Skip to main content
SpringerLink
Log in

Pyridine-2,6-bis(thiocarboxylic acid) Produced by Pseudomonas stutzeri KC Reduces Chromium(VI) and Precipitates Mercury, Cadmium, Lead and Arsenic

  • Original Paper
  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Interactions of the Pseudomonas stutzeri KC siderophore pyridine-2,6-bis(thiocarboxylic acid) (pdtc) with chromium(VI), mercury(II), cadmium(II), lead(II), and arsenic(III) are described. Pdtc was found to reduce Cr(VI) to Cr(III) in both bacterial cultures and in abiotic reactions with chemically synthesized pdtc. Cr(III) subsequently formed complexes with pdtc and pdtc hydrolysis products, and their presence was confirmed using electrospray ionization-mass spectrometry (ESI-MS). Cr(III):pdtc complexes were found to slowly release Cr(III) as chromium sulfide and possibly Cr(III) oxides. Pdtc also formed poorly soluble complexes with Hg, Cd, Pb, and As(III). Hydrolysis of those complexes led to the formation of their respective metal sulfides as confirmed by energy dispersive X-ray spectroscopy (EDS) elemental analysis. The pdtc-producing strain P. stutzeri KC showed higher tolerance to most of these metals as compared to a pdtc-negative mutant. A novel role of pdtc is postulated as its involvement in providing an extracellular pool of thiols that are used for redox processes in detoxification of the bacterial extracellular environment. These redox processes can be mediated by transition metal:pdtc complexes.

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

Similar content being viewed by others

References

  • Aguilera S, Aguilar MaE, Chavez MP et al (2004) Essential residues in the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol Lett 232:107–112

    Article  PubMed  CAS  Google Scholar 

  • Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339

    Article  PubMed  CAS  Google Scholar 

  • Budzikiewicz H (2003) Heteroaromatic monothiocarboxylic acids from Pseudomonas spp. Biodegradation 14:65–72

    Article  PubMed  CAS  Google Scholar 

  • Cervantes C, Campos-Garcia J, Devars S et al (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  PubMed  CAS  Google Scholar 

  • Chardin B, Giudici-Orticoni MT, De Luca G, Guigliarelli B, Bruschi M (2003) Hydrogenases in sulfate-reducing bacteria function as chromium reductase. Appl Microbiol Biotechnol 63:315–321

    Article  PubMed  CAS  Google Scholar 

  • Cortese MS, Paszczynski AJ, Lewis TA et al (2002) Metal chelating properties of pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities of the formed complexes. Biometals 15:103–120

    Article  PubMed  CAS  Google Scholar 

  • Criddle CS, DeWitt JT, Grbic-Galic D, McCarty PL (1990) Transformation of carbon tetrachloride by Pseudomonas sp. strain KC under denitrification conditions. Appl Environ Microbiol 56:3240–3246

    PubMed  CAS  Google Scholar 

  • Diels L, van der Lelie N, Bastiaens L (2002) New developments in treatment of heavy metal contaminated soils. Rev Env Sci Biotechnol 1:75–82

    Article  CAS  Google Scholar 

  • Dionex Corporation. 2000 Determination of dissolved hexavalent chromium in drinking water, groundwater and industrial waste water effluents by ion chromatography. Application Note 80

  • Dionex Corporation. 1996 Determination of Cr(VI) in water, waste water, and solid waste extracts. Technical Note 26

  • Dybas MJ, Barclona M, Bezborodnikov S, Davies S, Forney L, Heuer H, Kawka O, Mayotte T, Sepulveda-Torres LdC, Smalla C, Sneathen M, Tiedje J, Voice T, Wiggert DD, Witt ME, Criddle CS (1998) Pilot-scale evaluation of bioaugmentation for in-situ remediation of a carbon tetrachloride-contaminated aquifer. Environ Sci Technol 32:3598–3611

    Article  CAS  Google Scholar 

  • Environmental Protection Agency. 2000 In situ treatment of soil and groundwater contaminated with chromium: technical resource guide. EPA National Risk Management Research Laboratory, Cincinnati, OH, EPA/625/R-00/005. Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC

  • Evanko CR, Dzombak DA. 1997. Remediation of metals-contaminated soils and ground water: technical report TE-97-01. USEPA Ground Water Remediation Technologies Analysis Center, Pitlsburg, PA, 46 pp

  • Feistner GJ (1995) Suggestion for a new, semirational nomenclature for the free chelators of ferrioxamines. Biometals 8:193–196

    CAS  Google Scholar 

  • Fekete FA, Barton LL (1992) Effects of iron(III) analogs on growth and pseudobactin synthesis in a chromium-tolerant Pseudomonas isolate. Biol Met 4:211–216

    Article  Google Scholar 

  • Fendorf S, Li H (1996) Kinetics of chromate reduction by ferrous iron. Environ Sci Technol 30:1614–1617

    Article  CAS  Google Scholar 

  • Figueira EMdAP, Lima AIG, Pereira SIA (2005) Cadmium tolerance plasticity in Rhizobium leguminosarum bv. viviae: glutathione as a detoxifying agent. Can J Microbiol 51:7–14

    Article  PubMed  CAS  Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119

    Article  CAS  Google Scholar 

  • Gustin MS, Taylor GE, Leonard TL (1994) High levels of mercury contamination in multiple media of the Carson River drainage basin of Nevada: implications for risk assessment. Environ Health Perspect 102:772–778

    Article  PubMed  CAS  Google Scholar 

  • Hildebrand U, Ockels W, Lex J, Budzikiewicz H (1983) Zur struktur eines 1:1-adduktes von pyridin-2,6-dicarbothiosäure und pyridin. Phosphorus Sulfur 16:361–364

    CAS  Google Scholar 

  • Hou Z, Raymond KN, O’Sullivan B, Esker TW (1998) A preorganized siderophore:Thermodynamic and structural characterization of alcaligin and bisucaberin, microbial macrocyclic dihydroxamate chelating agents. Inorg Chem 37:6630–6637

    Article  PubMed  CAS  Google Scholar 

  • Hu XC, Boyer GL (1996) Siderophore-mediated aluminum uptake by Bacillus megaterium ATCC 19213. Appl Environ Microbiol 62:4044–4048

    PubMed  CAS  Google Scholar 

  • International Programme on Chemical Safety. 2001 Environmental health criteria monograph 224: arsenic and arsenic compounds. [Online.] http://www.inchem.org/documents/ehc/ehc/ehc224.htm. Accessed 25 April 2006.

  • Kessi J, Hanselmann KW (2004) Similarities between the abiotic reduction of selenite with glutathione and the dissimilatory reaction mediated by Rhodospirillum rubrum and Escherichia coli. J Biol Chem 279:50662–50669

    Article  PubMed  CAS  Google Scholar 

  • Kim M-J, Ahn K-H, Jung Y, Lee S, Lim B-R (2003) Arsenic, cadmium, chromium, copper, lead, and zinc contamination in mine tailings and nearby streams of three abandoned mines from Korea. Bull Environ Contam Toxicol 70:942–947

    Article  PubMed  CAS  Google Scholar 

  • Lee C-H, Lewis TA, Paszczynski AJ, Crawford RL (1999) Identification of an extracellular catalyst of carbon tetrachloride dehalogenation from Pseudomonas stutzeri strain KC as pyridine-2,6-bis(thiocarboxylate). Biochem Biophys Res Commun 261:562–566

    Article  PubMed  CAS  Google Scholar 

  • Lewis TA, Cortese MS, Sebat JL et al (2000) A Pseudomonas stutzeri gene cluster encoding biosynthesis of the CCl4-dechlorination agent pyridine-2,6-bis(thiocarboxylic acid). Environ Microbiol 2: 407–416

    Article  PubMed  CAS  Google Scholar 

  • Lewis TA, Leach L, Morales S et al (2004) Physiological and molecular genetic evaluation of the dechlorination agent, pyridine-2,6-bis(monothiocarboxylic acid) (PDTC) as a secondary siderophore of Pseudomonas. Environ Microbiol 6:159–169

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Mabbett A, Williams DR, Macaskie LE (2001) Metal reduction by sulfate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy 59:327–337

    Article  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1994) Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Appl Environ Microbiol 60:726–728

    PubMed  CAS  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26: 311–325

    Article  PubMed  CAS  Google Scholar 

  • Newman DK, Beveridge TJ, Morel FMM (1997) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Appl Environ Microbiol 63:2022–2028

    PubMed  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  PubMed  CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  PubMed  CAS  Google Scholar 

  • Nies DH, Koch S, Wachi S, Peitzsch N, Saier MH Jr (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180:5799–5802

    PubMed  CAS  Google Scholar 

  • Nyman MD, Hampden-Smith MJ, Duesler EN (1997) Synthesis, characterization, and reactivity of group 12 metal thiocarboxylates, M(SOCR)2Lut2 [M = Cd, Zn; R = CH3, C(CH3)3; Lut = 3,5-dimethylpyridine (Lutidine)]. Inorg Chem 36:2218–2224

    Article  PubMed  CAS  Google Scholar 

  • Ockels W, Römer A, Budzikiewicz H (1978) An Fe(III) complex of pyridine-2,6-di(monothiocarboxylic acid) - A novel bacterial metabolic product. Tetrahedron Lett 36:3341–3342

    Article  Google Scholar 

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944

    Article  PubMed  CAS  Google Scholar 

  • Park CH, Keyhan M, Wielinga B, Fendorf S, Matin A (2000) Purification to homogenity and characterization of a novel Pseudomonas putida chromate reductase. Appl Environ Microbiol 66:1788–1795

    Article  PubMed  CAS  Google Scholar 

  • Raab A, Feldmann J (2003) Microbial transformation of metals and metalloids. Sci Prog 86:179–202

    Article  PubMed  CAS  Google Scholar 

  • Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92

    Article  PubMed  CAS  Google Scholar 

  • Sebat JL, Paszczynski AJ, Cortese MS, Crawford RL (2001) Antimicrobial properties of pyridine-2,6-dithiocarboxylic acid, a metal chelator produced by Pseudomonas spp. Appl Environ Microbiol 67:3934–3942

    Article  PubMed  CAS  Google Scholar 

  • Smillie RH, Hunter K, Loutit M (1981) Reduction of chromium(VI) by bacterially produced hydrogen sulfide in a marine environment. Water Res 15:1351–1354

    Article  CAS  Google Scholar 

  • Smith WL, Gadd GM (2000) Reduction and precipitation of chromate by mixed culture sulphate-reducing bacterial biofilms. J Appl Microbiol 88:983–991

    Article  PubMed  CAS  Google Scholar 

  • Stolworthy JC, Paszczynski AJ, Korus R, Crawford RL (2001) Metal binding by pyridine-2,6-bis(monothiocarboxylic acid), a biochelator produced by Pseudomonas stutzeri and Pseudomonas putida. Biodegradation 12:411–418

    Article  PubMed  CAS  Google Scholar 

  • Turner RJ, Aharonowitz Y, Weiner JH, Taylor DE (2001) Glutathione is a target in tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli. Can J Microbiol 47:33–40

    Article  PubMed  CAS  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338

    PubMed  CAS  Google Scholar 

  • Visca P, Colotti G, Serino L et al (1992) Metal regulation of siderophore synthesis in Pseudomonas aruginosa and functional effects of siderophore-metal complexes. Appl Environ Microbiol 58:2886–2893

    PubMed  CAS  Google Scholar 

  • Winkelmann G (1991) Specificity of iron transport in bacteria and fungi. In: Winkelmann G (eds) CRC Handbook of microbial iron chelates. CRC Press, Boca Raton FL, pp. 65–106

    Google Scholar 

  • Zawadzka AM, Crawford RL, Paszczynski AJ (2006) Pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas stutzeri KC reduces and precipitates selenium and tellurium oxyanions. Appl Environ Microbiol 72, 3119–3129

    Google Scholar 

Download references

Acknowledgements

This research was supported by an Inland Northwest Research Alliance Subsurface Science Research Institute Fellowship to A. Zawadzka (#60-4006-102) and by the Environmental Biotechnology Institute at the University of Idaho in Moscow, ID. We acknowledge the M. J. Murdock Charitable Trust for supporting acquisition of the EDS instrument used during the research. We express appreciation to Franklin Bailey from the Electron Microscopy Center at the University of Idaho; we thank Cornelia Sawatzky for manuscript editing.

Author information

Authors and Affiliations

  1. Environmental Biotechnology Institute, University of Idaho, Food Research Center 103, P.O. Box 441052, Moscow, Idaho, 83844–1052, USA

    Anna M. Zawadzka, Ronald L. Crawford & Andrzej J. Paszczynski

Authors
  1. Anna M. Zawadzka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ronald L. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrzej J. Paszczynski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrzej J. Paszczynski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zawadzka, A.M., Crawford, R.L. & Paszczynski, A.J. Pyridine-2,6-bis(thiocarboxylic acid) Produced by Pseudomonas stutzeri KC Reduces Chromium(VI) and Precipitates Mercury, Cadmium, Lead and Arsenic. Biometals 20, 145–158 (2007). https://doi.org/10.1007/s10534-006-9022-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-006-9022-2

Keywords

Search

Navigation