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. 2002 Dec;110(Suppl 6):1005–1011. doi: 10.1289/ehp.02110s61005

Biodegradation kinetics of aromatic hydrocarbon mixtures by pure and mixed bacterial cultures.

Kenneth F Reardon 1, Douglas C Mosteller 1, Julia Bull Rogers 1, Nancy M DuTeau 1, Kee-Hong Kim 1
PMCID: PMC1241285  PMID: 12634132

Abstract

Microbial growth on pollutant mixtures is an important aspect of bioremediation and wastewater treatment. However, efforts to develop mathematical models for mixed substrate kinetics have been limited. Nearly all models group either the microbial population (as "biomass") or the chemical species (e.g., as biological oxygen demand). When individual chemical species are considered, most models assume either no interaction or that the nature of the interaction is competition for the same rate-limiting enzyme. And when individual microbial species are considered, simple competition for the growth substrate is the only interaction included. Here, we present results using Pseudomonas putida F1 and Burkholderia sp. strain JS150 growing individually and together on benzene, toluene, phenol, and their mixtures and compare mathematical models to describe these results. We demonstrate that the simple models do not accurately predict the outcome of these biodegradation experiments, and we describe the development of a new model for substrate mixtures, the sum kinetics with interaction parameters (SKIP) model. In mixed-culture experiments, the interactions between species were substrate dependent and could not be predicted by simple competition models. Together, this set of experimental and modeling results presents our current state of work in this area and identifies challenges for future modeling efforts.

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Selected References

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  1. Alvarez P. J., Vogel T. M. Substrate interactions of benzene, toluene, and para-xylene during microbial degradation by pure cultures and mixed culture aquifer slurries. Appl Environ Microbiol. 1991 Oct;57(10):2981–2985. doi: 10.1128/aem.57.10.2981-2985.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bartels I., Knackmuss H. J., Reineke W. Suicide Inactivation of Catechol 2,3-Dioxygenase from Pseudomonas putida mt-2 by 3-Halocatechols. Appl Environ Microbiol. 1984 Mar;47(3):500–505. doi: 10.1128/aem.47.3.500-505.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. COHEN-BAZIRE G., SISTROM W. R., STANIER R. Y. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol. 1957 Feb;49(1):25–68. doi: 10.1002/jcp.1030490104. [DOI] [PubMed] [Google Scholar]
  4. DuTeau N. M., Rogers J. D., Bartholomay C. T., Reardon K. F. Species-specific oligonucleotides for enumeration of Pseudomonas putida F1, Burkholderia sp. strain JS150, and Bacillus subtilis ATCC 7003 in biodegradation experiments. Appl Environ Microbiol. 1998 Dec;64(12):4994–4999. doi: 10.1128/aem.64.12.4994-4999.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Finette B. A., Subramanian V., Gibson D. T. Isolation and characterization of Pseudomonas putida PpF1 mutants defective in the toluene dioxygenase enzyme system. J Bacteriol. 1984 Dec;160(3):1003–1009. doi: 10.1128/jb.160.3.1003-1009.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Guha S., Peters C. A., Jaffé P. R. Multisubstrate biodegradation kinetics of naphthalene, phenanthrene, and pyrene mixtures. Biotechnol Bioeng. 1999 Dec 5;65(5):491–499. doi: 10.1002/(sici)1097-0290(19991205)65:5<491::aid-bit1>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  7. Haigler B. E., Pettigrew C. A., Spain J. C. Biodegradation of mixtures of substituted benzenes by Pseudomonas sp. strain JS150. Appl Environ Microbiol. 1992 Jul;58(7):2237–2244. doi: 10.1128/aem.58.7.2237-2244.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Harder W., Dijkhuizen L. Strategies of mixed substrate utilization in microorganisms. Philos Trans R Soc Lond B Biol Sci. 1982 Jun 11;297(1088):459–480. doi: 10.1098/rstb.1982.0055. [DOI] [PubMed] [Google Scholar]
  9. Irie S., Doi S., Yorifuji T., Takagi M., Yano K. Nucleotide sequencing and characterization of the genes encoding benzene oxidation enzymes of Pseudomonas putida. J Bacteriol. 1987 Nov;169(11):5174–5179. doi: 10.1128/jb.169.11.5174-5179.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klecka G. M., Gibson D. T. Inhibition of catechol 2,3-dioxygenase from Pseudomonas putida by 3-chlorocatechol. Appl Environ Microbiol. 1981 May;41(5):1159–1165. doi: 10.1128/aem.41.5.1159-1165.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lau P. C., Bergeron H., Labbé D., Wang Y., Brousseau R., Gibson D. T. Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. Gene. 1994 Aug 19;146(1):7–13. doi: 10.1016/0378-1119(94)90827-3. [DOI] [PubMed] [Google Scholar]
  12. Lendenmann U., Snozzi M., Egli T. Kinetics of the simultaneous utilization of sugar mixtures by Escherichia coli in continuous culture. Appl Environ Microbiol. 1996 May;62(5):1493–1499. doi: 10.1128/aem.62.5.1493-1499.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Liao Kai H., Dobrev Ivan D., Dennison James E., Jr, Andersen Melvin E., Reisfeld Brad, Reardon Kenneth F., Campain Julie A., Wei Wei, Klein Michael T., Quann Richard J. Application of biologically based computer modeling to simple or complex mixtures. Environ Health Perspect. 2002 Dec;110 (Suppl 6):957–963. doi: 10.1289/ehp.02110s6957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Menn F. M., Zylstra G. J., Gibson D. T. Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase in Pseudomonas putida F1. Gene. 1991 Jul 31;104(1):91–94. doi: 10.1016/0378-1119(91)90470-v. [DOI] [PubMed] [Google Scholar]
  15. Reardon K. F., Mosteller D. C., Bull Rogers J. D. Biodegradation kinetics of benzene, toluene, and phenol as single and mixed substrates for Pseudomonas putida F1. Biotechnol Bioeng. 2000 Aug 20;69(4):385–400. doi: 10.1002/1097-0290(20000820)69:4<385::aid-bit5>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  16. Reardon Kenneth F., Kim Kee-Hong. Two-dimensional electrophoresis analysis of protein production during growth of Pseudomonas putida F1 on toluene, phenol, and their mixture. Electrophoresis. 2002 Jul;23(14):2233–2241. doi: 10.1002/1522-2683(200207)23:14<2233::AID-ELPS2233>3.0.CO;2-B. [DOI] [PubMed] [Google Scholar]
  17. Rogers J. B., DuTeau N. M., Reardon K. F. Use of 16S-rRNA to investigate microbial population dynamics during biodegradation of toluene and phenol by a binary culture. Biotechnol Bioeng. 2000 Nov 20;70(4):436–445. [PubMed] [Google Scholar]
  18. Rogers J. B., Reardon K. F. Modeling substrate interactions during the biodegradation of mixtures of toluene and phenol by Burkholderia species JS150. Biotechnol Bioeng. 2000 Nov 20;70(4):428–435. doi: 10.1002/1097-0290(20001120)70:4<428::aid-bit8>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
  19. Saéz P. B., Rittmann B. E. Biodegradation kinetics of a mixture containing a primary substrate (phenol) and an inhibitory co-metabolite (4-chlorophenol). Biodegradation. 1993;4(1):3–21. doi: 10.1007/BF00701451. [DOI] [PubMed] [Google Scholar]
  20. Schmidt S. K., Alexander M. Effects of dissolved organic carbon and second substrates on the biodegradation of organic compounds at low concentrations. Appl Environ Microbiol. 1985 Apr;49(4):822–827. doi: 10.1128/aem.49.4.822-827.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Spain J. C., Gibson D. T. Oxidation of substituted phenols by Pseudomonas putida F1 and Pseudomonas sp. strain JS6. Appl Environ Microbiol. 1988 Jun;54(6):1399–1404. doi: 10.1128/aem.54.6.1399-1404.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Spain J. C., Zylstra G. J., Blake C. K., Gibson D. T. Monohydroxylation of phenol and 2,5-dichlorophenol by toluene dioxygenase in Pseudomonas putida F1. Appl Environ Microbiol. 1989 Oct;55(10):2648–2652. doi: 10.1128/aem.55.10.2648-2652.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Subramanian V., Liu T. N., Yeh W. K., Serdar C. M., Wackett L. P., Gibson D. T. Purification and properties of ferredoxinTOL. A component of toluene dioxygenase from Pseudomonas putida F1. J Biol Chem. 1985 Feb 25;260(4):2355–2363. [PubMed] [Google Scholar]
  24. Yeh W. K., Gibson D. T., Liu T. N. Toluene dioxygenase: a multicomponent enzyme system. Biochem Biophys Res Commun. 1977 Sep 9;78(1):401–410. doi: 10.1016/0006-291x(77)91268-2. [DOI] [PubMed] [Google Scholar]
  25. Yoon H., Klinzing G., Blanch H. W. Competition for mixed substrates by microbial populations. Biotechnol Bioeng. 1977 Aug;19(8):1193–1210. doi: 10.1002/bit.260190809. [DOI] [PubMed] [Google Scholar]
  26. Zylstra G. J., Gibson D. T. Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli. J Biol Chem. 1989 Sep 5;264(25):14940–14946. [PubMed] [Google Scholar]

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