Cometabolism of chlorinated solvents by nitrifying bacteria: Kinetics, substrate interactions, toxicity effects, and bacterial response

Biotechnology and Bioengineering

Volumn 54, Issue 6, 1997, Pages 520-534

  Ely, Roger L ^a,b   Williamson, Kenneth J ^a   Hyman, Michael R ^c   Arp, Daniel J ^c  

^a 1148 Kelley Engineering Center Corvallis   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

ammonia monooxygenase; biodegradation; cometabolism; nitrifying bacteria; Nitrosomonas europaea

Indexed keywords

BACTERIA; BIODEGRADATION; CHLORINE COMPOUNDS; CURVE FITTING; ENZYME INHIBITION; ENZYME KINETICS; MATHEMATICAL MODELS; METABOLISM; NITRIFICATION; OPTIMIZATION; SUBSTRATES; TOXICITY;

CHLORINATED SOLVENTS; COMETABOLISM; NITRIFYING BACTERIA;

ORGANIC SOLVENTS;

1,2 DICHLOROETHANE; AMMONIA; CARBON TETRACHLORIDE; CHLORINE DERIVATIVE; CHLOROFORM; SOLVENT; TRICHLOROETHYLENE; UNSPECIFIC MONOOXYGENASE; VINYLIDENE CHLORIDE;

ARTICLE; BACTERIAL METABOLISM; BIOREACTOR; CONTROLLED STUDY; ENZYME KINETICS; ENZYME SUBSTRATE; NITRIFICATION; NITROSOMONAS; NONHUMAN; TOXICITY TESTING;

EID: 0343581199     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0290(19970620)54:6<520::AID-BIT3>3.0.CO;2-L     Document Type: Article

References (77)

1. Alvarez-Cohen, L., McCarty, P. L. 1991a. A cometabolic biotransformation model for halogenated aliphatic compounds exhibiting product toxicity. Environ. Sci. Technol. 25(8): 1381-1387.
2. Alvarez-Cohen, L., McCarty, P. L. 1991b. Effects of toxicity, aeration, and reductant supply on trichloroethylene transformation by a mixed methanotrophic culture. Appl. Environ. Microbiol. 57(1): 228-235.
3. Alvarez-Cohen, L., McCarty, P. L. 1991c. Product toxicity and cometabolic inhibition modeling of chloroform and trichloroethylene transformation by methanotrophic resting cells. Appl. Environ. Microbiol. 57(4): 1031-1037.
4. Alvarez-Cohen, L., McCarty, P. L. 1991d. Two-stage dispersed growth treatment of halogenated aliphatic compounds by cometabolism. Environ. Sci. Technol. 25(8): 1387-1393.
5. Ames, G. F. L., Prody, C., Kustu, S. 1984. Simple, rapid, and quantitative release of periplasmic proteins by chloroform. J. Bacteriol. 160(3): 1181-1183.
6. Arciero, D., Vannelli, T., Logan, M., Hooper, A. B. 1989. Degradation of trichloroethylene by the ammonia-oxidizing bacterium Nitrosomonas europaea. Biochem. Biophys. Res. Commun. 159(2): 640-643.
7. Bailey, J. E., Ollis, D. F. 1986. Biochemical engineering fundamentals. McGraw-Hill, New York.
8. 4, and CO oxidation by methanotrophs and nitrifiers. Microbiol. Rev. 53(1): 68-84.
9. Blom, A., Harder, W., Matin, A. 1992. Unique and overlapping pollutant stress proteins of Escherichia coli. Appl. Environ. Microbiol. 58(1): 331-334.
10. Broholm, K., Christensen, T. H., Jensen, B. K. 1992. Modeling TCE degradation by a mixed culture of methane-oxidizing bacteria. Water Res. 26(9): 1177-1185.
11. Chang, H. L., Alvarez-Cohen, L. 1995. Transformation capacities of chlorinated organics by mixed cultures enriched on methane, propane, toluene, or phenol. Biotechnol. Bioeng. 45: 440-449.
12. Chang, M. K., Voice, T. C., Criddle, C. S. 1993. Kinetics of competitive inhibition and cometabolism in the biodegradation of benzene, toluene, and p-xylene by two Pseudomonas isolates. Biotechnol. Bioeng. 41: 1057-1065.
13. Colby, J., Stirling, D. I., Dalton, H. 1977. The soluble methane monooxygenase of Methylococcus capsulatus (Bath): Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds. Biochem. J. 165: 395-402.
14. Conover, W. J. 1980. Practical nonparametric statistics. Wiley, New York.
15. Cresteil, T., Beaune, P., Leroux, J. P., Lange, M., Mansuy, D. 1979. Biotransformation of chloroform by rat and human liver microsomes: In vitro effect on some enzyme activities and mechanism of irreversible binding to macromolecules. Chem. Biol. Interac. 24: 153-165.
16. Criddle, C. S. 1993. The kinetics of cometabolism. Biotechnol. Bioeng. 41: 1048-1056.
17. Dabrock, B., Riedel, J., Bertram, J., Gottschalk, G. 1992. Isopropylbenzene (cumene) - a new substrate for the isolation of trichloroethene-degrading bacteria. Arch. Microbiol. 158: 9-13.
18. Dolan, M. E., McCarty, P. L. 1994. Factors affecting transformation of chlorinated aliphatic hydrocarbons by methanotrophs, pp. 303-308. In: R. E. Hinchee, A. Leeson, L. Semprini, and S. K. Ong (eds.), Bioremediation of chlorinated and polycyclic aromatic hydrocarbon compounds. Lewis Publishers, Boca Raton, FL.
19. Dolan, M. E., McCarty, P. L. 1995. Methanotrophic chloroethene transformation capacities and 1,1-dichloroethene transformation product toxicity. Environ. Sci. Technol. 29(11): 2741-2747.
20. Ely, R. L., Williamson, K. J., Guenther, R. B., Hyman, M. R., Arp, D. J. 1995a. A cometabolic kinetics model incorporating enzyme inhibition, inactivation, and recovery. I. Model development, analysis, and testing. Biotechnol. Bioeng. 46: 218-231.
21. Ely, R. L., Hyman, M. R., Arp, D. J., Guenther, R. B., Williamson, K. J. 1995b. A cometabolic kinetics model incorporating enzyme inhibition, inactivation, and recovery. II. Trichloroethylene degradation experiments. Biotechnol. Bioeng. 46: 232-245.
22. Ewers, J., Freier-Schroder, D., Knackmuss, H. 1990. Selection of trichloroethene (TCE) degrading bacteria that resist inactivation by TCE. Arch. Microbiol. 154: 410-413.
23. Fersht, A. 1985. Enzyme structure and mechanism. W. H. Freeman, New York.
24. Folsom, B. R., Chapman, P. J., Pritchard, P. H. 1990. Phenol and trichloroethylene degradation by Pseudomonas cepacia G4: Kinetics and interactions between substrates. Appl. Environ. Microbiol. 56(5): 1279-1285.
25. Fox, B. G., Borneman, J. G., Wackelt, L. P., Lipscomb, J. D. 1990. Haloalkene oxidation by the soluble methane monooxygenase from Methylosinus trichosporium OB3b: Methanistic and environmental implications. Biochemistry 29(27): 6419-6427.
26. Gilbert, P. 1984. The revival of micro-organisms sublethally injured by chemical inhibitors, pp. 175-198. In: M. H. E. Andrew and A. D. Russell (eds.), The revival of injured microbes. Academic, London.
27. Gornall, A. G., Bardawill, C. J., David, M. M. 1949. Determination of serum proteins by means of the Biuret reaction. J. Biol. Chem. 177: 751-766.
28. Green, J., Dalton, H. 1989. Substrate specificity of soluble methane monooxygenase. J. Biol. Chem. 264(30): 17698-17703.
29. Guengerich, F. P. 1990. Enzymatic oxidation of xenobiotic chemicals. Crit. Rev. Biochem. Molec. Biol. 25(2): 97-153.
30. Guengerich, F. P., Strickland, T. W. 1977. Metabolism of vinyl chloride: Destruction of the heme of highly purified liver microsomal cytochrome P-450 by a metabolite. Mol. Pharmacol. 13: 993-1004.
31. Guengerich, F. P., Mason, P. S., Stott, W. T., Fox, T. R., Watanabe, P. G. 1981. Roles of 2-haloethane oxides and 2-haloacetaldehydes derived from vinyl bromide and vinyl chloride in irreversible binding to protein and DNA. Cancer Res. 41: 4391-4398.
32. Hanson, R. S., Tsien, H. C., Tsuji, K., Brusseau, G. A., Wackelt, L. P. 1990. Biodegradation of low-molecular-weight halogenated hydrocarbons by methanotrophic bacteria. FEMS Microbiol. Rev. 87: 273-278.
33. Harker, A. R., Kim, Y. 1990. Trichloroethylene degradation by two independent aromatic-degrading pathways in Alcaligenes eutrophus JMP134. Appl. Environ. Microbiol. 56(4): 1179-1181.
34. Henry, S. M., Grbic-Galic, D. 1991. Influence of endogenous and exogenous electron donors and trichloroethylene oxidation toxicity on trichloroethylene oxidation by methanotropic cultures from a groundwater aquifer. Appl. Environ. Microb. 57(1): 236-244.
35. Hopkins, G. D., Munakata, J., Semprini, L., McCarty, P. L. 1993. Trichloroethylene concentration effects on pilot field-scale in-situ groundwater bioremediation phenol-oxidizing microorganisms. Environ. Sci. Technol. 27(12): 2542-2547.
36. Hyman, M. R., Wood, P. M. 1983. Methane oxidation by Nitrosomonas europaea. Biochem. J. 212: 31-37.
37. Hyman, M. R., Sansome-Smith, A. W., Shears, J. H., Wood, P. M. 1985. A kinetic study of benzene oxidation to phenol by whole cells of Nitrosomonas europaea and evidence for the further oxidation of phenol to hydroquinone. Arch. Microbiol. 143: 302-306.
38. Hyman, M. R., Russell, S. A., Ely, R. L., Williamson, K. J., Arp, D. J. 1995. Inhibition, inactivation, and recovery of ammonia-oxidizing activity in cometabolism of trichloroethylene by Nitrosomonas europaea. Appl. Environ. Microbiol. 61(4): 1480-1487.
39. Janke, D., Ihn, W. 1989. Cometabolic turnover of aniline, phenol, and some of their monochlorinated derivatives by the Rhodococcus mutant strain AM 144. Arch. Microbiol. 152: 347-352.
40. Keenan, J. E., Strand, S. E., Stensel, H. D. 1994. Degradation kinetics of chlorinated solvents by a propane-oxidizing enrichment culture, pp. 1-13. In: R. E. Hinchee, A. Leeson, L. Semprini, and S. K. Ong (eds.), Bioremediation of chlorinated and polycyclic aromatic hydrocarbon compounds. Lewis Publishers, Boca Raton, FL.
41. Kohler, H.-P. E., Kohler-Staub, D., Focht, D. D. 1988. Cometabolism of polychlorinated biphenyls: Enhanced transformation of Arochlor 1254 by growing bacterial cells. Appl. Environ. Microbiol. 54(8): 1940-1945.
42. Lemaux, P. G., Herendeen, S. L., Bloch, P. L., Neidhart, F. C. 1978. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell. 13: 427-434.
43. Li, S., Wackelt, L. P. 1992. Trichloroethylene oxidation by toluene dioxygenase. Biochem. Biophys. Res. Comm. 185(1): 443-451.
44. Liebler, D. C., Guengench, F. P. 1983. Olefin oxidation by cytochrome P-450: Evidence for group migration in catalytic intermediates formed with vinylidene chloride and trans-1-phenyl-1-butene. Biochemistry 22: 5482-5489.
45. Little, C. D., Palumbo, A. V., Herbes, S. E., Lidstrom, M. E., Tyndall, R. L., Gilmer, P. J. 1988. Trichloroethylene biodegradation by a methane-oxidizing bacterium. Appl. Environ. Microbiol. 54(4): 951-956.
46. Little, C. D., Fraley, C. D., McCann, M. P., Matin, A. 1991. Use of bacterial stress promoters to induce biodegradation under conditions of environmental stress. In: R. E. Hinchee and R. F. Olfenbuttel (eds.), On-site bioreclamation processes for xenobiotic and hydrocarbon treatment. Butterworth-Heinemann, Stoneham, MS.
47. McCarty, P. L. 1971. Energetics and bacterial growth. In: S. Faust and J. Hunter (eds.), Organic compounds in aquatic environments. Marcel Dekker, New York.
48. McCarty, P. L. 1976. Stoichiometry of biological reactions. Prog. Wat. Tech. 7(1): 157-172.
49. Miller, R. E., Guengerich, F. P. 1983. Metabolism of trichloroethylene in isolated hepatocytes, microsomes, and reconstituted enzyme systems containing cytochrome P-450. Cancer Res. 43: 1145-1152.
50. Morimoto, R. I., Tissieres, A., Georgopoulos, C. 1990. The stress response, function of the proteins, and perspectives, pp. 1-36. In: R. I. Morimoto, A. Tissieres, and C. Georgopoulos (eds.), Stress proteins in biology and medicine. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
51. Oldenhuis, R., Vink, R. L. J. M., Janssen, D. B., Witholt, B. 1989. Degradation of chlorinated hydrocarbons by Methylosinus trichosporium OB3b expressing soluble methane monooxygenase. Appl. Environ. Microbiol. 55(11): 2819-2826.
52. Oldenhuis, R., Oedzes, J. Y., van der Waarde, J. J., Janssen, D. B. 1991. Kinetics of chlorinated hydrocarbon degradation by Methylosinus trichosporium OB3b and toxicity of trichloroethylene. Appl. Environ. Microbiol. 57(1): 7-14.
53. Oliver, J. D. 1993. Formation of viable but nonculturable cells, pp. 239-272. In: S. Kjelleberg (ed.), Starvation in bacteria. Plenum, New York.
54. Oritz de Montellano, P. R., Correia, M. A. 1983. Suicidal destruction of cytochrome P-450 during oxidative drug metabolism. Ann. Rev. Pharmacol. 23: 481-503.
55. Ortiz de Montellano, P. R., Reich, N. O. 1986. Inhibition of cytochrome P-450 enzymes. In: P. R. Ortiz de Montellano (ed.), Cytochrome P-450: Structure, mechanism, and biochemistry. Plenum, New York.
56. Ortiz de Monellano, P. R., Yost, G. S., Mico, B. A., Dinizo, S. E., Correia, M. A., Kumbara, H. 1979. Destruction of cytochrome P-450 by 2-isopropyl-4-pentenamide and methyl 2-isopropyl-pentenoate: Mass spectrometric characterization of prosthetic heme adducts and nonparticipation of epoxide metabolities. Arch. Biochem. Biophys. 197(2): 524-533.
57. Ortiz de Montellano, P. R., Beilan, H. S., Kunze, K. L., Mico, B. A. 1981. Destruction of cytochrome P-450 by ethylene. Structure of the resulting prosthetic heme adduct. J. Biol. Chem. 256(9): 4395-4399.
58. Ortiz de Montellano, P. R., Kunze, K. L., Beilan, H. L., Wheeler, C. 1982. Destruction of cytochrome P-450 by vinyl fluoride, fluroxene, and acetylene. Evidence for a radical intermediate in olefin oxidation. Biochemistry 21: 1331-1339.
59. Parsell, D. A., Lindquist, S. 1993. The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27: 437-496.
60. Patel, R., Hou, C., Laskin, A., Felix, A. 1982. Microbial oxidation of gaseous hydrocarbons: Properties of a soluble methane monooxygenase from a facultative methane-utilizing organism. Methylobacterium sp. Appl. Environ. Microbiol. 44(5): 1130-1137.
61. Pohl, L. R., Bhooshan, B., Whittaker, N. F., Krishna, G. 1977. Phosgene: A metabolite of chloroform. Biochem. Biophys. Res. Commun. 79(3): 684-691.
62. Press, W. H., Flannery, B. P., Teukolsky, S. A., Vetterling, W. T. 1989. Numerical recipes: The art of scientific computing (FORTRAN Version). Cambridge University Press, Cambridge.
63. Rasche, M. E., Hyman, M. R., Arp, D. J. 1991. Factors limiting aliphatic chlorocarbon degradation by Nitrosomonas europaea: Cometabolic inactivation of ammonia monooxygenase and substrate specificity. Appl. Environ. Microbiol. 57(10): 2986-2994.
64. Robinson, J. A. 1985. Determining microbial kinetic parameters using nonlinear regression analysis, pp. 61-114. In: K. C. Marshal (ed.), Advances in microbial ecology, vol. 8. Plenum, New York.
65. m, and the rate of endogenous substrate production (R) from the substrate depletion data. Microb. Ecol. 10: 165-178.
66. Robinson, J. A., Tiedje, J. M. 1983. Nonlinear estimation of Monod growth kinetic parameters from a single substrate depletion curve. Appl. Environ. Microbiol. 45(5): 1453-1458.
67. Russell, A. D. 1984. Potential sites of damage in micro-organisms exposed to chemical or physical agents, pp. 1-18. In: M. H. E. Andrew and A. D. Russell (eds.), The revival of injured microbes. Academic, London.
68. Semprini, L., Hopkins, G. D., Roberts, P. V., Grbic-Galic, D., McCarty, P. L. 1991. A field evaluation of in-situ biodegradation of chlorinated ethenes. Part 3, Studies in competitive inhibition. Ground Water 29: 239-250.
69. Semprini, L., Ely, R. L., Lang, M. M. Modeling of cometabolism for the in-situ biodegradation of trichloroethylene and other chlorinated aliphatic hydrocarbons. In: S. Sikdar and R. L. Irvine (eds.), Bioremediation principles and practices. Technomic Publishing, to appear.
70. Strand, S. E., Bjelland, M. D., Stensel, H. D. 1990. Kinetics of chlorinated hydrocarbon degradation by suspended cultures of methaneoxidizing bacteria. Res. J. Water Pollut. Control Fed. 62(2): 124-129.
71. Suzuki, I., Dular, U., Kwok, S. C. 1974. Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J. Bacteriol. 120(1): 556-558.
72. Vannelli, T., Logan, M., Arciero, D. M., Hooper, A. B. 1990. Degradation of halogenated aliphatic compounds by the ammonia-oxidizing bacterium Nitrosomonas europaea. Appl. Environ. Microbiol. 56(4): 1169-1171.
73. Wackett, L. P., Gibson, D. T. 1988. Degradation of trichloroethylene by toluene dioxygenase in whole-cell studies with Pseudomonas putida F1. Appl. Environ. Microbiol. 54(7): 1703-1708.
74. Wackett, L., Householder, S. 1989. Toxicity of trichloroethylene to Pseudomonas putida F1 is mediated by toluene dioxygenase. Appl. Environ. Microbiol. 55(10): 2723-2725.
75. Wackett, L. P., Brusseau, G. A., Householder, S. R., Hanson, R. S. 1989. Survey of microbial oxygenases: Trichloroethylene degradation by propane-oxidizing bacteria. Appl. Environ. Microbiol. 55(11): 2960-2964.
76. Weisburger, E.K. 1980. Metabolism and activation of chemical carcinogens. Mol. Cell. Biochem. 32: 95-104.
77. Zar, J. H. 1984. Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ.