Front. Environ. Sci. Eng.

2019, 13(6): 89
https://doi.org/10.1007/s11783-019-1173-9

REVIEW ARTICLE

Advances in Fe(III) bioreduction and its application prospect

for groundwater remediation: A review

Yu Jiang1,2, Beidou Xi (✉)1,2, Rui Li (✉)2, Mingxiao Li2, Zheng Xu2,3, Yuning Yang2,3, Shaobo Gao2,4
1 School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China
2 State Environmental Protection Key Laboratory of Simulation and Control of Groundwater Pollution, Chinese Research Academy of Environmental
Sciences, Beijing 100012, China
3 Municipal and Environmental Engineering College, Jilin Jianzhu University, Changchun 130118, China
4 School of Water Resources and Environment, China University of Geosciences (Beijing), Beijing 100083, China*

HIGHLIGHTS GRAPHIC ABSTRACT

• 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.

ARTICLE INFO
Article history:
Received 28 June 2019
Revised 31 August 2019
Accepted 13 October 2019
Available online 25 November 2019

Keywords:
Microbial Fe(III) reduction
Mechanism ABSTRACT
Groundwater contamination
Microbial Fe(III) reduction is a significant driving force for the biogeochemical cycles of C, O, P, S, N,
Remediation 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.
© Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

✉ Corresponding authors
E-mail: xibeidou@263.net (B. Xi); 518lirui@163.com (R. Li)
Special Issue—China Urban Water Environment and Water Ecology (Responsible Editors: Huijuan Liu & Shubo Deng)
2 Front. Environ. Sci. Eng. 2019, 13(6): 89
1 Introduction
Iron, the fourth abundant element by mass in the earth crust
(Al-Abadleh, 2015), primarily exists in the form of Fe(III)
(hydro)oxides in different sediment types in natural
environments (Weber et al., 2006; Hori et al., 2015).
There are mainly two forms of Fe(III) (hydro)oxides:
Amorphous (e.g., ferrihydrite) and crystalline (e.g.,
lepidocrocite, goethite, maghemite, and hematite) (Roden
and Urrutia, 2002; Machala et al., 2011). Crystalline Fe
(III) (hydro)oxides are more widespread due to its stable
physical/chemical properties at neutral alkalinity (Roden
and Zachara, 1996; Lovley et al., 2004). In the early 1860s,
Fe(III) reduction was considered to be an abiotic
phenomenon in sedimentary and subsurface environments
(Luu and Ramsay, 2003). However, in 1919, it was
identified as a bioprocess (Esther et al., 2015). Several
heterotrophic microorganisms, namely the Fe(III) reducing
bacteria (FeRB), can anaerobically reduce crystalline or
amorphous Fe(III) (hydro)oxides (Lovley et al., 1993;
Zachara et al., 1998). This microbial Fe(III) reducing
process is a significant driving force for the biogeochem-
ical cycles of C, O, P, S, N, and a number of metallic
elements on the Earth (Nealson and Saffarini, 1994; Zhang
et al., 1998). Moreover, it is one of the natural bio-
purification processes for organic contaminants that have
invaded the terrestrial ecosystem (Yao et al., 1999).
Accordingly, Fe(III) bioreduction has become a hot topic
of environmental science (Fortin and Langley, 2005;
Amstaetter et al., 2012; Li et al., 2017).
As shown in Fig. 1, aerobic degradation, denitrification,
Fig. 1 Microbial reduction processes in a petroleum-contaminated aquifer.
manganese oxides reduction, Fe(III) (hydro)oxides reduc-
tion, sulfate reduction, and methanogenesis are the
dominating natural bio-attenuation processes of reduced-
state contaminants such as organic matter, ammonium, and
arsenite in the groundwater plume (Lovley, 2001).
Pseudomonas putida spp. (Heald and Jenkins, 1994),
Nitrobacter agilis spp. (Savard et al., 2007), Geobacter
metallireducens spp. (Tuntoolavest and Burgos, 2005),
Desulfovibrio spp. (Anderson and Lovley, 2000) and
Methanobacteriales spp. (Lorah and Voytek, 2004) can
utilize dissolved oxygen, nitrate, manganese oxides, Fe
(III) (hydro)oxides, sulfate, or carbon dioxide as electron
acceptors, respectively, while gaining energy from the
degradation of contaminants (Eisele and Gabby, 2014).
The natural self-cleaning capacity of the groundwater eco-
system is limited by excessive pollutant invasion (Liao and
Cirpka, 2011). Appropriate electron acceptors addition can
enhance the natural biodegradation rate of organic
contaminants in groundwater (Lovley, 2001). As shown
in Fig. 1, ordered by their redox potential or oxidability,
different natural electron acceptors in the groundwater
plume follow: O2>NO3‒>Mn(IV)>Fe(III)>SO42‒>CO2.
Furthermore, a higher yield of the absolute free energy of
reduction reaction indicates more available bio-process
contribution (Luu and Ramsay, 2003). Fe(III) reduction
yields more free energy than both sulfate reduction and
methanogenesis, but less than O2, nitrate, and manganese
oxides reduction. The dissolved oxygen, the solubility or
replenishment of which is generally limited (Essaid et al.,
2015), can be rapidly depleted in severely contaminated
groundwater (Lovley, 2001). Nitrate and sulfate are typical
 Yu Jiang et al. Advances in Fe(Ⅲ) bioreduction and application for groundwater remediation
inorganic groundwater pollutants, while secondary pollu-
tants such as N2O, NH4+, NO2‒, H2S, and SO2 can
accumulate if nitrate or sulfate reduction is incomplete
(Bjerg et al., 2011). Since the abundance of Fe(III) (hydro)
oxides is relatively high than Mn(IV) oxides in many
anaerobic subsurface environments (e.g., groundwater
aquifers and freshwater lake sediments) (Eisele and
Gabby, 2014), microbial mediated Fe(III) reduction is a
more common phenomenon. Fe(III) bioreduction can be
more favorable for the artificial bioremediation of
petroleum (Anderson et al., 1998; Lin et al., 2002), and
landfill leachates (Li et al., 2018a) contaminated ground-
water. From the above, Fe(III) was more appropriate to
serve as additional electron acceptor to enhance the natural
bio-attenuation processes in groundwater plume.
Tailings are detrimental to the safety of groundwater
environment and human health surrounding mining areas
(Kossoff et al., 2014). It contains bioavailable metallic
compounds for environmental restoration (Lovley and
Anderson, 2000). Natural mineral materials are more cost-
effective than many artificial synthetic materials, e.g.,
nanometer materials, bio-ceramic, and activated carbon,
the preparation techniques of which are sophisticated,
energy-intensive, and generate secondary pollution (Vogan
et al., 1999). In comparison, Fe(III)-containing minerals
are appropriate additional electron acceptors, enhancing
natural bio-attenuation processes, and having good
application potential for groundwater remediation. The
present review summarizes the advances in the research on
microbial reduction mechanisms of various polymorphs of
Fe(III) (hydro)oxides, such as hematite (Liu et al., 2007),
lepidocrocite (O’Loughlin et al., 2010; Shi et al., 2012),
magnetite (Kostka and Nealson, 1995; Latta et al., 2012),
goethite (Roden and Zachara, 1996; Liu et al., 2001), and
ferrihydrite (Benner et al., 2002; Hansel et al., 2003;
Hansel et al., 2005). Furthermore, the critical restrictive
factors of microbial Fe(III) reducing processes are
analyzed and the environmental significance of Fe(III)
bioreduction in many pollutant removal processes has been
summarized (e.g. organic compounds, ammonia, and
heavy metals). At the same time, some relative applied
bioremediation technologies for contaminated ground
water are also introduced, which includes in situ injection
and permeable reactive barriers and the innovative Kariz
wells system.
2 Mechanisms of microbial Fe(III) (hydro)
oxides reduction
Fe(III) has a solubility of approximately 10–9 M at neutral
pH and is generally present as insoluble or crystalline
forms under anaerobic subsurface environments (Luu and
Ramsay, 2003). Magnetite (FeO-Fe2O3), hematite (α-
Fe2O3), and maghemite (γ-Fe2O3) are the natural crystal-
3
line forms (Fortin and Langley, 2005). β-Fe2O3 and ε-
Fe2O3 are two polymorphs of synthesized crystalline
nanoparticles (Zboril et al., 2002). The microbial avail-
ability of crystalline Fe(III) (hydro)oxides is restricted due
to its high thermodynamic stability (Fredrickson et al.,
1998). Previous reports have shown that only amorphous
Fe(III) (hydro)oxides are bioavailable (Qian et al., 2014).
However, it has recently been reported that crystalline Fe
(III) (hydro)oxides can be also utilized by FeRB (Lovley
and Phillips, 1987). As shown in Fig. 2, three mainstream
reaction mechanisms of microbial Fe(III) reduction have
been proposed.
(a) Direct contact reduction through the flagellum
As shown in Fig. 2(a), the flagella of FeRB adhere to the
surface of crystalline Fe(III) (hydro)oxides, where they
function as an electrical bridge that facilitates electron
transfer (Caccavo and Das, 2002). The main components
of flagellum are hydrophobic proteins (also called
nanowires). Flagellated cells (e.g. Shewanella) have been
demonstrated to be more hydrophobic than aflagellate cells
(Qian et al., 2014). Meanwhile, the majority of crystalline
Fe(III) (hydro)oxides are hydrophobic minerals. Accord-
ing to the hydrophobic interaction, FeRB can directly
contact the surface of crystalline Fe(III) (hydro)oxides via
their flagella (Childers et al., 2002). Therefore, flagellated
cells showed a more powerful reducing capacity and
oxidized organic matters to CO2 and H2O, while Fe(III)
was reduced to Fe(II).
(b) Indirect reduction mediated by ligands
As shown in Fig. 2(b), the microbiological ligands can
accelerate the dissolution of solid-phase Fe(III) (hydro)
oxides and provide a soluble Fe(III) form that is more
readily available to FeRB (Childers et al., 2002). The
major components of ligands are polymerase, melanin, and
nucleotides (Weber et al., 2006), which can accelerate the
rate of electron transfer between FeRB and Fe(III) (hydro)
oxides. In addition, the ligand can also be absorbed with Fe
(III)/Fe(II), and more Fe(III)/Fe(II) is bonded to the solid
surface, which leads to a higher bioavailability of Fe(III)
(hydro)oxides (Ma et al., 2015).
(c) Indirect reduction mediated by electron shuttles
As shown in Fig. 2(c), exogenous and endogenous
electron shuttles can transmit electrons to solid-phase Fe
(III) (hydro)oxides (Weber et al., 2006). Endogenous
electron shuttles, such as riboflavin and riboflavin mono-
nucleotide, are self-produced by FeRB. Exogenous
electron shuttles, e.g., anthraquinone-2,6-disulphonate
(AQDS), riboflavin, humic substances, and sulfur com-
pounds, are natural substance or artificially synthesized
materials (e.g. biochar) (Ma et al., 2015). Electron shuttle-
mediated extracellular electron transfer generally involves
the following reactions (Ma et al., 2015): the oxidized form
of electron shuttles (ESox) accepts electrons from the
oxidization of organic matters and becomes the reduced
form of electron shuttles (ESred); then, ESred transfer
4 Front. Environ. Sci. Eng. 2019, 13(6): 89
Fig. 2 Microbial strategies mediating electron transfer to crystalline Fe(III) (hydro)oxides (L refer to ligands): Direct contact reduction
through the flagellum (a), Indirect reduction by ligands (b) and electron shuttles (c).
electrons to extracellular electron acceptors and return to
ESox. Through these steps, electron shuttles can be
reversibly oxidized and reduced.
Compared to crystalline Fe(III) (hydro)oxides, amor-
phous Fe(III) (hydro)oxides are more bioavailable (Hori et
al., 2015). Fe(III) can be easier dissolved and quickly bio-
reduced by FeRB. The majority of biological Fe(III)
reduction mechanisms use direct contact reduction
between Fe(III) (hydro)oxides and FeRB. Moreover, the
indirect reduction process, which is mediated by ligands
and electron shuttles, also plays an important role in Fe(III)
reduction (Kügler et al., 2019). FeRB transfers the
electrons to Fe(III), Fe(III) is reduced to Fe(II), and
organic compounds are mineralized (Mejia et al., 2016).
3 Environmental significance
3.1 Degradation of organic compounds
Over the past several decades, the research of organics
degradation derived from Fe(III) (hydro)oxides bioreduc-
tion mostly focused on the macromolecular organics such
as aromatic hydrocarbons and chlorobenzene (Table 1). It
was first reported that laboratory-cultured Geobacter
metallireducens can anaerobically biodegrade aromatic
hydrocarbons, and FeRB can obtain necessary energy
required for metabolism (Lovley et al., 1993). Both in the
laboratory-scale condition as well as in a number of actual
petroleum-contaminated groundwater aquifer sites, Fe(III)
(hydro)oxides are the exclusive terminal electron accep-
tors. Benzene compounds can be oxidized to CO2 derived
from Geobacter metallireducens mediated Fe(III) reduc-
tion (Lovley et al., 1994). With the development of
microbial sequencing technology, mounted FeRB that can
degrade benzene compounds have been discovered.
Prominent examples are Geothrix fermentans (Coates et
al., 1999), Rhodoferax populations (Farkas et al., 2017),
and Deltaproteobacteria (Aburto-Medina and Ball, 2015).
In addition, the other FeRB has also been discovered that
can utilize chlorinated organics (tetrachloroethylene and
trichloroethylene) as terminal electron acceptors, including
Geobacteraceae (Krumholz et al., 1996), and Desulfito-
bacterium dehalogenans (Utkin et al., 1994). Currently,
most studies utilize pure cultured-FeRB for batch experi-
ments (Cutting et al., 2009; Bongoua-Devisme et al.,
2013). Considering the diversity of FeRB and the
complexity of the environment of actual contaminated
sites, the experimental conclusions obtained under labora-
tory-cultured FeRB conditions may deviate from the actual
environment. Furthermore, the functional genes of FeRB
and the mechanism between cells and Fe(III) (hydro)
oxides micro-interfaces both require further clarification.
The approach to extract, culture, and incubate the
functional FeRB from the complicated environment and
apply it to the bioremediation of organic contaminated
 Yu Jiang et al. Advances in Fe(Ⅲ) bioreduction and application for groundwater remediation 5

Table 1 Degradation of organic compounds with Fe(III) (hydro)oxides reduction

Organic contaminants Degradation reaction References
Formic acid HCOO‒ + 2Fe(III) ! HCO3‒ + 2Fe(II) + 2H+ Lovley et al. (1994);
Coates et al. (1999);
Lactic acid CH3CHOHCOO‒ + 4Fe(III) + 2H2O ! CH3COO‒ + HCO3‒ + 4Fe(II) + 5H+
Aburto-Medina and Ball (2015);
Pyruvic acid CH3COCOO‒ + 2Fe(III) + 2H2O ! CH3COO‒ + HCO3‒+ 2Fe(II) + 3H+ Farkas et al. (2017)
Benzoic acid C7H6O2 + 30Fe(III) + 19H2O ! 7HCO3‒ + 30Fe(II) + 37H+
Methylbenzene C7H8 + 36Fe(III) + 21H2O ! 7HCO3‒ + 36Fe(II) + 43H+
Phenol C6H5OH + 28Fe(III) + 17H2O ! 6HCO3‒ + 28Fe(II) + 3H+
P-cresol C7H8O + 34Fe(III) + 20H2O ! 7HCO3‒ + 34Fe(II) + 41H+
Syringic acid C9H10O5 + 36Fe(III) + 22H2O ! 9HCO3‒ + 36Fe(II) + 45H+
Ferulic acid C10H10O4 + 42Fe(III) + 26H2O ! 10HCO3‒ + 42Fe(II) + 52H+
Nicotinic acid C6H5NO2 + 22Fe(III) + 16H2O ! 6HCO3‒ + 22Fe(II) + NH4+ + 27H+
M-hydroxy benzoic acid C7H6O3 + 28Fe(III) + 18H2O ! 7HCO3‒ + 28Fe(II) + 35H+
2,5-DHBA C7H6O4 + 26Fe(III) + 17H2O ! 6HCO3‒ + 26Fe(II) + 32H+
M-cresol C7H8O + 34Fe(III) + 20H2O ! 7HCO3‒ + 34Fe(II) + 41H+
O-phthalic acid C8H6O4 + 30Fe(III) + 20H2O + 8HCO3‒ + 30Fe(II) + 38H+

groundwater will become a research topic of interest in the
future.
There are many factors that influence the rate and extent
of organic degradation derived from Fe(III) (hydro)oxides
bioreduction. The existing form of Fe(III) (hydro)oxides
(crystalline or amorphous) is decisive (Roden and Zachara,
1996). Most Fe(III) (hydro)oxides in the subsurface
environment exist in amorphous forms. The biodegrad-
ability of organics in the contaminated groundwater plume
is affected by the concentration of FeRB available Fe(III).
Furthermore, the contact path between Fe(III) (hydro)
oxides add FeRB is of great importance. Previous studies
reported that addition of the Fe(III) chelating agent
nitrilotriacetic acid (NTA) to petroleum-contaminated
aquifers significantly enhanced the degradation efficiency
of toluene. This is because NTA can catalyze the reductive
dissolution of crystalline Fe(III) (hydro)oxides to their
amorphous forms (Lovley et al., 1994). FeRB is no longer
necessary to directly contact Fe(III) (hydro)oxides. Except
for NTA, humic substances, AQDS, and other substances
can also accelerate this reaction. Electron spin resonance
(ESR) measurement indicates that the quinone groups of
the above-mentioned substances play an important role in
the electron transfer (Scott et al., 1998). In conclusion, the
limiting factors of Fe(III) (hydro)oxides bioreduction
should be further investigated to reveal the microscopic
mechanism. This will improve the bioavailability of
crystalline Fe(III) (hydro)oxides and accelerate the anae-
robic oxidation efficiency of organics.
3.2 Anaerobic oxidation of ammonia
The NH4+ oxidation coupled with the Fe(III) bioreduction
process under the anaerobic conditions is known as
Feammox, which is an important pathway for nitrogen
transformation in aquifer sediments. It was first discovered
in a forested riparian wetland located close to New Jersey,
USA (Clement et al., 2005), where NH4+ was oxidized to
NO2– and Fe(III) was reduced to Fe(II). Fe(III) served as
electron acceptor and the reaction formula of this process is
shown in the Eq. (1).
3Fe2 O3 ⋅0:5H2 O þ 10Hþ þ NH4 þ
↕ ↓6Fe2þ þ 8:5H2 O þ NO2 (1)
After this report, many studies explored the product of
Feammox under anaerobic conditions. Several studies
found that NH4+ can be oxidized to NO3– when it co-
existed with Fe(III)-Ethylenediaminetetraacetic acid
(EDTA) and anaerobic FeRB (Sawayama, 2006). Shrestha
et al. used 15N labeled 15NH4+ as electron donor and
detected 15N2 in the product, which directly indicated that
NH4+ was converted to N2 (Shrestha et al., 2009). Under
different conditions, NH4+ can be oxidized to disparate
products such as NO3, NO2, N2, or their combination
(Table 2). The distinct primary product may be related to
reaction conditions. Regarding reaction kinetics, Feammox
is more likely to produce N2 rather than NO2 and/or NO3.
Considering the strict reaction conditions of one-step
denitrification (such as dissolved oxygen and pH), how the
reaction conditions should be regulated to realize direct
oxidation (made NH4+ translate to N2) remains unknown
and should be studied in the future.
The discovery of Feammox expands the circulation of
nitrogen and provides novel research ideas for ground-
water contaminated with nitrogen pollutants. In recent
years, numerous studies have utilized EDTA as Fe(III)
chelate to explore the mechanism of Feammox (Netto and
Stadtman, 1996; Sawayama, 2006; Li et al., 2018b). In
6 Front. Environ. Sci. Eng. 2019, 13(6): 89
Table 2 Reactions of NH4+ and Fe3+ in different environments
Environment Degradation reaction
Wetland soil NH4+ + 6FeOOH + 10H+ ! NO2‒ + 6Fe2+ + 10H2O
Sludge after NH4+ + 2H2O + 6Fe3+ ! NO2‒ + 6Fe2+ + 8H+
domestication
NH4+ + 1.32NO2‒ ! 0.26NO3‒ + 1.02N2
Upland soil 3Fe(OH)3 + 5H+ + NH4+ ! 3Fe2+ + 9H2O + 0.5N2
+ +
6Fe(OH)3 + 10H + NH4 ! 6Fe 2+
+ 16H2O + NO2
+ +
8Fe(OH)3 + 14H + NH4 ! 8Fe 2+
+ 21H2O + NO3‒
general, Feammox can only completely react when the
concentration of bioavailable Fe(III) is high. Fe(III) is easy
to precipitate under non-acidic conditions, and EDTA can
be chelated with Fe(III), which ensures a smooth Feammox
(Sawayama, 2006). However, EDTA is organic and
contains nitrogen. It will therefore cause secondary
pollution if EDTA is used in the bioremediation of actually
contaminated sites and its use is not economically
practical. Currently, many studies focused on pH while
few focused on the influencing factors of Feammox. A
number of studies have shown that Feammox is a pH-
increasing process and the pH increases from 6.7 to 7.8
(Sawayama, 2006). Park et al. suggested that the optimum
pH of Feammox was around 6.8, which they corroborated
experimentally (Park et al., 2009). However, Yang et al.
suggested that only at a pH below 6.5, Feammox would
proceed smoothly and produce NO2–, which differed from
other researchers' conclusions (Yang et al., 2012). This is
possibly related to the existing form of Fe(III) (hydro)
oxides. Theoretically, Fe(III) tends to generate precipitates
under alkaline conditions (Komulainen et al., 2013).
Chemically, it is not likely that Feammox occurs under
overbasic conditions. Therefore, future research should
investigate the optimal influencing factors and mechanisms
underlying Feammox, and thus maximizing the denitrifi-
cation efficiency.
The combination of Feammox and Anammox may
provide more possibilities for the remediation of ground-
water pollution. The nitrosation control has always been a
difficult aspect of Anammox (Li et al., 2018c), but
Feammox can solve this problem well. If Feammox is
associated with Anammox, the NO2– produced during
Feammox reacts with NH4+, which promotes the reaction
of Anammox (Li et al., 2018b). When the bioreduced Fe
(II) has contact with air, it can be oxidized to Fe(III), thus
realizing Fe circulation, which increases the economic
efficiency. Isotope tracer technique and molecular biology
method should be combined to explore the product chain
and the realization approach of this reaction. Furthermore,
the species of functional microorganisms should also be
identified and the microbial survival characteristics should
be investigated. The combination of Feammox and
Anammox can provide a more efficient and convenient
method for groundwater pollutant denitrification.
Primary product References
Fe2+, NO2– Clement et al. (2005)
Fe2+, NO2‒, NO3‒, N2 Park et al. (2009)
Fe2+, NO2‒, NO3‒, N2 Yang et al. (2012)
‒
3.3 Heavy metal transformation
Dissimilatory Fe(III) reduction is closely related to the
existence of heavy metals in groundwater such as Cr(VI),
U(VI), and As(V). For example, Geobacter sulfurreducens
can reduce soluble and highly toxic Cr(VI) to the less
soluble and less toxic Cr(III), which can then be removed
from the groundwater via precipitation process (Lovley,
1995). In U(VI)-contaminated groundwater aquifers,
Shewanella spp. can reduce U(VI) to U(IV), which
transforms Uranium into a water-insoluble state that can
then be precipitated (Zobrist et al., 2000; Anderson et al.,
2003). According to the form transformation of heavy
metals, the mechanism of dissimilatory Fe(III) reduction
can be divided into redox, immobilization, and methyla-
tion. Through the redox process, the valence state of heavy
metals in groundwater such as Cr(VI), U(VI), and As(V)
can be changed during the metabolism of FeRB.
Immobilization refers to the process of immobilizing
heavy metals by Fe(III) oxides via surface coordination
and complexation. Methylation refers to the biomethyla-
tion process with which dissimilatory FeRB convert heavy
metals into organometallic compounds. For example,
Shewanella oneidensis MR-1 can convert inorganic
mercury, such as Hg(0) and Hg(II) to methylmercury
(MeHg), which causes the mutual transformation of
different forms of mercury in environment (Chen et al.,
2013). It should be noted that after methylation, heavy
metals are generally more toxic and may impose greater
harm to both humans and organisms. Microorganisms play
a vital role in the biomethylation process and organic
matter can act as the methyl carbon source. Seeking the
equilibrium of heavy metal methylation and demethylation
is greatly significant for the regulation of heavy metal
circulation (such as Hg) in soil sediments and groundwater.
The previous studies have investigated the mechanism
of heavy metal morphological transformation derived from
microbial Fe(III) reduction. It still needs to give a
systematic understanding of the occurrence and biotoxicity
of heavy metals in groundwater. Furthermore, identifying
an effective method for the removal of heavy metals in
groundwater has great significance. In consideration of the
great potential of FeRB in the bioremediation of heavy
metals in groundwater, the removal ability of FeRB for
 Yu Jiang et al. Advances in Fe(Ⅲ) bioreduction and application for groundwater remediation
different forms of heavy metals is unclear. The electron
donor should be added to stimulate FeRB growth which
should be increased to improve heavy metal removal
efficiency in the subsequent research. In addition, electron
shuttles (such as humus) should be added to increase the
electron transfer rate and ultimately improve the heavy
metal removal efficiency. Overall, the influence factor of
Fe(III) bioreduction on the valence state of heavy metals
has not been fully elucidated to date, and the reverse
damage effect of heavy metals on the reduction process of
dissimilatory Fe(III) remains to be further explored.
4 Application prospect of Fe(III) bioreduc-
tion for groundwater remediation
The following idea was proposed: the Fe(III) (hydro)
oxides, functional FeRB, artificial ligands and chelating
materials can be added to the injection wells for removing
the organic contaminants in groundwater aquifers, thus to
enhance the Fe(III) bioreduction process in these aquifers
(Fig. 3(a)). In general, FeRB used for in situ injection
groundwater remediation can be divided into two cate-
gories according to their source: indigenous and extra-
neous (Rayu et al., 2012). Currently, the research on the
functional genes of FeRB is still at a preliminary stage. It
still needs to further conduct in-depth research through the
scientific and technological methods. The technology of in
situ injection of functional microbes, and artificial
chelating materials has many unique advantages. First, it
can be constructed on polluted groundwater site in situ,
which can decrease the transportation costs and exert less
interference to the pollution site environment. Secondly,
enhancing the Fe(III) bioreduction process in the aquifer,
organic pollutants can be anaerobically oxidized into
inorganic substances such as carbon dioxide, water, and
bicarbonate. To a certain extent, these pollutants can be
degraded into harmless products or removed completely.
In addition, this technology can be used in conjunction
Fig. 3 Methods of engineering application: In situ injection (a), permeable reactive barriers (b), kariz system (c).
7
with other technologies to handle compound contaminated
sites.
Permeable reactive barrier (PRB) is an in situ ground-
water remediation technology that uses the specific
reaction medium to remove contaminants via physical,
chemical, and biological degradation (Martin and Kemp-
ton, 2000). At present, PRB gradually replaces the
traditional and liquid phase extraction technology due to
its low cost, no requirement for the additional power, the
sustainable treatment for various contaminants, good
treatment effect, and little interference in the ecological
environment (Gavaskar, 1999; VanStone et al., 2005).
Developed areas such as North America and Europe have
conducted a large number of PRB application cases
technology as well as practical engineering studies, and
commercial applications are gradually applied (Thiruver-
ikatachari et al., 2008). Currently, the key of PRB
technology is to find a suitable reaction medium, i.e., the
reaction medium needs to have a low secondary pollution
risk, good pollutant removal efficiency, and low treatment
cost. Otherwise, it will be difficult to widely apply this
technology to actual groundwater pollution sites. In
addition, the effect of PRB remediation is affected by the
types of pollutants, groundwater flow rates, and hydro-
geological parameters. For the actual application of PRB,
the most common PRB reaction medium is zero-valent
iron (You et al., 2005), which is a strong reductant. It has
the excellent reactivity with pollutants which can be
degraded to the micro-molecular organics, inorganic heavy
metals, and inorganic anions (Li et al., 2005). However, it
performs unfavorably in practical applications, e.g., it is
easy to inactivate fillers and block media, which may
produce more toxic byproducts (Puls et al., 1999). To
apply PRB technology to groundwater pollution sites that
are affected by various pollutant components, PRB
technology needs further improvement and perfection.
The chemical and biological reduction process of Fe(III)
(hydro)oxides transmitted by FeRB offers unique advan-
tages for the removal of organic pollutants, which is
8 Front. Environ. Sci. Eng. 2019, 13(6): 89
exemplified in the high removal efficiency of organisms,
excellent adaptability to sites with various types of organic
pollutants, and the thorough degradation of organisms.
However, by-products such as Fe(II) produced by the
chemical and biological reduction process of Fe(III)
(hydro)oxides also impose secondary risks. Besides, the
nitrite nitrogen produced by the anaerobic biological
oxidation of ammonia nitrogen has higher biological
toxicity. Specific groundwater contaminated sites have
less severe pollution, shallow groundwater levels, and poor
permeability of aquifers. Here, multi-level united PRB in
situ repair technology may be applied to remove different
types of pollutants in stages, which will finally maximize
the removal efficiency of pollutants (Fig. 3(b)). Currently,
China’s application of PRB technology is comparatively
limited, and it mainly focuses on aspects such as the
laboratory dynamic research of PRB and simulations of
pollution removal process through soil column experi-
ments. A few development and optimization studies focus
on novel reactive fillers and functional microorganism
species. The development and preparation of Fe(III)
(hydro)oxides reaction fillers that are available to FeRB
and offer good permeability should be supported. This will
lead to the acclimation and cultivation of functional FeRB
with good adaptability. This plays an important role in the
application of the in situ remediation of groundwater for
the chemical and biological reduction process of Fe(III)
(hydro)oxides.
The Kariz Well has a long history in China and is also
known as the well canal. Kariz is a particular irrigation
system in desert water-deficient regions of Xinjiang, China
(Deng, 2010). In a number of alluvial fan areas, the soil
contains gravels and most of the snow on the mountains
penetrates into the ground after melting, thus the ground-
water level is deep. The principle of the Kariz Well is to
find the groundwater source via the subsurface flow, dig
several vertical shafts at certain intervals, and then build an
underdrain at the bottom of the well that connects the wells
according to the relevant topography (Fig. 3(c)). The
outlets of underground and ground channels are connected
to bring groundwater to the surface. Therefore, we propose
that in groundwater contaminated sites with large hydrau-
lic gradient in the aquifer, the water diversion method of
Kariz can be combined with groundwater pollutant
remediation technology. This method would rely on
natural hydraulic gradients, which would realize the
drainage and follow-up treatment of contaminated ground-
water. The operability and maintenance of construction
process is strong, and the secondary risk is controllable. Fe
(III) (hydro)oxides can be used as the reaction medium for
the subsequent water-treatment reaction unit. Moreover,
nutrients and separately cultured FeRB functional micro-
bial bacterial liquid can be injected. Compared with
physical and chemical methods, this method offers the
advantages of simple operation and installation process, no
requirement for aeration, low energy consumption and
processing cost. According to the hydraulic gradient of the
aquifer, Kariz well groundwater pollution remediation
technology can be divided into buried type and surface
type. The main internal structure includes monitoring
wells, trunk pipes, and water-treatment reaction units.
Among these, the buried remediation technology is
suitable for contaminated sites with small surface gradi-
ents, and surface remediation technology can be applied to
contaminated sites with large surface gradients. When
0 < θ < arctanY/L, buried repair technology can be
adopted. When >arctanY/L, surface repair technology
can be used. “θ” represents the slope of the ground, “Y”
represents the best depth for the main trunk, and “L”
represents the length of the main trunk.
5 Conclusions
The research on mocrobial Fe(III) (hydro)oxides reduction
process is still at an initial stage. 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 mechanism of the process. Considering the growth
diversity of FeRB and the complexity of the actual
environment (much of which is a compound growth
system consisting of multiple FeRB, not a pure culture of a
single species), the research conclusions obtained under
pure culturing conditions in the laboratory may differ from
the actual situation. Furthermore, the approach to extract,
culture, and incubate the functional Fe(III) reducing
bacteria from actual complicated environment, and apply-
ing it to the bioremediation of organic, ammonia, and
heavy metals contaminated groundwater will become a
research topic in the future. The technology and principle
for the use of anaerobic microorganisms to degrade organic
pollutants by using Fe(III) (hydro)oxides as electron
receptor in the field of environmental pollution bioreme-
diation has wide application prospects. There are broad
application prospects of Fe(III) (hydro)oxides bioreduction
to groundwater bioremediation, which includes the in situ
injection and permeable reactive barriers and the innova-
tive Kariz wells system.
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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