Skip to main content
Log in

Advances in Fe(III) bioreduction and its application prospect for groundwater remediation: A review

  • Review Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Microbial Fe(III) reduction is a significant driving force for the biogeochemical cycles of C, O, P, S, N, and dominates the natural bio-purification of contaminants in groundwater (e.g., petroleum hydrocarbons, chlorinated ethane, and chromium). In this review, the mechanisms and environmental significance of Fe(III) (hydro)oxides bioreduction are summarized. Compared with crystalline Fe(III) (hydro)oxides, amorphous Fe(III) (hydro)oxides are more bioavailable. Ligand and electron shuttle both play an important role in microbial Fe(III) reduction. The restrictive factors of Fe(III) (hydro) oxides bioreduction should be further investigated to reveal the characteristics and mechanisms of the process. It will improve the bioavailability of crystalline Fe(III) (hydro)oxides and accelerate the anaerobic oxidation efficiency of the reduction state pollutants. Furthermore, the approach to extract, culture, and incubate the functional Fe(III) reducing bacteria from actual complicated environment, and applying it to the bioremediation of organic, ammonia, and heavy metals contaminated groundwater will become a research topic in the future. There are a broad application prospects of Fe (III) (hydro)oxides bioreduction to groundwater bioremediation, which includes the in situ injection and permeable reactive barriers and the innovative Kariz wells system. The study provides an important reference for the treatment of reduced pollutants in contaminated groundwater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aburto-Medina A, Ball A S (2015). Microorganisms involved in anaerobic benzene degradation. Annals of Microbiology, 65(3): 1201–1213

    Article  CAS  Google Scholar 

  • Al-Abadleh H A (2015). Review of the bulk and surface chemistry of iron in atmospherically relevant systems containing humic-like substances. RSC Advances, 5(57): 45785–45811

    Article  CAS  Google Scholar 

  • Amstaetter K, Borch T, Kappler A (2012). Influence of humic acid imposed changes of ferrihydrite aggregation on microbial Fe(III) reduction. Geochimica et Cosmochimica Acta, 85: 326–341

    Article  CAS  Google Scholar 

  • Anderson R T, Lovley D R (2000). Anaerobic bioremediation of benzene under sulfate-reducing conditions in a petroleum-contaminated aquifer. Environmental Science & Technology, 34(11): 2261–2266

    Article  CAS  Google Scholar 

  • Anderson R T, Rooney-Varga J N, Gaw C V, Lovley D R (1998). Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum contaminated aquifers. Environmental Science & Technology, 32(9): 1222–1229

    Article  CAS  Google Scholar 

  • Anderson R T, Vrionis H A, Ortiz-Bernad I, Resch C T, Long P E, Dayvault R, Karp K, Marutzky S, Metzler D R, Peacock A, White D C, Lowe M, Lovley D R (2003). Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Applied and Environmental Microbiology, 69(10): 5884–5891

    Article  CAS  Google Scholar 

  • Benner S G, Hansel C M, Wielinga B W, Barber T M, Fendorf S (2002). Reductive dissolution and biomineralization of iron hydroxide under dynamic flow conditions. Environmental Science & Technology, 36(8): 1705–1711

    Article  CAS  Google Scholar 

  • Bjerg P L, Tuxen N, Reitzel L A, Albrechtsen H J, Kjeldsen P (2011). Natural attenuation processes in landfill leachate plumes at three Danish sites. Ground Water, 49(5): 688–705

    Article  CAS  Google Scholar 

  • Bongoua-Devisme A J, Cebron A, Kassin K E, Yoro G R, Mustin C, Berthelin J (2013). Microbial communities involved in Fe reduction and mobility during soil organic matter (SOM) mineralization in two contrasted paddy soils. Geomicrobiology Journal, 30(4): 347–361

    Article  CAS  Google Scholar 

  • Caccavo Jr F C, Das A (2002). Adhesion of dissimilatory Fe(III)-reducing bacteria to Fe(III) minerals. Geomicrobiology Journal, 19(2): 161–177

    Article  CAS  Google Scholar 

  • Chen Y, Wang H, Si Y B (2013). Research on the bioaccesibility of HgS by Shewanella oneidensis MR-1. Environmental Science, 34(11): 4466–4472 (in Chinese)

    CAS  Google Scholar 

  • Childers S E, Ciufo S, Lovley D R (2002). Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature, 416(6882): 767–769

    Article  CAS  Google Scholar 

  • Clement J C, Shrestha J, Ehrenfeld J G, Jaffe P R (2005). Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biology & Biochemistry, 37(12): 2323–2328

    Article  CAS  Google Scholar 

  • Coates J D, Ellis D J, Gaw C V, Lovley D R (1999). Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. International Journal of Systematic Bacteriology, 49(4): 1615–1622

    CAS  Google Scholar 

  • Cutting R S, Coker V S, Fellowes J W, Lloyd J R, Vaughan D J (2009). Mineralogical and morphological constraints on the reduction of Fe (III) minerals by Geobacter sulfurreducens. Geochimica et Cosmochimica Acta, 73(14): 4004–4022

    Article  CAS  Google Scholar 

  • Deng M (2010). Kariz wells in arid land and mountain-front depressed ground reservoir. Advances in Water Science, 21(6): 748–756 (in Chinese)

    Google Scholar 

  • Eisele T C, Gabby K L (2014). Review of reductive leaching of iron by anaerobic bacteria. Mineral Processing and Extractive Metallurgy Review, 35(2): 75–105

    Article  CAS  Google Scholar 

  • Essaid H I, Bekins B A, Cozzarelli I M (2015). Organic contaminant transport and fate in the subsurface: evolution of knowledge and understanding. Water Resources Research, 51(7): 4861–4902

    Article  CAS  Google Scholar 

  • Esther J, Sukla L B, Pradhan N, Panda S (2015). Fe (III) reduction strategies of dissimilatory iron reducing bacteria. Korean Journal of Chemical Engineering, 32(1): 1–14

    Article  CAS  Google Scholar 

  • Farkas M, Szoboszlay S, Benedek T, Révész F, Veres P G, Kriszt B, Táncsics A (2017). Enrichment of dissimilatory Fe(III)-reducing bacteria from groundwater of the Siklós BTEX-contaminated site (Hungary). Folia Microbiologica, 62(1): 63–71

    Article  CAS  Google Scholar 

  • Fortin D, Langley S (2005). Formation and occurrence of biogenic iron-rich minerals. Earth-Science Reviews, 72(1–2): 1–19

    Article  CAS  Google Scholar 

  • Fredrickson J K, Zachara J M, Kennedy D W, Dong H L, Onstott T C, Hinman N W, Li S M (1998). Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochimica et Cosmochimica Acta, 62(19–20): 3239–3257

    Article  CAS  Google Scholar 

  • Gavaskar A R (1999). Design and construction techniques for permeable reactive barriers. Journal of Hazardous Materials, 68(1–2): 41–71

    Article  CAS  Google Scholar 

  • Hansel C M, Benner S G, Fendorf S (2005). Competing Fe (II)-induced mineralization pathways of ferrihydrite. Environmental Science & Technology, 39(18): 7147–7153

    Article  CAS  Google Scholar 

  • Hansel C M, Benner S G, Neiss J, Dohnalkova A, Kukkadapu R K, Fendorf S (2003). Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow. Geochimica et Cosmochimica Acta, 67(16): 2977–2992

    Article  CAS  Google Scholar 

  • Heald S, Jenkins R O (1994). Trichloroethylene removal and oxidation toxicity mediated by toluene dioxygenase of Pseudomonas putida. Applied and Environmental Microbiology, 60(12): 4634–4637

    Article  CAS  Google Scholar 

  • Hori T, Aoyagi T, Itoh H, Narihiro T, Oikawa A, Suzuki K, Ogata A, Friedrich M W, Conrad R, Kamagata Y (2015). Isolation of microorganisms involved in reduction of crystalline iron(III) oxides in natural environments. Frontiers in Microbiology, 6(386): 1–16

    Google Scholar 

  • Komulainen S, Pursiainen J, Peramaki P, Lajunen M (2013). Complexation of Fe(III) with water-soluble oxidized starch. Stärke, 65(3–4): 338–345

    Article  CAS  Google Scholar 

  • Kossoff D, Dubbin W E, Alfredsson M, Edwards S J, Macklin M G, Hudson-Edwards K A (2014). Mine tailings dams: characteristics, failure, environmental impacts, and remediation. Applied Geochemistry, 51: 229–245

    Article  CAS  Google Scholar 

  • Kostka J E, Nealson K H (1995). Dissolution and reduction of magnetite by bacteria. Environmental Science & Technology, 29(10): 2535–2540

    Article  CAS  Google Scholar 

  • Krumholz L R, Sharp R, Fishbain S S (1996). A freshwater anaerobe coupling acetate oxidation to tetrachloroethylene dehalogenation. Applied and Environmental Microbiology, 62(11): 4108–4113

    Article  CAS  Google Scholar 

  • Kügler S, Cooper R E, Wegner C E, Mohr J F, Wichard T, Küsel K (2019). Iron-organic matter complexes accelerate microbial iron cycling in an iron-rich fen. Science of the Total Environment, 646: 972–988

    Article  CAS  Google Scholar 

  • Latta D E, Gorski C A, Boyanov M I, O’Loughlin E J, Kemner K M, Scherer M M (2012). Influence of magnetite stoichiometry on U(VI) reduction. Environmental Science & Technology, 46(2): 778–786

    Article  CAS  Google Scholar 

  • Li L, Benson C H, Lawson E M (2005). Impact of mineral fouling on hydraulic behavior of permeable reactive barriers. Ground Water, 43(4): 582–596

    Article  CAS  Google Scholar 

  • Li L, Qu Z, Jia R, Wang B, Wang Y, Qu D (2017). Excessive input of phosphorus significantly affects microbial Fe(III) reduction in flooded paddy soils by changing the abundances and community structures of Clostridium and Geobacteraceae. Science of the Total Environment, 607–608: 982–991

    Article  CAS  Google Scholar 

  • Li R, Jiang Y, Xi B, Li M, Meng X, Feng C, Mao X, Liu H, Jiang Y (2018a). Raw hematite based Fe(III) bio-reduction process for humified landfill leachate treatment. Journal of Hazardous Materials, 355: 10–16

    Article  CAS  Google Scholar 

  • Li X, Huang Y, Liu H W, Wu C, Bi W, Yuan Y, Liu X (2018b). Simultaneous Fe(III) reduction and ammonia oxidation process in Anammox sludge. Journal of Environmental Sciences (China), 64: 42–50

    Article  Google Scholar 

  • Li X, Yuan Y, Huang Y, Liu H W, Bi Z, Yuan Y, Yang P B (2018c). A novel method of simultaneous NH4 + and NO3 removal using Fe cycling as a catalyst: Feammox coupled with NAFO. Science of the Total Environment, 631–632: 153–157

    Google Scholar 

  • Liao Z, Cirpka O A (2011). Shape-free inference of hyporheic traveltime distributions from synthetic conservative and smart tracer tests in streams. Water Resources Research, 47(7): 1–14

    Article  Google Scholar 

  • Lin B, Van Verseveld H W, Röling W F M (2002). Microbial aspects of anaerobic BTEX degradation. Biomedical and Environmental Sciences, 15(2): 130–144

    Google Scholar 

  • Liu C, Kota S, Zachara J M, Fredrickson J K, Brinkman C K (2001). Kinetic analysis of the bacterial reduction of goethite. Environmental Science & Technology, 35(12): 2482–2490

    Article  CAS  Google Scholar 

  • Liu C, Zachara J M, Foster N S, Strickland J (2007). Kinetics of reductive dissolution of hematite by bioreduced anthraquinone-2,6-disulfonate. Environmental Science & Technology, 41(22): 7730–7735

    Article  CAS  Google Scholar 

  • Lorah M M, Voytek M A (2004). Degradation of 1,1,2,2-tetrachloroethane and accumulation of vinyl chloride in wetland sediment microcosms and in situ porewater: biogeochemical controls and associations with microbial communities. Journal of Contaminant Hydrology, 70(1–2): 117–145

    Article  CAS  Google Scholar 

  • Lovley D R (1995). Bioremediation of organic and metal contaminants with dissimilatory metal reduction. Journal of Industrial Microbiology, 14(2): 85–93

    Article  CAS  Google Scholar 

  • Lovley D R (2001). Bioremediation. Anaerobes to the rescue. Science, 293(5534): 1444–1446

    Article  Google Scholar 

  • Lovley D R, Anderson R T (2000). Influence of dissimilatory metal reduction on fate of organic and metal contaminants in the subsurface. Hydrogeology Journal, 8(1): 77–88

    Article  CAS  Google Scholar 

  • Lovley D R, Giovannoni S J, White D C, Champine J E, Phillips E J, Gorby Y A, Goodwin S (1993). Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Archives of Microbiology, 159(4): 336–344

    Article  CAS  Google Scholar 

  • Lovley D R, Holmes D E, Nevin K P (2004). Advances in Microbial Physiology, vol. 49. Poole R K, ed., 219–286

  • Lovley D R, Phillips E J (1987). Rapid assay for microbially reducible ferric iron in aquatic sediments. Applied and Environmental Microbiology, 53(7): 1536–1540

    Article  CAS  Google Scholar 

  • Lovley D R, Woodward J C, Chapelle F H (1994). Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature, 370(6485): 128–131

    Article  CAS  Google Scholar 

  • Luu Y S, Ramsay J A (2003). Review: Microbial mechanisms of accessing insoluble Fe(III) as an energy source. World Journal of Microbiology & Biotechnology, 19(2): 215–225

    Article  CAS  Google Scholar 

  • Ma J, Ma C, Tang J, Zhou S, Zhuang L (2015). Mechanisms and applications of electron shuttle-mediated extracellular electron transfer. Progress in Chemistry, 27(12): 1833–1840 (in Chinese)

    CAS  Google Scholar 

  • Machala L, Tucek J, Zboril R (2011). Polymorphous transformations of nanometric iron(III) oxide: A review. Chemistry of Materials, 23(14): 3255–3272

    Article  CAS  Google Scholar 

  • Martin T A, Kempton J H (2000). In situ stabilization of metal-contaminated groundwater by hydrous ferric oxide: An experimental and modeling investigation. Environmental Science & Technology, 34(15): 3229–3234

    Article  CAS  Google Scholar 

  • Mejia J, Roden E E, Ginder-Vogel M (2016). Influence of oxygen and nitrate on Fe (Hydr)oxide mineral transformation and soil microbial communities during redox cycling. Environmental Science & Technology, 50(7): 3580–3588

    Article  CAS  Google Scholar 

  • Nealson K H, Saffarini D (1994). Iron and manganese in anaerobic respiration: Environmental significance, physiology, and regulation. Annual Review of Microbiology, 48(1): 311–343

    Article  CAS  Google Scholar 

  • Netto L E S, Stadtman E R (1996). The iron-catalyzed oxidation of dithiothreitol is a biphasic process: Hydrogen peroxide is involved in the initiation of a free radical chain of reactions. Archives of Biochemistry and Biophysics, 333(1): 233–242

    Article  CAS  Google Scholar 

  • O’Loughlin E J, Gorski C A, Scherer M M, Boyanov M I, Kemner K M (2010). Effects of oxyanions, natural organic matter, and bacterial cell numbers on the bioreduction of lepidocrocite (gamma-FeOOH) and the formation of secondary mineralization products. Environmental Science & Technology, 44(12): 4570–4576

    Article  CAS  Google Scholar 

  • Park W, Nam Y, Lee M, Kim T (2009). Anaerobic ammonia-oxidation coupled with Fe3+ reduction by an anaerobic culture from a piggery wastewater acclimated to NH4 +/Fe3+ medium. Biotechnology and Bioprocess Engineering; BBE, 14(5): 680–685

    Article  CAS  Google Scholar 

  • Puls R W, Blowes D W, Gillham R W (1999). Long-term performance monitoring for a permeable reactive barrier at the U.S. Coast Guard Support Center, Elizabeth City, North Carolina. Journal of Hazardous Materials, 68(1–2): 109–124

    Article  CAS  Google Scholar 

  • Qian F, Wang H, Ling Y, Wang G, Thelen M P, Li Y (2014). Photoenhanced electrochemical interaction between Shewanella and a hematite nanowire photoanode. Nano Letters, 14(6): 3688–3693

    Article  CAS  Google Scholar 

  • Rayu S, Karpouzas D G, Singh B K (2012). Emerging technologies in bioremediation: Constraints and opportunities. Biodegradation, 23(6): 917–926

    Article  CAS  Google Scholar 

  • Roden E E, Urrutia M M (2002). Influence of biogenic Fe(II) on bacterial crystalline Fe(III) oxide reduction. Geomicrobiology Journal, 19(2): 209–251

    Article  CAS  Google Scholar 

  • Roden E E, Zachara J M (1996). Microbial reduction of crystalline iron (III) oxides: Influence of oxide surface area and potential for cell growth. Environmental Science & Technology, 30(5): 1618–1628

    Article  CAS  Google Scholar 

  • Savard M M, Paradis D, Somers G, Liao S, Van Bochove E (2007). Winter nitrification contributes to excess NO3 in groundwater of an agricultural region: A dual-isotope study. Water Resources Research, 43(6): 1–10

    Article  CAS  Google Scholar 

  • Sawayama S (2006). Possibility of anoxic ferric ammonium oxidation. Journal of Bioscience and Bioengineering, 101(1): 70–72

    Article  CAS  Google Scholar 

  • Scott D T, Mcknight D M, Blunt-Harris E L, Kolesar S E, Lovley D R (1998). Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environmental Science & Technology, 32(19): 2984–2989

    Article  CAS  Google Scholar 

  • Shi Z, Zachara J M, Shi L, Wang Z, Moore D A, Kennedy D W, Fredrickson J K (2012). Redox reactions of reduced flavin mononucleotide (FMN), riboflavin (RBF), and anthraquinone-2,6-disulfonate (AQDS) with ferrihydrite and lepidocrocite. Environmental Science & Technology, 46(21): 11644–11652

    Article  CAS  Google Scholar 

  • Shrestha J, Rich J J, Ehrenfeld J G, Jaffe P R (2009). Oxidation of ammonium to nitrite under iron-reducing conditions in wetland soils laboratory, field demonstrations, and push-pull rate determination. Soil Science, 174(3): 156–164

    Article  CAS  Google Scholar 

  • Thiruvenkatachari R, Vigneswaran S, Naidu R (2008). Permeable reactive barrier for groundwater remediation. Journal of Industrial and Engineering Chemistry, 14(2): 145–156

    Article  CAS  Google Scholar 

  • Tuntoolavest M, Burgos W D (2005). Anaerobic phenol oxidation by Geobacter metallireducens using various electron acceptors. Environmental Engineering Science, 22(4): 421–426

    Article  CAS  Google Scholar 

  • 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. International Journal of Systematic Bacteriology, 44(4): 612–619

    Article  CAS  Google Scholar 

  • VanStone N, Przepiora A, Vogan J, Lacrampe-Couloume G, Powers B, Perez E, Mabury S, Sherwood Lollar B (2005). Monitoring trichloroethene remediation at an iron permeable reactive barrier using stable carbon isotopic analysis. Journal of Contaminant Hydrology, 78(4): 313–325

    Article  CAS  Google Scholar 

  • Vogan J L, Focht R M, Clark D K, Graham S L (1999). Performance evaluation of a permeable reactive barrier for remediation of dissolved chlorinated solvents in groundwater. Journal of Hazardous Materials, 68(1–2): 97–108

    Article  CAS  Google Scholar 

  • Weber K A, Achenbach L A, Coates J D (2006). Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews. Microbiology, 4(10): 752–764

    Google Scholar 

  • Yang W H, Weber K A, Silver W L (2012). Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nature Geoscience, 5(8): 538–541

    Article  CAS  Google Scholar 

  • Yao H, Conrad R, Wassmann R, Neue H U (1999). Effect of soil characteristics on sequential reduction and methane production in sixteen rice paddy soils from China, the Philippines, and Italy. Biogeochemistry, 47(3): 269–295

    Article  CAS  Google Scholar 

  • You Y, Han J, Chiu P C, Jin Y (2005). Removal and inactivation of waterborne viruses using zerovalent iron. Environmental Science & Technology, 39(23): 9263–9269

    Article  CAS  Google Scholar 

  • Zachara J M, Fredrickson J K, Li S M, Kennedy D W, Smith S C, Gassman P L (1998). Bacterial reduction of crystalline Fe3+ oxides in single phase suspensions and subsurface materials. American Mineralogist, 83(11–12 Part 2): 1426–1443

    Article  CAS  Google Scholar 

  • Zboril R, Mashlan M, Petridis D (2002). Iron(III) oxides from thermal processes-synthesis, structural and magnetic properties, Mossbauer spectroscopy characterization, and applications. Chemistry of Materials, 14(3): 969–982

    Article  CAS  Google Scholar 

  • Zhang C L, Vali H, Romanek C S, Phelps T J, Liu S V (1998). Formation of single-domain magnetite by a thermophilic bacterium. American Mineralogist, 83(11–12 Part 2): 1409–1418

    Article  CAS  Google Scholar 

  • Zobrist J, Dowdle P R, Davis J A, Oremland R S (2000). Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environmental Science & Technology, 34(22): 4747–4753

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 21606214) and the Water Pollution Control and Control of Major National Science and Technology Projects in China (No. 2018ZX07109-003). We also acknowledge the valuable comments from the reviewers and the associate editor.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Beidou Xi or Rui Li.

Additional information

Highlights

• Microbial Fe(III) reduction is closely related to the fate of pollutants.

• Bioavailability of crystalline Fe(III) oxide is restricted due to thermodynamics.

• Amorphous Fe(III) (hydro)oxides are more bioavailable.

• Enrichment and incubation of Fe(III) reducing bacteria are significant.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, Y., Xi, B., Li, R. et al. Advances in Fe(III) bioreduction and its application prospect for groundwater remediation: A review. Front. Environ. Sci. Eng. 13, 89 (2019). https://doi.org/10.1007/s11783-019-1173-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-019-1173-9

Keywords

Navigation