Skip to main content

Growth on dichlorobiphenyls with chlorine substitution on each ring by bacteria isolated from contaminated African soils

Applied Microbiology and Biotechnology volume 74, pages 484–492 (2007)Cite this article

Abstract

Until recently, it was generally believed that the presence of more than one chlorine substituent prevented chlorinated biphenyls from serving as a sole source of carbon and energy for aerobic bacteria. In this study, we report the isolation of three aerobic strains, identified as Enterobacter sp. SA-2, Ralstonia sp. SA-4, and Pseudomonas sp. SA-6 from Nigerian polluted soils, that were able to grow on a wide range of dichlorobiphenyls (diCBs). In addition to growing on all monochlorobiphenyls (monoCBs), the strains were all able to utilize 2,2′-, 2,4′-, and 2,3-diCB as a sole source of carbon and energy. With the exception of strain SA-2, growth was also sustainable on 3,3′-, and 3,5-diCB. Washed benzoate-grown cells were typically able to degrade 68 to 100% of the diCB (100 ppm) within 188 h, concomitant with a cell number increase of up to three orders-of-magnitude and elimination of varying amounts of chloride. In many cases, stoichiometric production of a chlorobenzoate (CBA) as a product was observed. During growth on 2,2′-, and 2,4′-diCB, organisms exclusively attacked an o-chlorinated ring resulting in the production of 2-CBA and 4-CBA, respectively. A gradual decline in the concentration of the latter was observed, which suggested that the product was being degraded further. In the case of 2,3-diCB, the unsubstituted ring was preferentially metabolized. Initial diCB degradation rates were greatest for 2,4′-diCB (11.2 ± 0.91 to 30.3 ± 7.8 nmol/min per 109 cells) and lowest for 2,2′-diCB (0.37 ± 0.12 to 2.7 ± 1.2 nmol/min per 109 cells).

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Abraham W-R, Nogales B, Golyshin PN, Pieper DH, Timmis KN (2002) Polychlorinated biphenyl-degrading microbial communities in soils and sediments. Curr Opin Microbiol 5:246–253

    CAS  Article  Google Scholar 

  • Abramowicz DA (1990) Aerobic and anaerobic biodegradation of PCBs: a review. Crit Rev Biotechnol 10:241–251

    CAS  Article  Google Scholar 

  • Ahmed M, Focht DD (1973) Degradation of polychlorinated biphenyls by two species of Archromobacter. Can J Microbiol 19:47–52

    CAS  Article  Google Scholar 

  • Bedard DL (2001) Microbial dechlorination of PCBs in aquatic sediments. In: Robertson LW, Hansen LG (eds) PCBs: recent advances in environmental toxicology and health effects. The University Press of Kentucky, Lexington, pp 27–33

    Google Scholar 

  • Bedard DL, Wagner RE, Brennan MJ, Haberl ML, Brown JF Jr (1987) Extensive degradation of Aroclors and environmentally transformed polychlorinated biphenyls by Alcaligenes eutrophus H850. Appl Environ Microbiol 53:1094–1102

    CAS  Article  Google Scholar 

  • Bopp L (1986) Degradation of highly chlorinated PCBs by Pseudomonas strain LB400. J Ind Microbiol 1:23–29

    CAS  Article  Google Scholar 

  • Boyle AW, Silvin CJ, Hassett JP, Nakas JP, Tanenbaum SW (1992) Bacterial PCB degradation. Biodegradation 3:285–298

    CAS  Article  Google Scholar 

  • Bruhlmann F, Chen W (1999) Transformation of polychlorinated biphenyls by a novel BphA variant through the meta-cleavage pathway. FEMS Microbiol Lett 179:203–208

    CAS  Article  Google Scholar 

  • Dai S, Vaillancourt FH, Maroufi H, Druoin NM, Neau DB, Snieckus V, Nolin JT, Eltis LD (2002) Identification and analysis of a bottleneck in PCB degradation. Nat Struct Biol 9:934–939

    CAS  Article  Google Scholar 

  • Diaz E, Fernandez A, Prieto MA, Garcia JL (2001) Bioremediation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65:523–569

    CAS  Article  Google Scholar 

  • Floyd MM, Tang J, Kane M, Emerson D (2005) Captured diversity in a culture collection: case study of the geographic and habitat distributions of environmental isolates held at the American Type Culture Collection. Appl Environ Microbiol 71:2813–2823

    CAS  Article  Google Scholar 

  • Furukawa K, Matsumura F, Tonomura A (1978) Alcaligenes and Acinetobacter strains capable of degrading polychlorinated biphenyls. Agric Biol Chem 42:543–548

    CAS  Google Scholar 

  • Furukawa K, Tomizuka N, Kamibayashi A (1979) Effect of chlorine substitution on the bacterial metabolism of various polychlorinated biphenyls. Appl Environ Microbiol 38:301–310

    CAS  Article  Google Scholar 

  • Grindle N, Tyner JJ, Clay K, Fuqua C (2003) Identification of Arsenophonus-type bacteria from the dog tick Dermacentor variabilis. J Invertebr Pathol 83:264–266

    Article  Google Scholar 

  • Hickey WJ, Brenner V, Focht DD (1992) Mineralization of 2-chloro- and 2,5-dichlorobiphenyl by Pseudomonas sp. strain UCR2. FEMS Microbiol Lett 98:175–180

    CAS  Article  Google Scholar 

  • Juhasz AL, Naidu R (2000) Enrichment and isolation of non-specific aromatic degraders from unique uncontaminated (plant and faecal material) sources and contaminated soils. J Appl Microbiol 89:642–650

    CAS  Article  Google Scholar 

  • Kepner J, Raymond L, Pratt JR (1994) Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Microbiol Rev 58:603–615

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Picardal F (2000) A novel bacterium that utilizes monochlorobiphenyls and 4-chlorobenzoate as growth substrates. FEMS Microbiol Lett 185:225–229

    CAS  Article  Google Scholar 

  • Kim S, Picardal F (2001) Microbial growth on dichlorobiphenyls chlorinated on both rings as a sole carbon and energy source. Appl Environ Microbiol 76:1953–1955

    Article  Google Scholar 

  • Maltseva OV, Tsoi, TV, Quensen JF III, Fukuda M, Tiedje JM (2000) Degradation of anaerobic reductive dechlorination products of Aroclor 1242 by four aerobic bacteria. Biodegradation 10:363–371

    Article  Google Scholar 

  • Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  Article  Google Scholar 

  • Parsons JR, Sijm DTHM, van Laar A, Hutzinger O (1988) Biodegradation of polychlorinated biphenyls and benzoic acids by a Pseudomonas strain. Appl Microbiol Biotechnol 29:81–84

    CAS  Article  Google Scholar 

  • Potrawfke T, Lohnert T-H, Timmis KN Wittich R-M (1998) Mineralization of low-chlorinated biphenyls by Burkholderia sp. strain LB400 and by a two-membered consortium upon directed interspecies transfer of chlorocatechol pathway genes. Appl Microbiol Biotechnol 50:440–446

    CAS  Article  Google Scholar 

  • Safe S (1992) Toxicology, structure-function relationship, and human and environmental health impacts of polychlorinated biphenyls: progress and problems. Environ Health Perspect 100:259–268

    Article  Google Scholar 

  • Seah SYK, Labbe G, Nerdinger S, Johnson MR, Snieckus V, Eltis LD (2000) Identification of a serine hydrolase as a key determinant in the microbial degradation of polychlorinated biphenyls. J Biol Chem 275:15701–15708

    CAS  Article  Google Scholar 

  • Seah SYK, Labbe G, Kaschabek SR, Reifenrath F, Reineke W, Eltis, LD (2001) Comparative specificities of two evolutionarily divergent hydrolases involved in microbial degradation of polychlorinated biphenyls. J Bacteriol 183:1511–1516

    CAS  Article  Google Scholar 

  • Seeger M, Timmis KN, Hofer B (1995) Conversion of chlorobiphenyls into phenylhexadienoates and benzoates by the enzymes of the upper pathway for polychlorobiphenyl degradation encoded by the bph locus of Pseudomonas sp. strain LB400. Appl Environ Microbiol 61:2654–2658

    CAS  Article  Google Scholar 

  • Sondossi M, Sylvestre M, Ahmad D (1992) Effects of chlorobenzoate transformation on the Pseudomonas testosteroni biphenyl and chlorobiphenyl degradation pathway. Appl Environ Microbiol 58:485–495

    CAS  Article  Google Scholar 

  • Sondossi M, Barriault D, Sylvestre M (2004) Metabolism of 2,2′- and 3,3′-dihydroxybiphenyl by the biphenyl catabolic pathway of Comamonas testosterone B-356. Appl Environ Microbiol 70:174–181

    CAS  Article  Google Scholar 

  • Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    CAS  Article  Google Scholar 

  • Walia S, Tewari R, Brieger G, Thimm V, Mcguire T (1988) Biochemical and genetic characterization of soil bacteria degrading polychlorinated biphenyl. In: Abbou R, Korte F, Truhaut R (eds) Hazardous waste: detection, control, treatment. Elsevier, Amsterdam, pp 1621–1632

    Google Scholar 

  • Wiegel J, Wu QZ (2000) Microbial reductive dehalogenation of polychlorinated biphenyls. FEMS Microbiol Ecol 32:1–15

    CAS  Article  Google Scholar 

  • Yagi O, Sudo R (1980) Degradation of polychlorinated biphenyls by microorganisms. J Water Pollut Control Fed 52:1035–1043

    CAS  Google Scholar 

Download references

Acknowledgement

The first author was supported by a fellowship grant from the ICSC-World Laboratory, Lausanne, Switzerland with additional funding provided by School of Public and Environmental Affairs, Indiana University, Bloomington, IN, USA.

Author information

Affiliations

  1. Department of Botany and Microbiology, University of Lagos, Lagos, Nigeria

    Sunday A. Adebusoye, Matthew O. Ilori & Olukayode O. Amund

  2. Environmental Science Research Center, School of Public and Environmental Affairs, Indiana University, Bloomington, IN, 47405, USA

    Flynn W. Picardal

  3. Department of Biological Sciences, Indiana University, Bloomington, IN, 47405, USA

    Clay Fuqua & Nathan Grindle

Authors
  1. Sunday A. Adebusoye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Flynn W. Picardal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew O. Ilori
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olukayode O. Amund
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Clay Fuqua
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nathan Grindle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Flynn W. Picardal.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Adebusoye, S.A., Picardal, F.W., Ilori, M.O. et al. Growth on dichlorobiphenyls with chlorine substitution on each ring by bacteria isolated from contaminated African soils. Appl Microbiol Biotechnol 74, 484–492 (2007). https://doi.org/10.1007/s00253-006-0651-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-006-0651-8

Keywords

  • Polychlorinated biphenyls
  • PCBs
  • Biodegradation