Skip to main content
SpringerLink
Log in

Substituent effects on the oxidation of substituted biphenyl congeners by type II methanotroph strain CSC1

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The oxidation potential of type II groundwater methanotroph, strain CSC1, expressing soluble methane monooxygenase, was measured in the presence of 10 ortho-substituted biphenyls with varying electronics, sterics, and hydrophobicity character for comparison with type II Methylosinus trichosporium OB3b. Strain CSC1 showed faster rates with all compounds tested, with the exception of 2-nitrobiphenyl, 2-hydroxybiphenyl, and 2-aminobiphenyl. Products of oxidation observed upon incubation of strain CSC1 with biphenyl and 2-hydroxybiphenyl were hydroxylated biphenyls that revealed less preference for the para position and different dihydroxylation positions, respectively, in comparison to those observed with M. trichosporium OB3b. Only the intramolecular hydrogen migration, or NIH-shift, product was observed in the case of 2-chlorobiphenyl, whereas M. trichosporium OB3b yielded a variety of chlorohydroxybiphenyls. Quantitative structure–biodegradation relationships constructed with the maximum observed oxygen uptake rates as a dependent variable and a variety of descriptors showed an influence of substituent electronic character on the oxidation activity of strain CSC1. However, compound hydrophobicity and not compound size, as was observed with M. trichosporium OB3b, was shown to influence rates to a greater extent. This suggests that transport of the compound through the cell membrane and to the sMMO active site is rate-determining for strain CSC1.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adriaens P (1994) Evidence for chlorine migration during oxidation of 2-chlorobiphenyl by a Type II methanotroph. Appl Environ Microbiol 60:1658–1662

    Google Scholar 

  • Adriaens P, Grbić-Galić D (1994) Cometabolic transformation of mono- and dichlorobiphenyls and chlorohydroxybiphenyls by methanotrophic groundwater isolates. Environ Sci Technol 28:1325–1330

    Google Scholar 

  • Banerjee S, Howard PH, Rosenberg AM, Dombrowski AE, Sikka H, Tullis DL (1984) Development of a general kinetic model for biodegradation and its application to chlorophenols and related compounds. Environ Sci Technol 18:416–422

    Google Scholar 

  • Bowman J (2000) The methanotrophs: the families Methylococcaceae and Methylocystaceae. In: Dworkin M, et al (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer , Berlin Heidelberg New York, release 3.1., http://link.springerny.com/link/service/books/10125/.

  • Bowman JP, Sayler GS (1994) Maximization of Methylosinus trichosporium OB3b soluble methane monooxygenase production in batch culture. Biodegradation 5:1–11

    Google Scholar 

  • Bowman JP, Sly LI, Nichols PD, Hayward AC (1993) Revised taxonomy of the methanotrophs: description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43:735–753

    Google Scholar 

  • Brigmon R (2002) Methanotrophic bacteria: use in bioremediation. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York, pp 1936–1944

    Google Scholar 

  • Brusseau GA, Tsien H-C, Hanson RS, Wackett LP (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase. Biodegradation 1:19–29

    Google Scholar 

  • Burrows KKJ, Cornish A, Scott D, Higgins IJ (1984) Substrates specificities of the soluble and particulate methane mono-oxygenases of Methylosinus trichosporium OB3b. J Gen Microbiol 130:3327–3333

    Google Scholar 

  • Choi D-W, Kunz RC, Boyd ES, Semrau JD, Antholine WA, Han J-I, Zahn JA, Boyd JM, del la Mora AM, DiSpirito AA (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase from Methylococcus capsulatus Bath. J Bacteriol 185:5755–5764

    Google Scholar 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    Google Scholar 

  • Dalton H, Golding BT, Waters BW, Higgins R, Taylor JA (1981) Oxidations of cyclopropane, methylcyclopropane, and arenes with the mono-oxygenase system from Methylococcus capsulatus. J Chem Soc Chem Commun 10:482–483

    Google Scholar 

  • Dalton H, Wilkins PC, Jiang Y (1993) Structure and mechanism of action of the hydroxylase of soluble methane monooxygenase. In: Murrell JC, Kelly DP (eds) Microbial growth on C1 compounds. Intercept, Andover, pp 65–80

    Google Scholar 

  • Damborsky J, Manova K, Kuty M (1996) A mechanistic approach to deriving quantitative structure biodegradability relationships. In: Peijnenburg WJGM, Damborsky J (eds) Biodegradability prediction. Kluwer, Dordrecht, pp 75–92

    Google Scholar 

  • Dearden JC, Nicholson RM (1987) Correlation of biodegradability with atomic charge difference and superdelocalizability. In: Kaiser KLE (ed) QSAR in environmental toxicology-II. D Reidel, Dordrecht, pp 83–89

    Google Scholar 

  • DiSpirito A, Gulledge J, Shiemke AK, Murrell JC, Lidstrom ME, Krema CL (1992) Trichloroethylene oxidation by the membrane-associated methane monooxygenase in type I, type II, and type X methanotrophs. Biodegradation 2:151–164

    Google Scholar 

  • Eriksson L, Johansson E, Wold S (1997) Quantitative structure–activity relationship model validation. In: Chen F, Schuurmann G (eds) Quantitative structure–activity relationships in environmental sciences-VII. Setac, Pensacola, pp 381–397

    Google Scholar 

  • Eriksson L, Jaworska J, Worth AP, Cronin MTD, McDowell RM, Gramatica P (2003) Methods for reliability and uncertainty assessment and for applicability evaluations of classification- and regression-based QSARs. Environ Health Perspect 111:1361–1375

    Google Scholar 

  • Foresman JB, Frisch A (1996) Exploring chemistry with electronic structure methods, 2nd edn. Gaussian, Pittsburgh

    Google Scholar 

  • Gaussian 94 software (revision A.1) (1996) Gaussian, Pittsburgh

  • Green J, Dalton H (1989) Substrate specificity of soluble methane monooxygenase–mechanistic implications. J Biol Chem 264:17698–17708

    Google Scholar 

  • Grosse S, Laramee L, Wendlandt K-D, McDonald IR, Miguez CB, Kleber H-P (1999) Purification and characterization of the soluble methane monooxygenase of the type II methanotrophic bacterium. Methylocystis sp. strain WI 14. Appl Environ Microbiol 65:3929–3935

    Google Scholar 

  • Hansch C, Caldwell J (1991) The structure–activity relationship of inhibitors of serotonin uptake and receptor binding. J Comput Aided Mol Des 5:441–453

    Google Scholar 

  • Hansch C, Leo A, Hoekman D (1995) Exploring QSAR: hydrophobic, electronic, and steric constants, ACS Professional Reference Book. American Chemical Society, Washington

    Google Scholar 

  • Henry SM, Grbić-Galić D (1990) Effect of mineral media on trichloroethylene oxidation by aquifer methanotrophs. Microb Ecol 20:151–169

    Google Scholar 

  • Hermens J, Balaz S, Damborsky J, Karcher W, Muller M, Peijnenburg W, Sabljic A, Sjostrom M (1995) Assessment of QSARs for predicting fate and effects of chemicals in the environment: an international European project. SAR QSAR Environ Res 3:223–236

    Google Scholar 

  • Hršak D (1996) Cometabolic transformation of linear alkylbenzenesulphonates by methanotrophs. Water Res 30:3092–3098

    Google Scholar 

  • Jezequel SG, Higgins IJ (1983) Mechanistic aspects of biotransformations by the monooxygenase systems of Methylosinus trichosporium OB3b. J Chem Tech Biotechnol 33B:139–144

    Google Scholar 

  • Kitson FG, Larsen BS, McEwen CN (1996) Gas chromatography and mass spectrometry: a practical guide. Academic, San Diego

    Google Scholar 

  • Kohler H-PE, Kohler-Staub D, Focht DD (1988) Degradation of 2-hydroxybiphenyl and 2,2′-dihydroxybiphenyl by Pseudomonas sp. strain HBP1. Appl Environ Microbiol 54:2683–2688

    Google Scholar 

  • Kohler H-PE, van der Maarel MJEC, Kohler-Staub D (1993) Selection of Pseudomonas sp. strain HBP1 Prp for metabolism of 2-propylphenol and elucidation of the degradative pathway. Appl Environ Microbiol 59:860–866

    Google Scholar 

  • Lindner AS, Adriaens P, Semrau JD (2000) Transformation of ortho-substituted biphenyls by Methylosinus trichosporium OB3b: substituent effects on oxidation kinetics and product formation. Arch Microbiol 174:35–41

    Google Scholar 

  • Lindner AS, Whitfield C, Chen N, Semrau JD, Adriaens P (2003) Quantitative structure–biodegradation relationships for ortho-substituted biphenyl compounds oxidized by Methylosinus trichosporium OB3b. Environ Toxicol Chem 22:2251–2257

    Google Scholar 

  • Lontoh S, DiSpirito AA, Semrau JD (1999) Dichloromethane and trichloroethylene inhibition of methane oxidation by the membrane-associated methane monooxygenase of Methylosinus trichosporium OB3b. Arch Microbiol 171:301–308

    Google Scholar 

  • Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. Wiley, New York

    Google Scholar 

  • Parsons JR, Opperhuizen A, Hutzinger O (1987) Influence of membrane permeation on biodegradation kinetics of hydrophobic compounds. Chemosphere 16:1361–1370

    Google Scholar 

  • Prior SD, Dalton H (1985) The effect of copper ions on membrane content and methane monooxygenase activity in methanol-grown cells of Methylococcus capsulatus (Bath). J Gen Microbiol 131:155–163

    Google Scholar 

  • Reeburgh WS (1996) Soft spots in the global methane budget. In: Lidstrom ME, Tabita FR (eds) Microbial growth on C1 compounds. Kluwer, Dordrecht, pp 334–342

    Google Scholar 

  • Shu L, Nesheim JC, Kauffmann K, Munck E, Lipscomb JD, Que L Jr (1997) An Fe2(IV)O2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 275:515–518

    Google Scholar 

  • Stanley SH, Prior SD, Leak DJ, Dalton H (1983) Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. Biotech Lett 5:487–492

    Google Scholar 

  • Taylor JK (1990) Statistical techniques for data analysis. Lewis, Boca Raton

    Google Scholar 

  • Topliss JG, Edwards RP (1979) Chance factors in studies of quantitative structure–activity relationships. J Med Chem 22:1238–1244

    Google Scholar 

  • Uchiyama H, Nakajima T, Yagi O, Tabuchi T (1989) Aerobic degradation of trichloroethylene by a new type II methane-utilizing bacterium, strain M. Agric Biol Chem 53:2903–2907

    Google Scholar 

  • Wilkins PC, Dalton H, Samuel CJ, Green J (1994) Further evidence for multiple pathways in soluble methane-monooxygenase-catalyzed oxidation from the measurement of deuterium kinetic isotope effects. Eur J Biochem 226:555–560

    Google Scholar 

Download references

Acknowledgements

We would like to thank Ms. Adriana Pacheco, a graduate research assistant in the Department of Environmental Engineering Sciences at the University of Florida, for her assistance in the laboratory. We wish to thank Dr. Ning Chen of ChemTrace in Fremont, Calif., for performing the Gaussian ab initio analysis. Fellowships to Angela S. Lindner from the NIH Cellular Biotechnology Training Program (grant 2T32GM08353-06) and the American Association of University Women are gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Environmental Engineering Sciences, University of Florida, A.P. Black Hall, P.O. Box 116450, Gainesville, FL, 32611-6450, USA

    A. S. Lindner

  2. Department of Civil and Environmental Engineering, University of Michigan, 1351 Beal Ave., Suite 181, Ann Arbor, MI, 48109-2125, USA

    J. D. Semrau & P. Adriaens

Authors
  1. A. S. Lindner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. D. Semrau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Adriaens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. S. Lindner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lindner, A.S., Semrau, J.D. & Adriaens, P. Substituent effects on the oxidation of substituted biphenyl congeners by type II methanotroph strain CSC1. Arch Microbiol 183, 266–276 (2005). https://doi.org/10.1007/s00203-005-0769-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-005-0769-6

Keywords

Search

Navigation