasmic cAMP phosphodiesterase of night play a role in degrading free cAMP in seawater or in a cAMP-mediated aspect of the light organ symbiosis with monocentrid fish.

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1992-01-01
2021-08-03
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References

  1. ABOU M., BURGER M. 1971; Cyclic 3’ : 5’ adenosine monophosphate-phosphodiesterase and the release of catabolite repression of β-galactosidase by exogenous cyclic 3’: 5’ adenosine monophosphate in Escherichia coli . Biochemical and Biophysical Research Communications 43:174–182
    [Google Scholar]
  2. ACKERM R. S., COZZAREL N. R., EPSTEIN W. 1974; Accumulation of toxic concentrations of methylglyoxal by wild-type Escherichia coli K-12. Journal of Bacteriology 119:357–362
    [Google Scholar]
  3. ALPER M. D., AMES B. N. 1975; Cyclic 3’,5’-adenosine monophosphate phosphodiesterase mutants of Salmonella typhimur-ium . Journal of Bacteriology 122:1081–1090
    [Google Scholar]
  4. AMES G. F.-L., PRODY C., KUSTU S. 1984; Simple, rapid, and quantitative release of periplasmic proteins by chloroform. Journal of Bacteriology 160:1181–1183
    [Google Scholar]
  5. AMMERMAN J. W., AZAM F. 1981; Dissolved cyclic adenosine monophosphate (cAMP) in the sea and uptake of cAMP by marine bacteria. Marine Ecology Progress Series 5:85–89
    [Google Scholar]
  6. AMMERMAN J. W., AZAM F. 1982; Uptake of cyclic AMP by natural populations of marine bacteria. Applied and Environmental Microbiology 43:869–876
    [Google Scholar]
  7. AMMERMAN J. W., AZAM F. 1985; Bacterial 5’-nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227:1338–1340
    [Google Scholar]
  8. AMMERMAN J. W., AZAM F. 1987; Characteristics of cyclic AMP transport by marine bacteria. Applied and Environmental Microbiology 53:2963–2966
    [Google Scholar]
  9. ANDERSON B. M., KAHN D. W., ANDERSON C. D. 1985; Studies of the 2’: 3’-cyclic nucleotide phosphodiesterase of Haemophilus influenzae . Journal of General Microbiology 131:2041–2045
    [Google Scholar]
  10. ANRAKU Y. 1964A; A new cyclic phosphodiesterase having a 3’- nucleotidase activity from Escherichia coli B. I. Purification and some properties of the enzyme. Journal of Biological Chemistry 239:3412–3419
    [Google Scholar]
  11. ANRAKU Y. 1964b; A new cyclic phosphodiesterase having a 3’- nucleotidase activity from Escherichia coli B. II. Further studies on substrate specificity and mode of action of the enzyme. Journal of Biological Chemistry 239:3420–3424
    [Google Scholar]
  12. AZAM F., HODSON R. E. 1977 Dissolved ATP in the sea and its utilization by marine bacteria. Nature London ; 267696–698
    [Google Scholar]
  13. BAUMANN P., BAUMANN L. 1981 The marine Gram-negative eubacteria: Genera Photobacterium, Beneckea, Alteromonas, and Alcaligenes. In The Prokaryotes . A Handbook on Habitats, Isolation and Identification of Bacteria,1302–1331 Starr M. P., Stolp H., Truper H. G., Balows A., Schlegel H. G. New York: Springer-Verlag;
    [Google Scholar]
  14. BEACHAM I. R. 1979; Periplasmic enzymes in Gram-negative bacteria. European Journal of Biochemistry 10:877–883
    [Google Scholar]
  15. BEACHAM I. R., GARRETT S. 1980; Isolation of Escherichia coli mutants (cpdB) deficient in periplasmic 2’: 3’-cyclic phosphodiesterase and genetic mapping of the cpdB locus. Journal of General Microbiology 119:31–34
    [Google Scholar]
  16. BEACHAM I. R., KAHANA R., LEVY L., YAGIL E. 1973; Mutants of Escherichia coli K-12 ‘cryptic,’ or deficient in 5’-nucleotidase (uridine diphosphate-sugar hydrolase) and 3’-nucleotidase (cyclic phosphodiesterase activity). Journal of Bacteriology 116:957–964
    [Google Scholar]
  17. BEACHAM I. R., HAAS D., YAGIL E. 1977; Mutants of Escherichia coli ‘cryptic’ for certain periplasmic enzymes: evidence for an alteration of the outer membrane. Journal of Bacteriology 129:1034–1044
    [Google Scholar]
  18. BENGIS-GARBER C. 1985; Membrane-bound 5’-nucleotidase in marine luminous bacteria: biochemical and immunological properties. Canadian Journal of Microbiology 31:543–548
    [Google Scholar]
  19. BENGIS-GARBER C., KUSHNER D. J. 1982; Role of membranebound 5’-nucleotidase in nucleotide uptake by the moderate halophile Vibrio costicola . Journal of Bacteriology 149:808–815
    [Google Scholar]
  20. BOTSFORD J. L. 1981; Cyclic nucleotides in procaryotes. Microbiological Reviews 45:620–642
    [Google Scholar]
  21. BOTSFORD J. L. 1984; Cyclic AMP phosphodiesterase in Salmonella typhimurium: characteristics and physiological function. Journal of Bacteriology 160:826–830
    [Google Scholar]
  22. BRADFORD M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254
    [Google Scholar]
  23. BRANA H., CHYTIL F. 1966; Splitting of the cyclic 3’,5’-adenosine monophosphate in cell-free system of Escherichia coli . Folia Microbiologia 11:43–46
    [Google Scholar]
  24. BUETTNER M. J., SPITZ E., RICKENBERG H. V. 1973; Cyclic adenosine 3’,5’-monophosphate in Escherichia coli . Journal of Bacteriology 114:1068–1073
    [Google Scholar]
  25. CALCOTT P. H., CALVERT T. J. 1981; Characterization of 3’:5’- cyclic AMP phosphodiesterase in Klebsiella aerogenes and its role in substrate-accelerated death. Journal of General Microbiology 122:313–321
    [Google Scholar]
  26. CATANESE C. A., EMERICH D. W., ZAHLER W. L. 1989; Adenylate cyclase and cyclic AMP phosphodiesterase in Bradyrhizobium japonicum bacteroids. Journal of Bacteriology 171:4531–4536
    [Google Scholar]
  27. CHEUNG W. Y. 1971; Cyclic 3’,5’-nucleotide phosphodiesterase. Journal of Biological Chemistry 246:2859–2869
    [Google Scholar]
  28. DAVIS R. W., BOTSTEIN D., ROTH J. R. 1980 Advanced Bacterial Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. DE ROBERTIS E. M., JR, JUDEWICZ N. D., TORRES H. N. 1973; On the control mechanism of bacterial growth by cyclic adenosine 3’,5’- monophosphate. Biochemical and Biophysical Research Communications 55:758–764
    [Google Scholar]
  30. DEVREOTES P. 1989; Dictyostelium discoideum: a model system for cell-cell interactions in development. Science 245:1054–1058
    [Google Scholar]
  31. DUNLAP P. V. 1985; Osmotic control of luminescence and growth in Photobacterium leiognathi from ponyfish light organs. Archives of Microbiology 141:44–50
    [Google Scholar]
  32. DUNLAP P. V. 1989; Regulation of luminescence by cyclic AMP in cya-like and crp-like mutants of Vibrio fischeri . Journal of Bacteriology 171:1199–1202
    [Google Scholar]
  33. DUNLAP P. V., GREENBERG E. P. 1985; Control of Vibrio fischeri luminescence gene expression in Escherichia coli by cyclic AMP and cyclic AMP receptor protein. Journal of Bacteriology 164:45–50
    [Google Scholar]
  34. DUNLAP P. V., GREENBERG E. P. 1988; Control of Vibrio fischeri lux gene transcription by a cyclic AMP receptor protein- LuxR protein regulatory circuit. Journal of Bacteriology 170:4040–4046
    [Google Scholar]
  35. DUNLAP P. V., GREENBERG E. P. 1991 The role of intercellular chemical communication in the Vibrio fischeri-monocentrid fish symbiosis. In Microbial Cell-Cell Interactions219–253 Dworkin M. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  36. DUNLAP P. V., RAY J. M. 1989; Requirement for autoinducer in transcriptional negative autoregulation of the Vibrio fischeri luxR gene in Escherichia coli . Journal of Bacteriology 171:3549–3552
    [Google Scholar]
  37. EBERHARD A. 1972; Inhibition and activation of bacterial luciferase synthesis. Journal of Bacteriology 109:1101–1105
    [Google Scholar]
  38. FISKE C. H., SUBBAROW Y. 1925; The colorimetric determination of phosphorus. Journal of Biological Chemistry 66:375–400
    [Google Scholar]
  39. FRANCKO D. A. 1983 Cyclic AMP in photosynthetic organisms: recent developments. In Advances in Cyclic Nucleotide Research97–117 Greengard P., Robison G. A. New York: Raven Press;
    [Google Scholar]
  40. FRANCKO D. A. 1989; Uptake, metabolism, and release of cAMP in Selenastrum capricomutum (Chlorophyceae). Journal of Phycology 25:300–304
    [Google Scholar]
  41. FRIEDRICH W. F., GREENBERG E. P. 1983; Glucose repression of luminescence and luciferase in Vibrio fischeri . Archives of Microbiology 134:87–91
    [Google Scholar]
  42. FUKASAWA S., DUNLAP P. V., BABA M., OSUMI M. 1987; Identification of an agar-digesting, luminous bacterium. Agricultural and Biological Chemistry 51:265–268
    [Google Scholar]
  43. GERBER L., NEUBAUER D. G., STUTZENBERGER F. J. 1987; Cyclic AMP phosphodiesterase in Thermomospora curvata . Journal of Bacteriology 169:2267–2271
    [Google Scholar]
  44. GULLETTA E., CAPUTO G., MACCHIA V. 1979; Cyclic 3’,5’- adenosine monophosphate phosphodiesterase in mutants of Escherichia coli altered in cAMP metabolism. Bulletin of Molecular Biology and Medicine 4:80–89
    [Google Scholar]
  45. HATCH T. P., AL-HOSSAINY E., SILVERMAN J. A. 1982; Adenine nucleotide and lysine transport in Chlamydia psittaci . Journal of Bacteriology 150:662–670
    [Google Scholar]
  46. HAYGOOD M. G., NEALSON K. H. 1985; Mechanisms of iron regulation of luminescence in Vibrio fischeri . Journal of Bacteriology 162:209–216
    [Google Scholar]
  47. IDE M., YOSHIMOTO A., OKABAYSHI T. 1967; Formation of adenosine cyclic 3’,5’phosphate by nonproliferating cells and cell- free extract of Brevibacterium liquefaciens . Journal of Bacteriology 94:317–322
    [Google Scholar]
  48. ITAMI H., SAKAI Y., SHIMAMOTO T., HAMA H., TSUDA M., TSUCHIYA T. 1989; Purification and characterization of membrane-bound 5’-nucleotidase of Vibrio parahaemolyticus . Journal of Biochemistry 105:785–789
    [Google Scholar]
  49. IUCHI S., KUBOTA Y., TANAKA S. 1975; Mutants defective in binding activity for cyclic adenosine 3’,5’-monophosphate in Vibrio parahaemolyticus . Journal of Bacteriology 124:567–569
    [Google Scholar]
  50. JUDEWICZ N. D., DE ROBERTIS E. M. JR., TORRES H. N. 1973; Inhibition of Escherichia coli growth by cyclic adenosine 3’,5’- monophosphate. Biochemical and Biophysical Research Communica-tions 52:1257–1262
    [Google Scholar]
  51. LEE C. H. 1978; 3’:5’-Cyclic nucleotide phosphodiesterase of Mycobacterium smegmatis . Journal of General Microbiology 107:177–181
    [Google Scholar]
  52. MAKEMSON J. C., HASTINGS J. W. 1982; Iron represses bioluminescence and affects catabolite repression in Vibrio harveyi . Current Microbiology 7:181–186
    [Google Scholar]
  53. MATIN A., MATIN M. K. 1982; Cellular levels, excretion, and synthesis rates of cyclic AMP in Escherichia coli grown in continuous culture. Journal of Bacteriology 149:801–807
    [Google Scholar]
  54. MIDDLEBROOK J. L., DORLAND R. B. 1984; Bacterial toxins: cellular mechanisms of action. Microbiological Reviews 48:199–221
    [Google Scholar]
  55. MONARD D., JANECEK J., RICKENBERG H. V. 1969; The enzymatic degradation of 3’,5’ cyclic AMP in strains of Escherichia coli sensitive and resistant to catabolite repression. Biochemical and Biophysical Research Communications 35:584–591
    [Google Scholar]
  56. NEALSON K. H. 1977; Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Archives of Microbiology 112:73–79
    [Google Scholar]
  57. NEALSON K. H. 1978; Isolation, identification, and manipulation of luminous bacteria. Methods in Enzymology 57:153–166
    [Google Scholar]
  58. NEALSON K. H. 1979; Alternative strategies of symbiosis of marine luminous fishes harboring light-emitting bacteria. Trends in Biochemical Science 4:105–110
    [Google Scholar]
  59. NEU H. C. 1967; The 5’-nucleotidase of Escherichia coli. I. Purification and properties. Journal of Biological Chemistry 242:3896–3904
    [Google Scholar]
  60. NEU H. C. 1968; The 5’-nucleotidases and cyclic phosphodiesterases (3’-nucleotidases) of the Enterobacteriaceae . Journal of Bacteriology 95:1732–1737
    [Google Scholar]
  61. NEUHARD J., NYGAARD P. 1987 Purines and pyrimidines. In Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology445–473 Neidhart F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  62. NIELSEN L. D., MONARD D., RICKENBERG H. V. 1973; Cyclic 3,5’- adenosine monophosphate phosphodiesterase of Escherichia coli . Journal of Bacteriology 116:857–866
    [Google Scholar]
  63. OKABAYASHI T., IDE M. 1970a; Cyclic 3’,5’-nucleotide phosphodiesterase of Serratia marcescens . Biochimica et Biophysica Acta 220:116–123
    [Google Scholar]
  64. OKABAYASHI T., IDE M. 1970b; Effect of dipicolinic acid on bacterial cyclic 3’,5’-nucleotide phosphodiesterase. Biochimica et Biophysica Acta 220:124–126
    [Google Scholar]
  65. OKADA Y. K. 1926; On the photogenic organ of the knight-fish Monocentris japonicus (Houttuyn). Biological Bulletin 50:365–373
    [Google Scholar]
  66. PASTAN I., ADHYA S. 1976; Cyclic adenosine 5’-monophosphate in Escherichia coli . Bacteriological Reviews 40:527–551
    [Google Scholar]
  67. REICHELT J. L., BAUMANN P. 1973; Taxonomy of marine, luminous bacteria. Archiv fur Mikrobiologie 94:283–330
    [Google Scholar]
  68. RIVERA R. P., BOTSFORD J. L. 1981; Cyclic 3’: 5’-adenosine monophosphate phosphodiesterase activity in Klebsiella pneumoniae . FEMS Microbiology Letters 10:147–149
    [Google Scholar]
  69. ROBISON G. A., BUTCHER R. W., SUTHERLAND E. W. 1971 Cyclic AMP. New York: Academic Press;
    [Google Scholar]
  70. RUBY E. G., MORIN J. G. 1978; Specificity of symbiosis between deep-sea fish and psychrotrophic luminous bacteria. Deep-Sea Research 25:161–171
    [Google Scholar]
  71. RUBY E. G., NEALSON K. H. 1976; Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica: a model of symbiosis based on bacterial studies. Biological Bulletin 151:574–586
    [Google Scholar]
  72. RUBY E. G., MCCABE J. B., BARKE J. I. 1985; Uptake of intact nucleoside monophosphates by Bdellovibrio bacteriovorus 109J. Journal of Bacteriology 163:1087–1094
    [Google Scholar]
  73. SAIER M. H., FEUCHT B. U., MCCAMAN M. T. 1975; Regulation of intracellular adenosine cyclic 3’: 5’-monophosphate levels in Escherichia coli and Salmonella typhimurium. Evidence for energy-dependent excretion of the cyclic nucleotide. Journal of Biological Chemistry 250:7593–7601
    [Google Scholar]
  74. SAKAI Y., TODA K., MITANI Y., TSUDA M., SHINODA S., TSUCHIYA T. 1987; Properties of the membrane-bound 5’-nucleotidase and utilization of extracellular ATP in Vibrio parahaemolyticus . Journal of General Microbiology 133:2751–2757
    [Google Scholar]
  75. SILHAVY T. I., BERMAN M. L., ENQUIST L. W. 1984 Experiments in Gene Fusions Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  76. TAMMINEN T. 1989; Dissolved organic phosphorus regeneration by bacterioplankton: 5’-nucleotidase activity and subsequent phosphate uptake in a mesocosm enrichment experiment. Marine Ecology Progress Series 58:89–100
    [Google Scholar]
  77. TEBO B. M., LINTHICUM D. S., NEALSON K. H. 1979; Luminous bacteria and light emitting fish: ultrastructure of the symbiosis. BioSystems 11:269–280
    [Google Scholar]
  78. UERKVITZ W., BECK C. F. 1981; Periplasmic phosphatases in Salmonella typhimurium LT2. A biochemical, physiological, and partial genetic analysis of three nucleoside monophosphate dephosphorylating enzymes. Journal of Biological Chemistry 256:382–389
    [Google Scholar]
  79. ULLMANN A., DANCHIN A. 1983 Role of cyclic AMP in bacteria. In Advances in Cyclic Nucleotide Research 151–52 Greengard P., Robison G. A. New York: Raven Press;
    [Google Scholar]
  80. UNEMOTO T., HAYASHI M., KOZUKA Y., HAYASHI M. 1978 Localizations of salt modifications of phosphohydrolases in slightly halophilic Vibrio alginolyticus . In Effect of the Ocean Environment on Microbial Activities46–71 Colwell R. R., Morita R. Y. Baltimore: University Park Press;
    [Google Scholar]
  81. WINKLER H. H. 1976; Rickettsial permeability. An ADP-ATP transport system. Journal of Biological Chemistry 251:389–396
    [Google Scholar]
  82. WINKLER U., SCHOLLE H., BOHNE L. 1975; Mutants of Serratia marcescens lacking cyclic nucleotide phosphodiesterase activity and requiring cyclic 3’,5’-AMP for the utilization of various carbohydrates. Archives of Microbiology 104:189–196
    [Google Scholar]
  83. YAGIL E., BEACHAM I. R. 1975; Uptake of adenosine 5’- monophosphate by Escherichia coli . Journal of Bacteriology 121:401–405
    [Google Scholar]
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