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.
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Aburto-Medina A, Ball A S (2015). Microorganisms involved in anaerobic benzene degradation. Annals of Microbiology, 65(3): 1201–1213
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
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
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
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
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
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
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
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
Caccavo Jr F C, Das A (2002). Adhesion of dissimilatory Fe(III)-reducing bacteria to Fe(III) minerals. Geomicrobiology Journal, 19(2): 161–177
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)
Childers S E, Ciufo S, Lovley D R (2002). Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature, 416(6882): 767–769
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
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
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
Deng M (2010). Kariz wells in arid land and mountain-front depressed ground reservoir. Advances in Water Science, 21(6): 748–756 (in Chinese)
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
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
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
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
Fortin D, Langley S (2005). Formation and occurrence of biogenic iron-rich minerals. Earth-Science Reviews, 72(1–2): 1–19
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
Gavaskar A R (1999). Design and construction techniques for permeable reactive barriers. Journal of Hazardous Materials, 68(1–2): 41–71
Hansel C M, Benner S G, Fendorf S (2005). Competing Fe (II)-induced mineralization pathways of ferrihydrite. Environmental Science & Technology, 39(18): 7147–7153
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
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
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
Komulainen S, Pursiainen J, Peramaki P, Lajunen M (2013). Complexation of Fe(III) with water-soluble oxidized starch. Stärke, 65(3–4): 338–345
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
Kostka J E, Nealson K H (1995). Dissolution and reduction of magnetite by bacteria. Environmental Science & Technology, 29(10): 2535–2540
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
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
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
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
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
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
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
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
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
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
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
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
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
Lovley D R (1995). Bioremediation of organic and metal contaminants with dissimilatory metal reduction. Journal of Industrial Microbiology, 14(2): 85–93
Lovley D R (2001). Bioremediation. Anaerobes to the rescue. Science, 293(5534): 1444–1446
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
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
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
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
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
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)
Machala L, Tucek J, Zboril R (2011). Polymorphous transformations of nanometric iron(III) oxide: A review. Chemistry of Materials, 23(14): 3255–3272
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
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
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
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
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
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
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
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
Rayu S, Karpouzas D G, Singh B K (2012). Emerging technologies in bioremediation: Constraints and opportunities. Biodegradation, 23(6): 917–926
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
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
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
Sawayama S (2006). Possibility of anoxic ferric ammonium oxidation. Journal of Bioscience and Bioengineering, 101(1): 70–72
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
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
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
Thiruvenkatachari R, Vigneswaran S, Naidu R (2008). Permeable reactive barrier for groundwater remediation. Journal of Industrial and Engineering Chemistry, 14(2): 145–156
Tuntoolavest M, Burgos W D (2005). Anaerobic phenol oxidation by Geobacter metallireducens using various electron acceptors. Environmental Engineering Science, 22(4): 421–426
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
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
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
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
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
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
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
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
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
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
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
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.
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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.
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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
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DOI: https://doi.org/10.1007/s11783-019-1173-9