Advances in Fe(III) bioreduction and its application prospect for groundwater remediation: A review
Yu Jiang, Beidou Xi, Rui Li, Mingxiao Li, Zheng Xu, Yuning Yang, Shaobo Gao
Advances in Fe(III) bioreduction and its application prospect for groundwater remediation: A review
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.
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.
Microbial Fe(III) reduction / Mechanism / Groundwater contamination / Remediation
[1] |
Aburto-Medina A, Ball A S (2015). Microorganisms involved in anaerobic benzene degradation. Annals of Microbiology, 65(3): 1201–1213
CrossRef
Google scholar
|
[2] |
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
CrossRef
Google scholar
|
[3] |
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
CrossRef
Google scholar
|
[4] |
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
CrossRef
Google scholar
|
[5] |
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
CrossRef
Google scholar
|
[6] |
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
CrossRef
Pubmed
Google scholar
|
[7] |
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
CrossRef
Pubmed
Google scholar
|
[8] |
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
CrossRef
Pubmed
Google scholar
|
[9] |
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
CrossRef
Google scholar
|
[10] |
Caccavo Jr F C, Das A (2002). Adhesion of dissimilatory Fe(III)-reducing bacteria to Fe(III) minerals. Geomicrobiology Journal, 19(2): 161–177
CrossRef
Google scholar
|
[11] |
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)
Pubmed
|
[12] |
Childers S E, Ciufo S, Lovley D R (2002). Geobacter metallireducensaccesses insoluble Fe(III) oxide by chemotaxis. Nature, 416(6882): 767–769
CrossRef
Pubmed
Google scholar
|
[13] |
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
CrossRef
Google scholar
|
[14] |
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
CrossRef
Pubmed
Google scholar
|
[15] |
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
CrossRef
Google scholar
|
[16] |
Deng M (2010). Kariz wells in arid land and mountain-front depressed ground reservoir. Advances in Water Science, 21(6): 748–756 (in Chinese)
|
[17] |
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
CrossRef
Google scholar
|
[18] |
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
CrossRef
Google scholar
|
[19] |
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
CrossRef
Google scholar
|
[20] |
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
CrossRef
Pubmed
Google scholar
|
[21] |
Fortin D, Langley S (2005). Formation and occurrence of biogenic iron-rich minerals. Earth-Science Reviews, 72(1–2): 1–19
CrossRef
Google scholar
|
[22] |
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
CrossRef
Google scholar
|
[23] |
Gavaskar A R (1999). Design and construction techniques for permeable reactive barriers. Journal of Hazardous Materials, 68(1-2): 41–71
CrossRef
Pubmed
Google scholar
|
[24] |
Hansel C M, Benner S G, Fendorf S (2005). Competing Fe (II)-induced mineralization pathways of ferrihydrite. Environmental Science & Technology, 39(18): 7147–7153
CrossRef
Pubmed
Google scholar
|
[25] |
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
CrossRef
Google scholar
|
[26] |
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
Pubmed
|
[27] |
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
CrossRef
Pubmed
Google scholar
|
[28] |
Komulainen S, Pursiainen J, Peramaki P, Lajunen M (2013). Complexation of Fe(III) with water-soluble oxidized starch. Stärke, 65(3–4): 338–345
CrossRef
Google scholar
|
[29] |
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
CrossRef
Google scholar
|
[30] |
Kostka J E, Nealson K H (1995). Dissolution and reduction of magnetite by bacteria. Environmental Science & Technology, 29(10): 2535–2540
CrossRef
Pubmed
Google scholar
|
[31] |
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
Pubmed
|
[32] |
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
CrossRef
Pubmed
Google scholar
|
[33] |
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
CrossRef
Pubmed
Google scholar
|
[34] |
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
CrossRef
Pubmed
Google scholar
|
[35] |
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
CrossRef
Pubmed
Google scholar
|
[36] |
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
CrossRef
Pubmed
Google scholar
|
[37] |
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
CrossRef
Pubmed
Google scholar
|
[38] |
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
CrossRef
Pubmed
Google scholar
|
[39] |
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
CrossRef
Google scholar
|
[40] |
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
Pubmed
|
[41] |
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
CrossRef
Pubmed
Google scholar
|
[42] |
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
CrossRef
Pubmed
Google scholar
|
[43] |
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
CrossRef
Pubmed
Google scholar
|
[44] |
Lovley D R (1995). Bioremediation of organic and metal contaminants with dissimilatory metal reduction. Journal of Industrial Microbiology, 14(2): 85–93
CrossRef
Pubmed
Google scholar
|
[45] |
Lovley D R (2001). Bioremediation. Anaerobes to the rescue. Science, 293(5534): 1444–1446
CrossRef
Pubmed
Google scholar
|
[46] |
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
CrossRef
Google scholar
|
[47] |
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
CrossRef
Pubmed
Google scholar
|
[48] |
Lovley D R, Holmes D E, Nevin K P (2004). Advances in Microbial Physiology, vol. 49. Poole R K, ed., 219–286
|
[49] |
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
Pubmed
|
[50] |
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
CrossRef
Pubmed
Google scholar
|
[51] |
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
CrossRef
Google scholar
|
[52] |
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)
|
[53] |
Machala L, Tucek J, Zboril R (2011). Polymorphous transformations of nanometric iron(III) oxide: A review. Chemistry of Materials, 23(14): 3255–3272
CrossRef
Google scholar
|
[54] |
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
CrossRef
Google scholar
|
[55] |
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
CrossRef
Pubmed
Google scholar
|
[56] |
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
CrossRef
Pubmed
Google scholar
|
[57] |
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
CrossRef
Pubmed
Google scholar
|
[58] |
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
CrossRef
Pubmed
Google scholar
|
[59] |
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
CrossRef
Google scholar
|
[60] |
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
CrossRef
Pubmed
Google scholar
|
[61] |
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
CrossRef
Pubmed
Google scholar
|
[62] |
Rayu S, Karpouzas D G, Singh B K (2012). Emerging technologies in bioremediation: Constraints and opportunities. Biodegradation, 23(6): 917–926
CrossRef
Pubmed
Google scholar
|
[63] |
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
CrossRef
Google scholar
|
[64] |
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
CrossRef
Google scholar
|
[65] |
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
CrossRef
Google scholar
|
[66] |
Sawayama S (2006). Possibility of anoxic ferric ammonium oxidation. Journal of Bioscience and Bioengineering, 101(1): 70–72
CrossRef
Pubmed
Google scholar
|
[67] |
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
CrossRef
Google scholar
|
[68] |
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
CrossRef
Pubmed
Google scholar
|
[69] |
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
CrossRef
Google scholar
|
[70] |
Thiruvenkatachari R, Vigneswaran S, Naidu R (2008). Permeable reactive barrier for groundwater remediation. Journal of Industrial and Engineering Chemistry, 14(2): 145–156
CrossRef
Google scholar
|
[71] |
Tuntoolavest M, Burgos W D (2005). Anaerobic phenol oxidation by Geobacter metallireducens using various electron acceptors. Environmental Engineering Science, 22(4): 421–426
CrossRef
Google scholar
|
[72] |
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
CrossRef
Pubmed
Google scholar
|
[73] |
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
CrossRef
Pubmed
Google scholar
|
[74] |
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
CrossRef
Pubmed
Google scholar
|
[75] |
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
CrossRef
Pubmed
Google scholar
|
[76] |
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
CrossRef
Google scholar
|
[77] |
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
CrossRef
Google scholar
|
[78] |
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
CrossRef
Pubmed
Google scholar
|
[79] |
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
CrossRef
Google scholar
|
[80] |
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
CrossRef
Google scholar
|
[81] |
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
CrossRef
Google scholar
|
[82] |
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
CrossRef
Google scholar
|
/
〈 | 〉 |