Skip to main content
SpringerLink
Log in

Hexavalent chromium reduction by Cellulomonas sp. strain ES6: the influence of carbon source, iron minerals, and electron shuttling compounds

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

Abstract

The reduction of hexavalent chromium, Cr(VI), to trivalent chromium, Cr(III), can be an important aspect of remediation processes at contaminated sites. Cellulomonas species are found at several Cr(VI) contaminated and uncontaminated locations at the Department of Energy site in Hanford, Washington. Members of this genus have demonstrated the ability to effectively reduce Cr(VI) to Cr(III) fermentatively and therefore play a potential role in Cr(VI) remediation at this site. Batch studies were conducted with Cellulomonas sp. strain ES6 to assess the influence of various carbon sources, iron minerals, and electron shuttling compounds on Cr(VI) reduction rates as these chemical species are likely to be present in, or added to, the environment during in situ bioremediation. Results indicated that the type of carbon source as well as the type of electron shuttle present influenced Cr(VI) reduction rates. Molasses stimulated Cr(VI) reduction more effectively than pure sucrose, presumably due to presence of more easily utilizable sugars, electron shuttling compounds or compounds with direct Cr(VI) reduction capabilities. Cr(VI) reduction rates increased with increasing concentration of anthraquinone-2,6-disulfonate (AQDS) regardless of the carbon source. The presence of iron minerals and their concentrations did not significantly influence Cr(VI) reduction rates. However, strain ES6 or AQDS could directly reduce surface-associated Fe(III) to Fe(II), which was capable of reducing Cr(VI) at a near instantaneous rate. These results suggest the rate limiting step in these systems was the transfer of electrons from strain ES6 to the intermediate or terminal electron acceptor whether that was Cr(VI), Fe(III), or AQDS.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amonette J, Workman D, Kennedy D, Fruchter J, Gorby Y (2000) Dechlorination of carbon tetrachloride by Fe(II) associated with goethite. Environ Sci Technol 34:4606–4613

    Article  CAS  Google Scholar 

  • Anonymous (2005) GAO-06-77R Columbia River contamination from the Hanford site. United States Government Accountability Office, Washington, DC

    Google Scholar 

  • Barceloux D (1999) Chromium. Clin Toxicol 37:173–194

    Article  CAS  Google Scholar 

  • Borch T, Inskeep W, Harwood J, Gerlach R (2005) Impact of ferrihydrite and anthraquinone-2,6-disulfonate on the reductive transformation of 2,4,6-trinitrotoluene by a gram-positive fermenting bacterium. Environ Sci Technol 39:7126–7133

    Google Scholar 

  • Brose D, James B (2010) Oxidation-reduction transformations of chromium in aerobic soils and the role of electron-shuttling quinones. Environ Sci Technol 44:9438–9444

    Article  PubMed  CAS  Google Scholar 

  • Buerge I, Hug S (1997) Kinetics and pH dependence of chromium(VI) reduction by iron(II). Environ Sci Technol 31:1426–1432

    Article  CAS  Google Scholar 

  • Calder L (1988) Chromium contamination of groundwater. In: Niebaer E, Niragu J (eds) Chromium in the natural and human environments. Wiley, New York, pp 215–228

    Google Scholar 

  • Chen J, Hao O (1998) Microbial chromium(VI) reduction. Crit Rev Environ Sci Technol 28:219–251

    Article  Google Scholar 

  • Eary L, Rai D (1988) Chromate removal from aqueous wastes by reduction with ferrous ion. Environ Sci Technol 22:972–977

    Article  PubMed  CAS  Google Scholar 

  • Francisco R, Alpoim M, Morais P (2002) Diversity of chromium-resistant and-reducing bacteria in a chromium-contaminated activated sludge. J Appl Microbiol 92:837–843

    Article  PubMed  CAS  Google Scholar 

  • Fredrickson J, Zachara J, Kennedy D, Dong H, Onstott T, Hinman N, Li S (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim Cosmochim Acta 62:3239–3257

    Article  CAS  Google Scholar 

  • Fredrickson J, Kostandarithes H, Li S, Plymale A, Daly M (2000) Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Appl Environ Microbiol 66:2006–2011

    Article  PubMed  CAS  Google Scholar 

  • Gerlach R, Field E, Viamajala S, Peyton B, Apel W, Cunningham A (2011) Influence of carbon sources and electron shuttles on ferric iron reduction by Cellulomonas sp. strain ES6. Biodegradation 22:983–995

    Article  PubMed  CAS  Google Scholar 

  • Hayes R (1997) The carcinogenicity of metals in humans. Cancer Causes Control 8:371–385

    Article  PubMed  CAS  Google Scholar 

  • James B (1994) Hexavalent chromium solubility and reduction in alkaline soils enriched with chromite ore processing residue. J Environ Qual 23:227–233

    Article  CAS  Google Scholar 

  • Jung Y, Choi J, Lee W (2007) Spectroscopic investigation of magnetite surface for the reduction of hexavalent chromium. Chemosphere 68:1968–1975

    Article  PubMed  CAS  Google Scholar 

  • Krishna K, Philip L (2005) Bioremediation of Cr(VI) in contaminated soils. J Hazard Mater 121:109–117

    Article  PubMed  CAS  Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—a review. Waste Manag 28:215–225

    Article  PubMed  CAS  Google Scholar 

  • Kwon M, Finneran K (2009) Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) reduction is concurrently mediated by direct electron transfer from hydroquinones and resulting biogenic Fe(II) formed during electron shuttle-amended biodegradation. Environ Eng Sci 26:961–971

    Article  CAS  Google Scholar 

  • Li Y, Low G, Scott J, Amal R (2009) The role of iron in hexavalent chromium reduction by municipal landfill leachate. J Hazard Mater 161:657–662

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler F (2002) Unsaturated O- and N-heterocycles from carbohydrate feedstocks. Acc Chem Res 35:728–737

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Gorby Y, Zachara J, Fredrickson J, Brown C (2002) Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI), and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol Bioeng 80:637–649

    Article  PubMed  CAS  Google Scholar 

  • Liu T, Rao P, Lo I (2009) Influences of humic acid, bicarbonate and calcium on Cr(VI) reductive removal by zero-valent iron. Sci Total Environ 407:3407–3414

    Article  PubMed  CAS  Google Scholar 

  • Lovley D (1997) Microbial Fe(III) reduction in subsurface environments. FEMS Microbiol Rev 20:305–313

    Article  CAS  Google Scholar 

  • Lovley D, Blunt-Harris E (1999) Role of humic-bound iron as an electron transfer agent in dissimilatory Fe(III) reduction. Appl Environ Microbiol 65:4252–4254

    PubMed  CAS  Google Scholar 

  • Lovley D, Phillips E (1986a) Availability of ferric iron for microbial reduction in bottom sediments of the freshwater tidal Potomac River. Appl Environ Microbiol 52:751–757

    PubMed  CAS  Google Scholar 

  • Lovley D, Phillips E (1986b) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689

    PubMed  CAS  Google Scholar 

  • Lovley D, Phillips E (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540

    PubMed  CAS  Google Scholar 

  • Lovley D, Fraga J, Blunt-Harris E, Hayes L, Phillips E, Coates J (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26:152–157

    Article  CAS  Google Scholar 

  • Nealson K, Saffarini D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol 48:311–343

    Article  PubMed  CAS  Google Scholar 

  • Nevin K, Lovley D (2000) Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ Sci Technol 34:2472–2478

    Article  CAS  Google Scholar 

  • Newman D (2001) How bacteria respire minerals. Science 292:1312–1313

    Article  PubMed  CAS  Google Scholar 

  • Nyman J, Caccavo F, Cunningham A, Gerlach R (2002) Biogeochemical elimination of chromium(VI) from contaminated water. Biorem J 6:39–55

    Article  CAS  Google Scholar 

  • Okutman Tas D, Pavlostathis S (2007) The influence of iron reduction on the reductive biotransformation of pentachloronitrobenzene. Eur J Soil Biol 43:264–275

    Article  CAS  Google Scholar 

  • Pettine M, D’Ottone L, Campanella L, Millero F, Passino R (1998) The reduction of chromium(VI) by iron(II) in aqueous solutions. Geochim Cosmochim Acta 62:1509–1519

    Article  CAS  Google Scholar 

  • Prescott S, Dunn C (1983) Prescott and Dunn’s industrial microbiology. AVI, Westport

    Google Scholar 

  • Roden E, Zachara J (1996) Microbial reduction of crystalline iron(III) oxides: influence of oxide surface area and potential for cell growth. Environ Sci Technol 30:1618–1628

    Article  CAS  Google Scholar 

  • Royer R, Burgos W, Fisher A, Unz R, Dempsey B (2002) Enhancement of biological reduction of hematite by electron shuttling and Fe(II) complexation. Environ Sci Technol 36:1939–1946

    Article  PubMed  CAS  Google Scholar 

  • Sani R, Peyton B, Smith W, Apel W, Petersen J (2002) Dissimilatory reduction of Cr(VI), Fe(III), and U(VI) by Cellulomonas isolates. Appl Microbiol Biotechnol 60:192–199

    Article  PubMed  CAS  Google Scholar 

  • Seaman J, Bertsch P, Schwallie L (1999) In situ Cr(VI) reduction within coarse-textured, oxide-coated soil and aquifer systems using Fe(II) solutions. Environ Sci Technol 33:938–944

    Article  CAS  Google Scholar 

  • Smith W, Apel W, Peterson J, Peyton B (2002) Effect of carbon and energy source on bacterial chromate reduction. Biorem J 6:205–215

    Article  CAS  Google Scholar 

  • Tseng J, Bielefeldt A (2002) Low-temperature chromium(VI) biotransformation in soil with varying electron acceptors. J Environ Qual 31:1831–1841

    Article  PubMed  CAS  Google Scholar 

  • Turick C, Apel W, Carmiol N (1996) Isolation of hexavalent chromium-reducing anaerobes from hexavalent-chromium-contaminated and noncontaminated environments. Appl Microbiol Biotechnol 44:683–688

    Article  PubMed  CAS  Google Scholar 

  • Turick C, Tisa L, Caccavo F Jr (2002) Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl Environ Microbiol 68:2436–2444

    Article  PubMed  CAS  Google Scholar 

  • Tzou Y, Wang M, Loppert R (2003) Sorption of phosphate and Cr(VI) by Fe(III) and Cr(III) hydroxides. Arch Environ Contam Toxicol 44:445–453

    Article  PubMed  CAS  Google Scholar 

  • Vázquez-Morillas A, Vaca-Mier M, Alvarez P (2006) Biological activation of hydrous ferric oxide for reduction of hexavalent chromium in the presence of different anions. Eur J Soil Biol 42:99–106

    Article  Google Scholar 

  • Viamajala S, Peyton B, Apel W, Peterson J (2002) Chromate reduction in Shewanella oneidensis MR-1 is an inducible process associated with anaerobic growth. Biotechnol Prog 18:290–295

    Article  PubMed  CAS  Google Scholar 

  • Viamajala S, Smith W, Sani R, Apel W, Petersen J, Neal A, Roberto F, Newby D, Peyton B (2007) Isolation and characterization of Cr(VI) reducing Cellulomonas spp. from subsurface soils: implications for long-term chromate reduction. Bioresour Technol 98:612–622

    Article  PubMed  CAS  Google Scholar 

  • Viamajala S, Peyton B, Gerlach R, Sivaswamy V, Apel W, Petersen J (2008) Permeable reactive biobarriers for in situ Cr(VI) reduction: bench scale tests using Cellulomonas sp. strain ES6. Biotechnol Bioeng 101:1150–1162

    Article  PubMed  CAS  Google Scholar 

  • Wielinga B, Mizuba M, Hansel C, Fendorf S (2001) Iron promoted reduction of chromate by dissimilatory iron-reducing bacteria. Environ Sci Technol 35:522–527

    Article  PubMed  CAS  Google Scholar 

  • Workman D, Woods S, Gorby Y, Fredrickson J, Truex M (1997) Microbial reduction of vitamin B12 by Shewanella alga strain BrY with subsequent transformation of carbon tetrachloride. Environ Sci Technol 31:2292–2297

    Article  CAS  Google Scholar 

  • Xu W, Liu Y, Zeng G, Li X, Tang C, Yuan X (2005) Enhancing effect of iron on chromate reduction by Cellulomonas flavigena. J Hazard Mater 126:17–22

    Article  PubMed  CAS  Google Scholar 

  • Yassi A, Nieboer E (1988) Carcinogenicity of chromium compounds. In: Niragu J, Niebaer E (eds) Chromium in the natural and human environments. Wiley, New York, pp 443–478

    Google Scholar 

  • Zachara J, Fredrickson J, Li S, Kennedy D, Smith S, Gassman P (1998) Bacterial reduction of crystalline Fe3+ oxides in single phase suspensions and subsurface materials. Am Mineral 83:1426–1443

    CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Lindsey Hopper, Kristy Weaver, Nicholas Ballor and Crystal Russell for their various contributions in the laboratory. This research was supported by the U.S. Department of Energy, Office of Science, Subsurface Biogeochemical Research Program, under Grant Nos. DE-FG02-03ER63582 and DOE-NE Idaho Operations Office Contract DE-AC07-05ID14517. Partial financial support was provided by a grant from the Inland Northwest Research Alliance (INRA) under contract MSU 002. We thank Thomas Borch, Matthew Marcus (ALS) and Matthew Ginder-Vogel for their help with synchrotron-based analyses. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.

Author information

Authors and Affiliations

  1. Department of Microbiology and Center for Biofilm Engineering, Montana State University, Bozeman, MT, 59717, USA

    Erin K. Field

  2. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, 04544, USA

    Erin K. Field

  3. Department of Chemical and Biological Engineering and Center for Biofilm Engineering, Montana State University, 366 EPS Building, Bozeman, MT, 59717, USA

    Robin Gerlach, Laura K. Jennings & Brent M. Peyton

  4. Department of Chemical and Environmental Engineering, The University of Toledo, Toledo, OH, 43606, USA

    Sridhar Viamajala

  5. Biological Systems Department, Idaho National Laboratory, Idaho Falls, ID, 83415, USA

    William A. Apel

Authors
  1. Erin K. Field
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robin Gerlach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sridhar Viamajala
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura K. Jennings
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brent M. Peyton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. William A. Apel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robin Gerlach.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 493 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Field, E.K., Gerlach, R., Viamajala, S. et al. Hexavalent chromium reduction by Cellulomonas sp. strain ES6: the influence of carbon source, iron minerals, and electron shuttling compounds. Biodegradation 24, 437–450 (2013). https://doi.org/10.1007/s10532-012-9600-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-012-9600-7

Keywords

Search

Navigation