1887

Abstract

The application of toxic triphenylmethane dyes such as crystal violet (CV) in various industrial processes leads to large amounts of dye-contaminated sludges that need to be detoxified. Specific bacteria residing in wastewater treatment plants (WWTPs) are able to degrade triphenylmethane dyes. The objective of this work was to gain insights into the genetic background of bacterial strains capable of CV degradation. Three bacterial strains isolated from a municipal WWTP harboured IncP-1β plasmids mediating resistance to and decolorization of CV. These isolates were assigned to the genera and . The CV-resistance plasmid pKV29 from sp. KV29 was completely sequenced. In addition, nucleotide sequences of the accessory regions involved in conferring CV resistance were determined for plasmids pKV11 and pKV36 from the other two isolates. Plasmid pKV29 contains typical IncP-1β backbone modules that are highly similar to those of previously sequenced IncP-1β plasmids that confer antibiotic resistance, degradative capabilities or mercury resistance. The accessory regions located between the conjugative transfer () and mating pair formation modules () of all three plasmids analysed share common modules and include a triphenylmethane reductase gene, , that is responsible for decolorization of CV. Moreover, these accessory regions encode other enzymes that are dispensable for CV degradation and hence are involved in so-far-unknown metabolic pathways. Analysis of plasmid-mediated degradation of CV in by ultra-high-performance liquid chromatography-electrospray ionization-quadrupole-time-of-flight MS revealed that leuco crystal violet was the first degradation product. Michler’s ketone and 4-dimethylaminobenzaldehyde appeared as secondary degradation metabolites. Enzymes encoded in the chromosome seem to be responsible for cleavage of leuco crystal violet. Plasmid-mediated degradation of triphenylmethane dyes such as CV is an option for the biotechnological treatment of sludges contaminated with these dyes.

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2012-08-01
2020-01-25
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References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. ( 1997;). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  2. Au W., Pathak S., Collie C. J., Hsu T. C.. ( 1978;). Cytogenetic toxicity of gentian violet and crystal violet on mammalian cells in vitro. Mutat Res58:269–276 [CrossRef][PubMed]
    [Google Scholar]
  3. Azmi W., Sani R. K., Banerjee U. C.. ( 1998;). Biodegradation of triphenylmethane dyes. Enzyme Microb Technol22:185–191 [CrossRef][PubMed]
    [Google Scholar]
  4. Bumpus J. A., Brock B. J.. ( 1988;). Biodegradation of crystal violet by the white rot fungus Phanerochaete chrysosporium . Appl Environ Microbiol54:1143–1150[PubMed]
    [Google Scholar]
  5. Cavener D. R.. ( 1992;). GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol223:811–814 [CrossRef][PubMed]
    [Google Scholar]
  6. Chapman J. A., Kirkness E. F., Simakov O., Hampson S. E., Mitros T., Weinmaier T., Rattei T., Balasubramanian P. G., Borman J.. & other authors ( 2010;). The dynamic genome of Hydra . Nature464:592–596 [CrossRef][PubMed]
    [Google Scholar]
  7. Chen C. C., Liao H. J., Cheng C. Y., Yen C. Y., Chung Y. C.. ( 2007;). Biodegradation of crystal violet by Pseudomonas putida . Biotechnol Lett29:391–396 [CrossRef][PubMed]
    [Google Scholar]
  8. Chen C. H., Chang C. F., Ho C. H., Tsai T. L., Liu S. M.. ( 2008;). Biodegradation of crystal violet by a Shewanella sp. NTOU1. Chemosphere72:1712–1720 [CrossRef][PubMed]
    [Google Scholar]
  9. Díaz E., Ferrández A., Prieto M. A., García J. L.. ( 2001;). Biodegradation of aromatic compounds by Escherichia coli . Microbiol Mol Biol Rev65:523–569 [CrossRef][PubMed]
    [Google Scholar]
  10. Docampo R., Moreno S. N.. ( 1990;). The metabolism and mode of action of gentian violet. Drug Metab Rev22:161–178 [CrossRef][PubMed]
    [Google Scholar]
  11. Eikmeyer F., Hadiati A., Szczepanowski R., Wibberg D., Schneiker-Bekel S., Rogers L. M., Brown C. J., Top E. M., Pühler A., Schlüter A.. ( 2012;). The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution. Plasmid68:13–24 [CrossRef][PubMed]
    [Google Scholar]
  12. Gordon D., Abajian C., Green P.. ( 1998;). Consed: a graphical tool for sequence finishing. Genome Res8:195–202[PubMed][CrossRef]
    [Google Scholar]
  13. Gordon D., Desmarais C., Green P.. ( 2001;). Automated finishing with Autofinish. Genome Res11:614–625 [CrossRef][PubMed]
    [Google Scholar]
  14. Götz A., Pukall R., Smit E., Tietze E., Prager R., Tschäpe H., van Elsas J. D., Smalla K.. ( 1996;). Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl Environ Microbiol62:2621–2628[PubMed]
    [Google Scholar]
  15. Grant S. G., Jessee J., Bloom F. R., Hanahan D.. ( 1990;). Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A87:4645–4649 [CrossRef][PubMed]
    [Google Scholar]
  16. Heinl S., Wibberg D., Eikmeyer F., Szczepanowski R., Blom J., Linke B., Goesmann A., Grabherr R., Schwab H.. & other authors ( 2012;). Insights into the completely annotated genome of Lactobacillus buchneri CD034, a strain isolated from stable grass silage. J Biotechnol [CrossRef][PubMed]
    [Google Scholar]
  17. Hynes M. F., Simon R., Pühler A.. ( 1985;). The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid13:99–105 [CrossRef][PubMed]
    [Google Scholar]
  18. Jang M. S., Lee Y. M., Kim C. H., Lee J. H., Kang D. W., Kim S. J., Lee Y. C.. ( 2005;). Triphenylmethane reductase from Citrobacter sp. strain KCTC 18061P: purification, characterization, gene cloning, and overexpression of a functional protein in Escherichia coli . Appl Environ Microbiol71:7955–7960 [CrossRef][PubMed]
    [Google Scholar]
  19. Jones J. J., Falkinham J. O. III. ( 2003;). Decolorization of malachite green and crystal violet by waterborne pathogenic mycobacteria. Antimicrob Agents Chemother47:2323–2326 [CrossRef][PubMed]
    [Google Scholar]
  20. Kwasniewska K.. ( 1985;). Biodegradation of crystal violet (hexamethyl-p-rosaniline chloride) by oxidative red yeasts. Bull Environ Contam Toxicol34:323–330 [CrossRef][PubMed]
    [Google Scholar]
  21. Littlefield N. A., Blackwell B. N., Hewitt C. C., Gaylor D. W.. ( 1985;). Chronic toxicity and carcinogenicity studies of gentian violet in mice. Fundam Appl Toxicol5:902–912 [CrossRef][PubMed]
    [Google Scholar]
  22. Ma Y. F., Zhang Y., Zhang J. Y., Chen D. W., Zhu Y., Zheng H., Wang S. Y., Jiang C. Y., Zhao G. P., Liu S. J.. ( 2009;). The complete genome of Comamonas testosteroni reveals its genetic adaptations to changing environments. Appl Environ Microbiol75:6812–6819[CrossRef]
    [Google Scholar]
  23. Margulies M., Egholm M., Altman W. E., Attiya S., Bader J. S., Bemben L. A., Berka J., Braverman M. S., Chen Y. J.. & other authors ( 2005;). Genome sequencing in microfabricated high-density picolitre reactors. Nature437:376–380[PubMed]
    [Google Scholar]
  24. Martinez B., Tomkins J., Wackett L. P., Wing R., Sadowsky M. J.. ( 2001;). Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol183:5684–5697 [CrossRef][PubMed]
    [Google Scholar]
  25. Meyer F., Goesmann A., McHardy A. C., Bartels D., Bekel T., Clausen J., Kalinowski J., Linke B., Rupp O.. & other authors ( 2003;). GenDB—an open source genome annotation system for prokaryote genomes. Nucleic Acids Res31:2187–2195 [CrossRef][PubMed]
    [Google Scholar]
  26. Mittal A., Mittal J., Malviya A., Kaur D., Gupta V. K.. ( 2010;). Adsorption of hazardous dye crystal violet from wastewater by waste materials. J Colloid Interface Sci343:463–473 [CrossRef][PubMed]
    [Google Scholar]
  27. Morita Y., Kodama K., Shiota S., Mine T., Kataoka A., Mizushima T., Tsuchiya T.. ( 1998;). NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli . Antimicrob Agents Chemother42:1778–1782[PubMed]
    [Google Scholar]
  28. Ren S., Guo J., Zeng G., Sun G.. ( 2006;). Decolorization of triphenylmethane, azo, and anthraquinone dyes by a newly isolated Aeromonas hydrophila strain. Appl Microbiol Biotechnol72:1316–1321 [CrossRef][PubMed]
    [Google Scholar]
  29. Sambrook J., Fritsch E. F., Maniatis T.. ( 1989;). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Sani R. K., Banerjee U. C.. ( 1999;). Decolorization of triphenylmethane dyes and textile and dye-stuff effluent by Kurthia sp.. Enzyme Microb Technol24:433–437 [CrossRef]
    [Google Scholar]
  31. Schlüter A., Heuer H., Szczepanowski R., Forney L. J., Thomas C. M., Pühler A., Top E. M.. ( 2003;). The 64 508 bp IncP-1β antibiotic multiresistance plasmid pB10 isolated from a waste-water treatment plant provides evidence for recombination between members of different branches of the IncP-1β group. Microbiology149:3139–3153 [CrossRef][PubMed]
    [Google Scholar]
  32. Schlüter A., Heuer H., Szczepanowski R., Poler S. M., Schneiker S., Pühler A., Top E. M.. ( 2005;). Plasmid pB8 is closely related to the prototype IncP-1β plasmid R751 but transfers poorly to Escherichia coli and carries a new transposon encoding a small multidrug resistance efflux protein. Plasmid54:135–148 [CrossRef][PubMed]
    [Google Scholar]
  33. Schlüter A., Krahn I., Kollin F., Bönemann G., Stiens M., Szczepanowski R., Schneiker S., Pühler A.. ( 2007;). IncP-1β plasmid pGNB1 isolated from a bacterial community from a wastewater treatment plant mediates decolorization of triphenylmethane dyes. Appl Environ Microbiol73:6345–6350 [CrossRef][PubMed]
    [Google Scholar]
  34. Smalla K., Haines A. S., Jones K., Krögerrecklenfort E., Heuer H., Schloter M., Thomas C. M.. ( 2006;). Increased abundance of IncP-1β plasmids and mercury resistance genes in mercury-polluted river sediments: first discovery of IncP-1β plasmids with a complex mer transposon as the sole accessory element. Appl Environ Microbiol72:7253–7259 [CrossRef][PubMed]
    [Google Scholar]
  35. Sota M., Kawasaki H., Tsuda M.. ( 2003;). Structure of haloacetate-catabolic IncP-1β plasmid pUO1 and genetic mobility of its residing haloacetate-catabolic transposon. J Bacteriol185:6741–6745 [CrossRef][PubMed]
    [Google Scholar]
  36. Szczepanowski R., Krahn I., Bohn N., Pühler A., Schlüter A.. ( 2007;). Novel macrolide resistance module carried by the IncP-1β resistance plasmid pRSB111, isolated from a wastewater treatment plant. Antimicrob Agents Chemother51:673–678 [CrossRef][PubMed]
    [Google Scholar]
  37. Szczepanowski R., Eikmeyer F., Harfmann J., Blom J., Rogers L. M., Top E. M., Schlüter A.. ( 2011;). Sequencing and comparative analysis of IncP-1α antibiotic resistance plasmids reveal a highly conserved backbone and differences within accessory regions. J Biotechnol155:95–103 [CrossRef][PubMed]
    [Google Scholar]
  38. Trefault N., De la Iglesia R., Molina A. M., Manzano M., Ledger T., Pérez-Pantoja D., Sánchez M. A., Stuardo M., González B.. ( 2004;). Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134 (pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol6:655–668 [CrossRef][PubMed]
    [Google Scholar]
  39. Wang Q., Garrity G. M., Tiedje J. M., Cole J. R.. ( 2007;). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol73:5261–5267 [CrossRef][PubMed]
    [Google Scholar]
  40. Yanisch-Perron C., Vieira J., Messing J.. ( 1985;). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119 [CrossRef][PubMed]
    [Google Scholar]
  41. Yatome C., Ogawa T., Matsui M.. ( 1991;). Degradation of crystal violet by Bacillus subtilis . J Environ Sci Health, Part A26:75–87 [CrossRef]
    [Google Scholar]
  42. Yatome C., Fujimi K., Ogawa T.. ( 1992;). Effect of inhibitors on azo-reduction of 4′-dimethylaminoazobenzene-2-carboxylic acid by Clostridium diaphorase. Bull Chem Soc Jpn65:2349–2351 [CrossRef]
    [Google Scholar]
  43. Yatome C., Yamada S., Ogawa T., Matsui M.. ( 1993;). Degradation of crystal violet by Nocardia corallina . Appl Microbiol Biotechnol38:565–569 [CrossRef]
    [Google Scholar]
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