Advertisement

World Journal of Microbiology and Biotechnology

, Volume 29, Issue 8, pp 1461–1471 | Cite as

Use of a glass bead-containing liquid medium for efficient production of a soil-free culture with polychlorinated biphenyl-dechlorination activity

  • Daisuke SuzukiEmail author
  • Daisuke Baba
  • Velayudhan Satheeja Santhi
  • Robinson David Jebakumar Solomon
  • Arata Katayama
Original Paper

Abstract

We established a soil-free culture capable of dechlorinating polychlorinated biphenyls (PCBs) in Kanechlor-300 and Kanechlor-400 by establishing a PCB-dechlorinating soil culture in liquid medium containing 0.5 mm glass beads. PCB-dechlorination activity in liquid cultures with glass beads appeared to depend on the size of the glass beads, and soil-free cultures with 0.05-, 1.0- or 2.0 mm glass beads did not dechlorinate PCBs. Soil-free culture without glass beads also failed to dechlorinate PCBs. The soil-free culture containing 0.5 mm glass beads dechlorinated 42.6 ± 12.0 mol% in total PCBs. This soil-free culture was more effective than soil culture for dechlorinating PCBs ranging from dichlorinated PCBs to tetrachlorinated PCBs. Clone analysis of the 16S rRNA gene sequences showed that one of the predominant groups of microorganisms in the soil-free culture comprised heat-tolerant and spore-forming bacteria from the phylum Firmicutes. Heat treatment (100 °C, 10 min) did not destroy the PCB-dechlorination activity of the soil-free culture with glass beads. These results suggest that unknown species of the phylum Firmicutes were involved in PCB dechlorination in the soil-free culture. In this study, we succeeded in using a liquid medium containing glass beads as an inorganic soil substitute and showed that such a medium enhances PCB-dechlorination activity. Our study provides valuable information for developing PCB-bioremediation techniques using dechlorinating bacteria in anoxic contaminated soils and sediments.

Keywords

Polychlorinated biphenyls Dechlorination Glass beads 16S rRNA gene 

Notes

Acknowledgments

This study was partially supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (23310055, 23658272).

References

  1. Adrian L, Dudková V, Demnerová K, Bedard DL (2009) “Dehalococcoides” sp. strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 75:4516–4524CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang J, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  3. Ashelford KE, Chuzhanova AN, Fry JC, Jones AJ, Weightman AJ (2005) At least one in twenty 16S rRNA sequence records currently held in public repositories estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736 [Pintail URL: http://www.bioinformatics-toolkit.org/Pintail/index.html]
  4. Baba D, Katayama A (2007) Enhanced anaerobic biodegradation of polychlorinated biphenyls in burnt soil culture. J Biosci Bioeng 104:62–68CrossRefGoogle Scholar
  5. Baba D, Yasuta T, Yoshida N et al (2007) Anaerobic biodegradation of polychlorinated biphenyls by a microbial consortium from uncontaminated paddy soil. World J Microbiol Biotechnol 23:1627–1636CrossRefGoogle Scholar
  6. Bedard DL (2008) A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls—from sediment to defined medium. Annu Rev Microbiol 62:253–270CrossRefGoogle Scholar
  7. Bedard DL, May RJ (1996) Characterization of the polychlorinated biphenyls in the sediments of Woods Pond: evidence for microbial dechlorination of Aroclor 1260 in situ. Environ Sci Technol 30:237–245CrossRefGoogle Scholar
  8. Bedard DL, Quensen JF III (1995) Microbial reductive dechlorination of polychlorinated biphenyls. In: Young LY, Cerniglia CE (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss Division, Wiley, New York, pp 127–216Google Scholar
  9. Bedard DL, Bailey JJ, Reiss BL, Jerzak GVS (2006) Development and characterization of stable sediment-free anaerobic bacterial enrichment cultures that dechlorinate Aroclor 1260. Appl Environ Microbiol 72:2460–2470CrossRefGoogle Scholar
  10. Borja J, Taleon DM, Auresenia J, Gallardo S (2005) Polychlorinated biphenyls and their biodegradation. Process Biochem 40:1999–2013CrossRefGoogle Scholar
  11. Brázová T, Miklsová D, Šalgovičová D, Turčeková L (2012) Biomonitoring of polychlorinated biphenyls (PCBs) in heavily polluted aquatic environment in different fish species. Environ Monit Assess 184:6553–6561CrossRefGoogle Scholar
  12. Collins MD, Widdel F (1986) Respiratory quinones of sulphate-reducing and sulphur-reducing bacteria: a systematic investigation. Syst Appl Microbiol 8:8–18CrossRefGoogle Scholar
  13. Cutter L, Sowers KR, May HD (1998) Microbial dechlorination of 2,3,5,6-tetrachlorobiphenyl under anaerobic conditions in the absence of soil or sediment. Appl Environ Microbiol 64:2966–2969Google Scholar
  14. Cutter LA, Watts JEM, Sowers R, May HD (2001) Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl. Environ Microbiol 3:699–709CrossRefGoogle Scholar
  15. Ehrenreich A, Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60:4517–4526Google Scholar
  16. Erickson MD, Kaley RG II (2011) Applications of polychlorinated biphenyls. Environ Sci Pollut Res 18:135–151CrossRefGoogle Scholar
  17. Fagervold SK, Watts JEM, May HD, Sowers KR (2005) Sequential reductive dechlorination of meta-chlorinated polychlorinated biphenyl congeners in sediment microcosms by two different Chloroflexi phylotypes. Appl Environ Microbiol 71:8085–8090CrossRefGoogle Scholar
  18. Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Häggblom HH (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081CrossRefGoogle Scholar
  19. German AV, Zakonnov VV (2003) Accumulation of polychlorinated biphenyls in the Sheksninskii Pool of the Rybinsk reservoir. Water Res 30:524–528CrossRefGoogle Scholar
  20. Gunsalus RP, Romesser JA, Wolfe RS (1978) Preparation of coenzyme M analogues and their activity in the methyl coenzyme M reductase system of Methanobacterium thermoautorophicum. Biochemistry 17:2374–2377CrossRefGoogle Scholar
  21. Holliger C, Hahn D, Harmsen H, Ludwig W, Schumacher W, Tindall B, Vazquez F, Weiss N, Zehnder JA (1998) Dehalobacter restrictus gen. nov. and sp. nov., a strictly anaerobic bacterium that reductively dechlorinates tetra- and trichloroethene in an anaerobic respiration. Arch Microbiol 169:313–321CrossRefGoogle Scholar
  22. Katayama A, Fujie K (2000) Characterization of soil microbiota with quinone profile. Soil Biochem 10:303–347Google Scholar
  23. Kim KS, Hirai Y, Kato M, Urano K, Masunaga S (2004) Detailed PCB congener patterns in incinerator flue gas and commercial PCB formulations (Kanechlor). Chemosphere 55:539–553CrossRefGoogle Scholar
  24. Kuever J, Rainey FA, Widdel F (2005) Genus I. Desulfovibrio Kluyver and van Niel 1936, 397AL. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 926–938CrossRefGoogle Scholar
  25. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  26. Lee W, Batchelor B (2004) Abiotic reductive dechlorination of chlorinated ethylenes by soil. Chemosphere 55:705–713CrossRefGoogle Scholar
  27. May HD, Cutter LA, Miller GS, Milliken CE, Watts JEM, Sowers KR (2006) Stimulatory and inhibitory effects of organohalides on the dehalogenating activities of PCB-dechlorinating bacterium o-17. Environ Sci Technol 40:5704–5709CrossRefGoogle Scholar
  28. May HD, Miller GS, Kjellerup BV, Sowers KR (2008) Dehalorespiration with polychlorinated biphenyls by an anaerobic ultramicrobacterium. Appl Environ Microbiol 74:2089–2094CrossRefGoogle Scholar
  29. Natarjan MR, Wu WM, Wang H, Bhatnagar L, Jain M (1998) Dechlorination of spiked PCBs in lake sediment by anaerobic microbial granules. Water Res 32:3013–3020CrossRefGoogle Scholar
  30. Pieper DH, Seeger M (2008) Bacterial metabolism of polychlorinated biphenyls. J Mol Microbiol Biotechnol 15:121–138CrossRefGoogle Scholar
  31. Quensen JF III, Boyd SA, Tiedje JM (1990) Dechlorination of four commercial polychlorinated biphenyl mixtures (Aloclors) by anaerobic microorganisms from sediments. Appl Environ Microbiol 56:2360–2369Google Scholar
  32. Sage S (1993) Toxicology, structure-function relationship, and human and environmental health impacts of polychlorinated biphenyls: progress and problems. Environ Health Perspect 100:259–268CrossRefGoogle Scholar
  33. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  34. Taylor B, Oremland RS (1979) Depletion of adenosine triphosphate in Desulfovibrio by oxyanions of group VI elements. Curr Microbiol 3:101–103CrossRefGoogle Scholar
  35. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  36. Utkin I, Woese C, Wiegel J (1994) Isolation and characterization of Desulfitobacterium dehalogenans gen. nov., sp. nov., an anaerobic bacterium which reductively dechlorinates chlorophenolic compounds. Int J Syst Bacteriol 44:612–619CrossRefGoogle Scholar
  37. Van Dort HM, Smullen LA, May RJ, Bedard DL (1997) Priming microbial meta-dechlorination of polychlorinated biphenyls that have persisted in Housatonic River sediments for decades. Environ Sci Technol 31:3300–3307CrossRefGoogle Scholar
  38. Villemur R, Lanthier M, Beaudet R, Lépine F (2006) The Desulfitobacterium genus. FEMS Microbiol Rev 30:706–733CrossRefGoogle Scholar
  39. Voice TC, Weber WJ (1983) Sorption of hydrophobic compounds by sediments, soils, and suspended solids-I. Water Res 10:1433–1441CrossRefGoogle Scholar
  40. Widdel F, Kohring GW, Mayer F (1983) Studies of dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. and sp. nov. and Desulfonema magnum sp. nov. Arch Microbiol 134:286–294CrossRefGoogle Scholar
  41. Wiegel J, Wu Q (2000) Microbial reductive dehalogenation of polychlorinated biphenyls. FEMS Microbiol Ecol 32:1–15CrossRefGoogle Scholar
  42. Wiegel J, Zhang X, Wu Q (1999) Anaerobic dehalogenation of hydroxylated polychlorinated biphenyls by Desulfitobacterium dehalogenans. Appl Environ Microbiol 65:2217–2221Google Scholar
  43. Williams WA (1994) Microbial reductive dechlorination of trichlorobiphenyls in anaerobic sediment slurries. Environ Sci Technol 28:630–635CrossRefGoogle Scholar
  44. Wu Q, Bedard DL, Wiegel J (1997) Effect of incubation temeperature on the route of microbial reductive dechlorination of 2,3,4,6-tetrachlorinated biphenyl (PCB)-contaminated and PCB-free freshwater sediments. Appl Environ Microbiol 63:2836–2843Google Scholar
  45. Wu Q, Sowers KR, May HD (1998) Microbial reductive dechlorination of Aroclor 1260 in anaerobic slurries of estuarine sediments. Appl Environ Microbiol 64:1052–1058Google Scholar
  46. Wu Q, Sowers KR, May HD (2000) Establishment of a polychlorinated biphenyl-dechlorinating microbial consortium, specific for double flanked chlorines, in a defined, sediment-free medium. Appl Environ Microbiol 66:49–53CrossRefGoogle Scholar
  47. Wu Q, Watts JEM, Sowers R, May HD (2002) Identification of a bacterium that specifically catalyzes the reductive dechlorination of polychlorinated biphenyls with doubly flanked chlorines. Appl Environ Microbiol 68:807–812CrossRefGoogle Scholar
  48. Yan T, LaPara TM, Novak PJ (2006) The effect of varying levels of sodium bicarbonate on polychlorinated biphenyl dechlorination in Hudson River sediment cultures. Environ Microbiol 8:1288–1298CrossRefGoogle Scholar
  49. Yoshida N, Ye N, Baba D, Katayama Y (2009a) A novel Dehalobacter sp. is involved in extensive 4,5,6,7-tetrachlorophthalide (fthalide) dechlorination. Appl Environ Microbiol 75:2400–2405CrossRefGoogle Scholar
  50. Yoshida N, Ye L, Baba D, Katayama A (2009b) Reductive dechlorination of polychlorinated biphenyls and dibenzo-p-dioxins in an enrichment culture containing Dehalobacter species. Microbes Environ 24:343–346CrossRefGoogle Scholar
  51. Zanaroli G, Balloi A, Negroni A, Daffonchio D, Young LY, Fava F (2010) Characterization of the microbial community from the marine sediment of the Venice lagoon capable of reductive dechlorination of coplanar polychlorinated biphenyls (PCBs). J Hazard Mater 178:417–426CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Daisuke Suzuki
    • 1
    Email author
  • Daisuke Baba
    • 1
  • Velayudhan Satheeja Santhi
    • 2
  • Robinson David Jebakumar Solomon
    • 2
  • Arata Katayama
    • 1
  1. 1.EcoTopia Science InstituteNagoya UniversityNagoyaJapan
  2. 2.Department of Molecular Microbiology, School of BiotechnologyMadurai Kamaraj UniversityMaduraiIndia

Personalised recommendations