Bioresource Technology: A 1 A 1 A A A A B C A

Bioresource Technology 297 (2020) 122416
Contents lists available at ScienceDirect
Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech
Recent advances in the recovery of metals from waste through biological T

processes
Zhengsheng Yua,1, Huawen Hana,1, Pengya Fenga, Shuai Zhaoa, Tuoyu Zhoua, Apurva Kakadea,
⁎
Saurabh Kulshresthab, Sabahat Majeedc, Xiangkai Lia,
a
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou University, No. 222 Tianshuinan Road, Lanzhou, Gansu
730000, People’s Republic of China
b
Faculty of Applied Sciences and Biotechnology, Shoolini University of Biotechnology and Management Sciences, Bajhol, Solan, Himachal Pradesh 173229, India
c
Department of Biosciences, COMSATS University, Park Road, Tarlai Kalan Islamabad, Islamabad 44000, Pakistan
G R A P H I C A L A B S T R A C T
A R T I C LE I N FO A B S T R A C T
Keywords: Wastes containing critical metals are generated in various fields, such as energy and computer manufacturing.
Biorecovery Metal-bearing wastes are considered as secondary sources of critical metals. The conventional physicochemical
Critical metals methods of metals recovery are energy-intensive and cause further pollution. Low-cost and eco-friendly tech-
Biological techniques nologies including biosorbents, bioelectrochemical systems (BESs), bioleaching, and biomineralization, have
Performance improvements
become alternatives in the recovery of critical metals. However, a relatively low recovery rate and selectivity
severely hinder their large-scale applications. Researchers have expanded their focus to exploit novel strain
resources and strategies to improve the biorecovery efficiency. The mechanisms and potential applicability of
modified biological techniques for improving the recovery of critical metals need more attention. Hence, this
review summarize and compare the strategies that have been developed for critical metals recovery, and pro-
vides useful insights for energy-efficient recovery of critical metals in future industrial applications.
1. Introduction because of their high scarcity, uneven distribution, and low substitut-
ability (Moss et al., 2011). Although the criteria for the criticality of
The rising demand for critical metals has attracted great attention metals varies worldwide and depends on national demands, there is a
⁎
Corresponding author.
E-mail address: xkli@lzu.edu.cn (X. Li).
1
These authors contributed equally to this work.
https://doi.org/10.1016/j.biortech.2019.122416
Received 26 September 2019; Received in revised form 8 November 2019; Accepted 10 November 2019
Available online 13 November 2019
0960-8524/ © 2019 Elsevier Ltd. All rights reserved.
Z. Yu, et al. Bioresource Technology 297 (2020) 122416
Fig. 1. Bisorbents derived from various bio-materials and their mechanisms for the recovery of critical metals.
consensus that critical metals comprise rare earth elements (REEs), relatively low selectivity always happened in biosorption process, and
platinum group elements (PGMs), and other metals, including nickel the application of BESs is still in lab-scale and low recovery rate oc-
(Ni), cobalt (Co), tellurium (Te), indium (In), gallium (Ga), mo- curred (Abourached et al., 2014; Qin et al., 2012), the mechanisms of
lybdenum (Mo), and tungsten (W) etc. (Hennebel et al., 2015; Won biomineralization processes are not clear. Thus, it is necessary to
et al., 2014). Among these metals, PGMs are representative of the high- ameliorate these technologies to obtain high recovery efficiencies.
scarcity group, 60% of the world’s cobalt stems from Congo, and 56% of Improvements and modifications of the application of the technol-
the lithium comes from Chile (Zhang et al., 2017). The increasing de- ogies to the biorecovery of critical metals have attracted interest (Park
mand for computer hard drives, permanent magnets, lamp phosphors, et al., 2017). For example, a light-emitting diode (LED) powder-adapted
catalysts and rechargeable batteries accelerated the exploitation of Acidithiobacillus ferrooxidans showed a 96% and 60% bioleaching rate
PGMs and REEs, resulting in the generation of various metal-bearing for nickel and gallium, respectively, while only 60% and 34% of these
solid and liquid wastes. Notably, there has been an explosive increase in metals leached when using a non-adapted A. ferrooxidans (Pourhossein
waste electric and electronic equipment (WEEE); the generation of and Mousavi, 2018). Moreover, a combination of microbial fuel cell
WEEE reached 44.7 million metric tons (Mt) in 2016, which equals (MFC) and microbial electrolysis cell (MEC) also improved the recovery
6.1 kg per inhabitant (Baldé et al., 2017). These E-wastes are estimated rate of critical metals (Shen et al., 2015). Besides, new methods or
over 52 million metric tons by 2021, which are regarded as better re- materials were applied to recover critical metals (Yuan et al., 2018).
cycling resources for critical metals (Işıldar et al., 2018), including However, there is a lack of comprehensive and comparative analyses of
silver (Ag), gold (Au), palladium (Pd), In, and REEs (Dias et al., 2018). the various biological recovery methods for guiding the development of
The traditional methods (e.g., solvent extraction, ion exchange, suitable techniques for the recovery of targeted critical metals. It is
coprecipitation, and crystallization) of recovery of critical metals from necessary to compare these technologies and explore suitable strategies
wastes are cost-inefficient or environment unfriendly (Xie et al., 2014; for recovery of critical metals at specific condition. The objectives of
Yin et al., 2017; Xie et al., 2014). Moreover, these methods are un- this review were to discuss the enhancement, mechanisms, current
feasible for the extraction of critical metals at low concentrations (Lo challenges, and future perspectives in the use of biorecovery technol-
et al., 2014). For example, the industrial practices developed for the ogies, and to explore the large-scale application of these techniques to
separation, purification, and pre-concentration of REEs are carried out waste management in the future.
in several pretreatment steps using strong acids or bases followed by
complex extraction cycles using organic solvents (Quinn et al., 2015). 2. Recovery of critical metals through biosorbents
These REE extraction methods are also energy-intensive and produce a
larg amount of toxic secondary wastes, including thorium, uranium, 2.1. Biosorbents
hydrogen fluoride, and acidic wastewater, thus causing severe en-
vironmental pollution (Dodson et al., 2015). Therefore, the develop- Biosorption is defined as the removal or binding of substances from
ment of alternative technologies that enable the efficient recovery of solution by bio-derived materials (Fig. 1), such as plant materials and
critical metals from wastes is highly desirable. microorganisms (e.g., algae, fungi, and bacteria) (Farooq et al., 2010;
Biological technologies offer obvious advantages because of their Ju et al., 2016). Biosorbents exhibited good performance for metal re-
low cost and eco-friendliness. Universally, biosorbents (Abdolali et al., moval and recovery from industrial effluents from the metallurgical
2017), bioelectrochemical systems (Nancharaiah et al., 2015), bio- industry and electroplating over the past few decades (Volesky and
leaching (Gu et al., 2018), and biomineralization (Lee et al., 2014) have Holan, 1995). The adsorption process has obvious superiority in the
been used to recover metals. Biosorbents showed high multiple-metal accessibility to renewable materials, simple processing, minimal sludge
binding properties (Abdolali et al., 2015; Abdolali et al., 2014). The production, high metal uptake rates (even in trace conditions), and
application of bioelectrochemical systems to metal removal and re- potential for regeneration and reusability (Vijayaraghavan and Yun,
covery was reported recently (Nancharaiah et al., 2015). The use of 2008). Generally, electrostatic interaction manipulates the mechanism
biomineralization contributed to the development of nanoparticles of adsorption of metals onto biosorbents, rather than chemical reaction,
(Mandal et al., 2006). Although these biotechnologies in recovery of ion exchange, and redox reaction (Cui and Zhang, 2008). In practical
critical metals showed superiority, disadvantages were also existed. A wastewater treatment, the competitive adsorption between critical
2
Table 1
Different adsorbents for recovery of critical metals.
Z. Yu, et al.
Critical Biosorbents Recovery Ability Reuse cycles Duration Estimated Adsorption model Mechanisms Potential application References
metals rate % mg/g costs ($/L)
Au (III) sugarcane bagasse 99 1497.5 NA 4h 0.5 Langmuir isotherm model hydroxyl Lab scale (Rubcumintara, 2015)
Au (III) extracellular proteins of 100 9700 NA 1h 0.7 Langmuir and Freundrich Cysteine and histidine 71% recovery rate from PCB (Han et al., 2017)
Tepidimonas fonticaldi AT-A2 models industrial wastewater
Au (III) Bacillus subtilis 100 119 NA 4h 0.82 ND Sulfhydryl Lab scale (Yu and Fein, 2017)
Au (III) Tetradesmus obliquus ND 169 NA 6h 0.5 Langmuir model NA Lab scale (Shen and Chirwa,
2018)
Au (III) Lysinibacillus sphaericus 100 NA 60% after 3 3h 0.5 ND S-layer protein Lab scale (Páez-Vélez et al.,
encapsulated into alginate cycles 2019)
matrix
Au (III) Fe3O4@SiO2@PT 100 917 NA 24 h 0.8 Langmuir model tannin Lab scale, acidic multiply (Fan et al., 2019)
metal ions system
Ag (I) Saccharomyces cerevisiae with 80 2.799 NA 2h 0.5 Langmuir and Freundlich CueR protein binding Lab scale (Tao et al., 2016)
enhanced displaying CueR model
protein
Pd (II) Providencia vermicola NA 119 NA 3h 0.64 Langmuir model amine, carboxyl, Lab scale, potential multiple (Xu et al., 2017)
hydroxyl, and industrial wastewater
phosphate groups
Pd (II) polyethylenimine-coated 97.4 216.9 > 5 cycles 24 h 0.8 Langmuir model NA Lab scale, potential for Pd(II) (Cho et al., 2016)
polysulfone Escherichia coli recovery from acidic
biomass composite fiber solutions
Pd (II) Aspergillus 65.7–98.8 4.28 NA 24 h 0.7 Langmuir model NA Lab scale (Godlewska-Żyłkiewicz
et al., 2019)
Pt (IV) Aspergillus 37.5–82.7 5.49 NA 24 h 0.7 Langmuir model NA Lab scale (Godlewska-Żyłkiewicz
et al., 2019)
3
Pt (IV) Providencia vermicola NA 30.2 NA 3h 0.64 Langmuir model amine groups Lab scale, potential multiple (Xu et al., 2017)
industrial wastewater
Pt (IV) surface-displaying EC20 on NA 239 NA 3h 2.3 Langmuir and Redlich-Peterson EC20 Lab scale (Tan et al., 2019)
Escherichia coli models
Pt (IV) polyethyleneimine modified NA 600 NA 24 h 1.1 Langmuir model NA Lab scale, simulated spent (Hong et al., 2019)
cellulose nano fibril from automobile catalyst leachate
tunicate
Dy (III) NaOH-treated bark powder of 92 55 NA 3h 0.7 Langmuier model Hydroxyl and carboxyl Lab scale (Devi and Mishra,
Mangifera indica 2019)
Eu (III) Bacillus thuringiensis 98 160 5 cycles 50 h 0.64 Langmuir model negative charge density Lab scale (Pan et al., 2017)
of functional groups
Eu (III) Saccharomyces cerevisiae 97.5 25.9 4 cycles 3h 0.69 Langmuier model amine, carboxyl, Lab scale in fluorescent lamp (Arunraj et al., 2019)
hydroxyl, and phosphor powder
polysaccharide
Eu (III) Acutodesmus acuminatus NA 174.2 NA 9h 2.6 Langmuier model phosphate groups, Lab scale (Furuhashi et al., 2019)
carboxyl group
Eu (III) Saccharomyces cerevisiae NA 19.41 > 4 cycles 1h 0.63 Langmuier model NA Lab scale (Arunraj et al., 2018)
immobilized on the chitosan
matrix
Sm (III) activated biochar from Opuntia 100 350 NA 24 h 0.5 NA carboxylic moieties Lab scale (Hadjittofi et al., 2016)
Ficus Indica
Sm (III) Turbinaria conoides 99.2 151.6 > 5 cycles 10 h 0.1 Langmuir and Redlich–Peterson negatively charged Lab scale (Vijayaraghavan et al.,
model binding sites such as 2017)
carboxyl
REEs LBT engineered E. coli 42–92 28.3 NA 0.5 h 0.64 NA lanthanide binding tag Lab scale, leachates from (Park et al., 2017)
metal-mine tailings and rare
earth deposits
(continued on next page)
metals ions and other ions and organic pollutants resulted in an obvious
decline in adsorption efficiency and selectivity for non-living biosor-
(Esmaeili and Beni,

(Tay et al., 2018)
(Ogi et al., 2016)

bents, and the growth conditions contributed to a low reuse possibility
for living cells as biosorbents (Vijayaraghavan and Yun, 2008). The
References
developments and modifications of biosorbents overcoming these
2015)
shortcomings which are essential for better application to actual was-
tewater treatment.
2.2. Improvements on adsorption capacity and selectivity

Lab scale, bauxite residue,
phosphogypsum, and
Potential application
Various biosorbents were developed recently to adsorb critical

metallurgicalslag
metals (Table 1). For non-living biosorbents, the introduction of func-

tional groups (e.g., eNH2, eC]O, eCOOH, and eOH) contributes to
Lab scale
Lab scale
metal sorption (Wang and Chen, 2009). So, improvements on the

density of functional groups would increase adsorption capacity. For
example, Lysinibacillus sphaericus encapsulated into alginate matrix re-
covered 100% of Au (III) after three hours at an initial concentration of
lanthanide binding tag
60 ppm (Páez-Vélez et al., 2019). In some cases, NaOH- or hexadecyl-

free amino acids
trimethylammonium bromide (CTAB)-modified bark powder of Man-

gifera indica improved dysprosium (Dy) (III) removal from aqueous
Mechanisms
solution (Devi and Mishra, 2019), with a resulting maximum adsorption

capacity of 55.04 mg/g and 34.4 mg/g, respectively. NaOH pretreat-
NA
ment provides additional active binding sites (eCOOH and eOH) on

the bark powder, which yielded better Dy (III) removal than that ob-
Dubinin–Radushkevich models
served for CTAB modification. A heat-treated E. coli cell suspension (90-

100℃) realized 100% W recovery in 1 h, while the biosorption time of
un-treated E. coli is more than 7 h. The zeta potential of the E. coli cells
NA: Not available. The estimated costs were calculated based on medium, instruments and other chemicals used in researches.
Adsorption model
which increased from 5 mV (un-treated) to 19–24 mV (heat-treated),

Langmuir and
contributed to the improved biosorption performance. Further analysis

with FTIR analysis, free amino acid, and LC-MS/MS revealed cell
membrane of the E. coli isdissolved in heat treatment, resulting in an
NA
NA
increase density of amino and carboxyl groups on the surface of E. coli

cells. The enhancement of positively charged amino groups in acidic
solution after heat treatment alters more tungsten anions adsorbed onto
costs ($/L)
Estimated
the cell surface (Ogi et al., 2016). The polyethyleneimine (PEI) mod-
0.64
ified cellulose nanofibril from tunicate showed the highest Pt adsorp-

0.2
0.1
tion capacity with 600 mg/g than PEI modified cellulose nanofibrils and
continuous
PEI modified cellulose nanocrystals obtained from hardwood pulp,

Duration
which is due to the highest negative charge and surface area of PEI
1.5 h
1h
modified cellulose nano-fibril from tunicate (Hong et al., 2019). Also,

this biosorbent exhibit higher selectivity to Pt than other metals. A
Reuse cycles
novel magnetic biosorbent was generated by immobilizing persimmon

continuous
tannin (PT) onto Fe3O4@SiO2 microspheres (Fe3O4@SiO2@PT) showed

high adsorption capacities (917.43 mg/g) of Au (III) with the partici-
NA
NA
pation of phenolic hydroxyl group. The high selectivity of Fe3O4@

SiO2@PT towards Au (III) was observed when Au (III), Pd (II), Zn (II),
Ability
Cu (II) and Fe (III) coexist in solution. The reduction of Au (III) to

297.8
mg/g
54.3
NA
metallic gold by Fe3O4@SiO2@PT realizes the convenient and efficient

recovery of Au (III) from acidic multiply metal ions system (Fan et al.,
2019).
Recovery
rate %
In contrast, extracellular proteins play a crucial role in the bio-

~70
100
sorption process of living-cell biosorbents. Similarly, an extracellular

91
protein from Tepidimonas fonticaldi sp. AT-A2, displayed an outstanding

adsorption capacity for gold (Au) (III) (9.7 mg Au/mg of protein). In the
Heat-treated Escherichia coli
treatment of industrial wastewater obtained from a manufacturing

factory of printed circuit boards (PCBs) (Han et al., 2017), the protein-
Sargassum glaucescens
based biosorbent also achieved a high adsorption capacity (1.45 mg

Au/mg of protein) and removal efficiency was reached to 71%. Sub-
curli-LBT E. coli
sequently, the overexpression of the CueR protein on the surface of

Biosorbents
Saccharomyces cerevisiae cells significantly enhanced the silver (Ag) (I)

Table 1 (continued)
binding capacity (Tao et al., 2016). The surface-engineered cells can

specifically adsorb 2.799 mg/g Ag (I) and exhibit increased adsorption
(87.3%) compared with the original cells. Overall, engineered S. cere-
visiae-CueR improved the Ag (I) adsorption capacity and selectivity. A
Tb (III)
Critical
W (VI)
Co (II)
metals
similar phage surface display technique also exhibited an affinity for Te

of ~100-fold and an affinity of Ni of ~20-fold compared with the
4
controls via the use of highly selective peptides (Braun et al., 2018). In
(Huang et al., 2015a)
(Huang et al., 2019a)

(Huang et al., 2019c)
(Wang et al., 2018b)

(Wang et al., 2017)
(Wang et al., 2015)

(Wang et al., 2015)
(Shen et al., 2015)
addition, displaying EC20 on the surface of E. coli increased the density
(Liu et al., 2019c)

(Ho et al., 2017b)
(Ho et al., 2017a)
(Kim et al., 2018)

(Lim et al., 2015)
(Lim et al., 2015)
(Ho et al., 2018)
(Ali et al., 2019)

of amine, carboxyl and phosphate groups and the biorecovery of Pt (IV)
reached to 112.67 mg/g, which is 1.6-fold higher than original strain
References
(Tan et al., 2019). In this regard, the expression of specific metal-

binding proteins on the surface of cells using the surface display tech-
nology may be a promising strategy to improve adsorption ability.
Columbic efficiency (%)
It is worth mentioning that the surface display technology offers

obvious advantages in the recovery of REEs (Park et al., 2017). Lan-
thanide-binding tags (LBTs) comprise 15–20 amino acids and can bind
terbium (Tb) (III) with high affinity (Sculimbrene and Imperiali, 2006).
The expression of the fusion protein OmpA–LBT on the surface of E. coli
19.89
12.74
21.61
28.74
increased the adsorption capacity to 28.3 ± 1.2 mg/g dry cell weight,
8.73
66.4
54.2
82.5
NA
NA
NA
NA
NA
NA
NA
NA
which is twice high than that detected in the un-induced control (Park
et al., 2017). During the treatment of different leachates (Lower Ra-
11340 mW/m3
Power density
844.0 mW/m2
5396 mW/m3
3795 mW/m3
8258 mW/m3
1930 mW/m3
3006 mW/m3
1500 mW/m3
dical, Round Top Mountain, and Togo leachates), an enhancement of

348 mW/m3
280 mW/m2
490 mW/m3
2–10-folds in the adsorption efficiency of REEs was observed through
the expression of LBTs on the cell surface of E. coli. The engineered E.
NA
NA
NA
NA
NA
coli strain selectively adsorbed REEs from the Lower Radical, Round
Top Mountain, and Togo leachates, which only contained 0.9, 5.5, and
Voltage/Applied voltage (mV)
0.5% REEs by mass of the total metals, respectively. Little to no ad-

sorption (< 10%) to the engineered E. coli strain was observed for Ca,
Ba, Zn, Mg, Na, K, Mn, and Rb from three leachates, despite their high
abundance. Thus, LBT-displaying E. coli systematically enhanced the
affinity and selectivity of REEs. Although the engineered E. coli was
selective for REEs over other metals, its performance in batch condi-
tions relied on the growth phase of living cells (Philip et al., 2000). To
410
441
340
970
650
710
230
340
863
520
200
500
340
210
300
address its low reuse potential, the engineered E. coli harboring a fused
85
protein (CsgA-LBT) for REE recovery via the secretion of functionalized

Estimated costs ($)
curli fibers (Tay et al., 2018). This extracellular display of curli-LBT

filters showed selective Tb (III)-binding capacity in the presence of 10-
fold higher concentrations of competing metals (i.e., Al (III), Fe (III), Ni
(II), and Ca (II)). The adsorbed fiber can be regenerated via simple
265
265
265
288
288
122
washing with diluted acid, which allows the reuse of the bacteria for
56
47
18
48
72
11
11
11
48
2
further material production. The curli-based filters are also more robust
Duration
at thetreat conditions that might compromise the viability of cell-based

sorbents or the structural integrity of other biopolymeric materials.
18 d
14 d
30 d
24 h
24 h
24 h
24 h
24 h
72 h
24 h
6h
6h
6h
6h
6h
4h
Overall, pretreatment of biosorbents contributes to the availability

of an increased number of metal-binding sites for enhancing adsorption
Recovery rate %
capacity, while filters generated using the surface display technology

favor high selectivity and recycling ability. The main advantages of
non-living biosorbents are the low cost of raw materials and high ad-
96.35
92.5
99.3
98.2
92.3
67.8
37.9
86.4
31.8
72.2
79.5
97.2
sorption capacity, while the relatively low selectivity is its short-

96
93
90
98
comings. Expressing metal-binding protein in living cells could improve

Concentration mg/L
the selectivity, while there are only a few metal-binding proteinsre-

ported previously. Hence, more attention should be paid to the dis-
covery of metal-binding protein. Most of the biosorbents were applied
in lab-scale synthetic wastewater, the breakthrough in performance on
16.88
2000
2000
1000
4000
Applications of MFC and MEC in critical metals recovery.
industrial application would be the main challenges in future studies.

500
200
100
200
50
30
40
50
50
40
96
3. Recovery of critical metals through bioelectrochemical systems

Membrane type/Applied voltage (V)
3.1. Bioelectrochemical systems
The bioelectrochemical systems (BESs) usually contains MFC, MEC,

microbial desalination cell, and other microbial electrochemical tech-
nologies (Logan et al., 2019). Over the past years, BESs have been
fabricated to deal with metal removal and recovery (Nancharaiah et al.,
2015). In which the MFC generates electricity, where the electrons
AEM
AEM
AEM
CEM
CEM
CEM
CEM
CEM
CEM
PEM
PEM
derived during microorganism metabolism can reduce some metal ions

0.2
0.5
0.5
0.3
NA
in wastewater on the cathode (Li and Zhou, 2019). This novel MFC-
mediated wastewater treatment can recover critical metals and produce
Critical metals
additional electricity simultaneously. Unlike that of the MFC, MEC

Mo (VI)
operation requires the use of external voltage, its application shifting

Mo(VI)
Mo(VI)
Table 2
Pt (IV)
In (III)
Co (II)
Co (II)
Co (II)
Co (II)
Co (II)
Ag (I)
Ag (I)
Ag (I)
Ag (I)
Ag (I)
Ag (I)
MEC
MFC
from hydrogen production (Cheng and Logan, 2011) to methane pro-

duction (Park et al., 2018), anaerobic digestion monitoring (Yu et al.,
5
2018), and metal removal (Qin et al., 2012). However, the low and concentration, temperature, and pH value are the main influential
unstable metal-recovery efficiencies of MFCs or MECs hardly meet the factors in the performance of MFC and MEC, which play important role
requirements of real wastewater treatment systems. in the metabolic mechanism of microorganisms in MFC and MEC.
Besides, the applied voltage used in MEC can affect the biorecovery rate
3.2. Improvements in biorecovery rate of critical metals. So, the exploration of optimal conditions for practical
applications of MEC and MFC on critical metals recovery from waste-
Many parameters (e.g., physicochemical factors, pure culture/mi- water can improve the biorecovery rate and provides a new insight in
crobial communities, and fabrication) affect the recovery behavior of the actual industrial wastewater treatment.
MFCs and MECs (Ali et al., 2019; Ho et al., 2017a). In the presence of
oxygen, MFCs showed an increased recovery rate of tungsten (W) and 4. Recovery of critical metals through bioleaching
molybdenum (Mo), by 2.4-fold and 1.3-fold, respectively (Table 2)
(Wang et al., 2017). A possible explanation for this observation is that 4.1. Bioleaching
the addition of oxygen accelerates the electron-transfer efficiency and
the generation of H2O2, resulting in enhanced reduction of W and Mo. Bioleaching has been employed by various researchers to recover
Furthermore, the externally one-time addition of H2O2 also improved W metals owing to a higher metal extraction rate from low-grade ores and
and Mo deposition (by 2.4 and 86.3%, respectively) and increased the complex resources (Gu et al., 2018; Xin et al., 2012). However, its
coulombic efficiency (CE) to 38.1%. In the MEC system, the combina- application is still in its infancy. A variety of chemolithotrophic bacteria
tion of light irradiation and in situ H2O2 production significantly in- (e.g., Acidithiobacillus thiooxidans and A. ferrooxidans), cyanogenic
creased the W and Mo deposition rate (shifted to 81.5 and 97.2%, re- bacteria (e.g., Chromobacterium violaceum, Pseudomonas sp., and Bacillus
spectively) along with 82.5% CE (Wang et al., 2018b). Light irradiation megaterium), and fungi (e.g., Aspergillus niger and Penicillium simpli-
altered the photocatalysis activity of W and Mo via a process in which cissimum) (Gu et al., 2018) are involved in the mobilization of metals
previous W and Mo deposits catalyzed the subsequent reduction of W from E-wastes (Table 3). These microorganisms produce inorganic or
(VI) and Mo (VI) by photogenerated electrons. In addition, oxygen- organic acids or cyanide to perform bioleaching process. The biogenic
exposing biocathode MFCs may exhibit a promising performance for the cyanide from microorganism metabolism was more secure than con-
recovery of cobalt from spent lithium-ions batteries (Huang et al., ventional chemical processes due to extremely lower concentrations
2015a). A nearly complete removal of W (97–98%), Mo (98–99%), and (Pollmann et al., 2018). In fact, bioleaching is only one first step in
acetate (95–96%) was obtained with an influent ratio of W:Mo:acetate metal recovery, these critical metals present dilute leachates can be
of 0.5:1.0:24 mM and a hydraulic residence time of 2 days in a 40 L recovered via classical methods (e.g. precipitation, comentation, sol-
cylindrical single-chamber MEC (Huang et al., 2019a). More im- vent extraction, ion exchange) (Li et al., 2013), newer approaches
portantly, the resultant wastewater treated with MEC meets national (membrane technologies and dialysis) and biobased approaches (bio-
wastewater discharge standards. adsorption, bioflotation, bio-reduction, microbial electrochemistry)
Microbial communities are the major driving force of metal re- (Hsu et al., 2019; Pollmann et al., 2018). Recently, much attention has
covery in the MFC or MEC system (Nancharaiah et al., 2015; Wu et al., been attributed to processes that allow the enhancement of the bio-
2018). After 25 days (MFC-Cr and MFC-Cu) and 10 days (MEC-Cd) of leaching rate from various wastes.
acclimatized incubation (Huang et al., 2015b), the complete and se-
lective metal reduction rates of Cr (VI), Cu (II), and Cd (II) reached 4.2. Improvements on the bioleaching rate
1.24 mg L−1 h−1, 1.07 mg L−1 h−1, and 0.98 mg L−1 h−1, respectively,
which is 2.5, 2.9, and 3.6 times higher than that observed for the non- Regarding the bioleaching process, pH adjustment significantly
adaptive controls. 16S rRNA sequencing revealed that microbial com- enhanced the bioleaching rate of Co and Ni from spent electric vehicle
munities with a lower diversity were observed in the adaptive groups Li-ion batteries (Xin et al., 2016). The release efficiencies of Co and Ni
vs. the control groups, and metal reduction had no significant impact on increased from 43.5 to 96% and from 38.3 to 97%, respectively, be-
the microbial communities of adaptive groups at the phylum and genus cause of the enhancement of the effect on cell growth. Similar results
levels (Huang et al., 2015b). Thus, the acclimatization of microbial were observed for the recovery of Li (I) and Co (II) from lithium cobalt
communities is beneficial for the improvement of critical metal bior- oxide by sulfur-oxidizing and iron-oxidizing bacteria (Wu et al., 2019b).
eduction and biorecovery from wastewaters. Another study first used The recovery of Li (I) and Co (II) by bacterial communities reached 100
MFC for the biorecovery of indium (In) from synthetic wastewater (Kim and 99.3% at 72 h compared with the chemical leaching method (91.4
et al., 2018), and reported that over 90% of In (III) was removed after and 94.2%, respectively). In addition to pH adjustment, the presence of
14 days of MFC operation; moreover, the cathode carbon electrode biochar led to a higher bioleaching efficiency of metals from E-wastes
generated amorphous and crystalline indium hydroxides. through the regulation of electron transfer from a Fe-mediated bacterial
Moreover, the combination of MFC with MEC yielded great progress community to metals (Wang et al., 2016).
in the recovery of critical metals. For example, higher Co (II) removal Microorganisms act as the prerequisite of the bioleaching process
rates (5.3 ± 0.4 mg L–1 h−1) was achieved at an initial Co (II) con- (Gu et al., 2018; Latorre et al., 2016; Ma et al., 2019). Although cya-
centration of 40 mg/L using MECs with biocathodes and driven by nogenic bacteria have been widely used for the bioleaching of precious
MFCs (Shen et al., 2015). This recovery rate is 3.3 times higher than metals, screening of novel isolates may provide increased performance.
observed for MECs with abiotic cathodes and driven by MFCs. The P. balearica SAE1 isolated from an e-waste recycling facility exhibited a
MFC–MEC hybrid systems were also applied to the recovery of other leaching rate of 68.5% for Au and of 33.8% for Ag from a 10 g/L pulp
metals, such as Cr, Pb, and Ni, with high removal rates of 32.7, 32.7, density under optimal conditions (Kumar et al., 2018). The cyanide
and 8.9 mg L−1 d−1 being achieved, respectively (Li et al., 2015b). production determines the recovery efficiency of precious metals. Yuan
Using the MEC-MEC coupled system together with adaptation strategies et al. found that maximum cyanide production by P. fluorescens strain
would be a potential approach to enhance the biorecovery rate of cri- P13 using optimized medium (6 g/L tryptone and 5 g/L yeast extract)
tical metals from wastewaters. was 1.5 times higher that of LB medium. Furthermore, the relationship
The application of MFC and MEC on the recovery of critical metals between cell growth and cyanide production revealed a novel kinetic
achieved great progress in recent years. These technologies conduct model for predicting cyanide production (Yuan et al., 2018). Another
removal of organic pollutants, recovery of critical metals and energy bacterial strain, Cellulosimicrobium funkei, from cadmium- and arsenic-
production simultaneously. However, biorecovery rates of critical me- contaminated soil showed an efficient leaching rate of 70% for gallium
tals are unstable and vary in larger range. The initial metal recovery from thin-film GaAs solar cell waste (Maneesuwannarat et al.,
6
Table 3
Bioleaching of critical metals.
Z. Yu, et al.
Critical Wastes sources microorganisms Pulp Estimated Duration Recovery Mechanisms Potential application References
metals density (g/ costs ($/L) rate %
L)
Au waste PCBs Pseudomonas balearica SAE1 10 0.64 7d 68.50 Produces hydrogen cyanide Lab scale, recovering precious gold (Kumar et al., 2018)
from e-waste
Au waste PCBs Chromobacterium violaceum 200 mesh 0. 4 7d 70.6 Produces hydrogen cyanide Lab scale, recovering gold from (Li et al., 2015a)
waste PCBs
Au waste PCBs Aspergillus niger 11 0.5 32 d 56 Produces hydrogen cyanide Lab scale, bioleaching of metals (Argumedo-Delira et al.,
from PCBs of cell phones or 2019)
computers
Ag waste PCBs Pseudomonas balearica SAE2 10 0.64 7d 33.80 Produces hydrogen cyanide Lab scale, recovering precious (Kumar et al., 2018)
silver from e-waste
Ag waste PCBs Sphingomonas sp. MXB8/C 0.5 0.52 35 d 54 form an Ag mirror Lab scale, recover metals from (Díaz-Martínez et al.,
WEEE 2019)
Au waste PCBs Orthopsilosis MXL20 0.5 0.52 35 d 44.20 form precipitates Lab scale, recover metals from (Díaz-Martínez et al.,
WEEE 2019)
REE FP Komagataeibacter hansenii 0.85 0.46 14 d 7.90 Dissolve the REE-compounds Lab scale, Leaching REE from FP (Hopfe et al., 2017)
powder
REE FP Zygosaccharomyces lentus 0.85 0.46 14 d 0.23 Dissolve the REE-compounds Lab scale, leaching REE from FP (Hopfe et al., 2017)
powder
REE FP Kombucha culture 0.85 0.32 14 d 7.20 Dissolve the REE-compounds Lab scale, leaching REE from FP (Hopfe et al., 2017)
powder
Sm EPs Aspergillus niger 0.0009 0.56 14 d 66.70 Produce Siderophores Lab scale, extract rare element (Osman et al., 2019)
from phosphorites
La EPs Aspergillus niger 0. 362 0.56 14 d 51 Produce Siderophores Lab scale, extract rare element (Osman et al., 2019)
7
from phosphorites
Ce EPs Aspergillus niger 0.866 0.56 14 d 50.10 Produce Siderophores Lab scale, extract rare element (Osman et al., 2019)
from phosphorites
Ga GaAs Cellulosimicrobium funkei 0.086 0.64 30 d 91 Amino acids of C. funkei are involved in Lab scale, bioleaching of gallium (Maneesuwannarat et al.,
Ga leaching from thin film GaAs solar cells 2016)
Ga LED Acidithiobacillus ferrooxidans 20 0. 4 30 d 60 NA Lab scale, direct metals (Pourhossein and
bioleaching from LED powder Mousavi, 2018)
Co arsenide Acidithiobacillus ferrooxidans and 20 0.46 8d 92 NA Lab scale, new approach to recycle (Giebner et al., 2019)
Leptospirillum ferriphilum semiconductor wastes
Co EV LIBs Acidithiobacillus thiooxidans and 10 0.48 11 d 96 Contact mechanism between the Lab scale, recover the valuable (Xin et al., 2016)
Leptospirillum ferriphilum cathodes material and cells metals from EV LIBs
Co EV LIBs Acidithiobacillus ferrooxidans and 100 0.2 2h 53.2 NA Lab scale, recovery of metals from (Boxall et al., 2018)
Acidithiobacillus thiooxidans LIB waste
Co LiCoO2 Leptospirillum ferriphilum and 15 0.4 7h 94.2 Hypothetical mechanism: electron Lab scale, commercial application (Wu et al., 2019b)
Sulfobacillus thermosulfidooxidans transfer or extracellular polymeric of the bioleaching of lithium-ion
substances that is beneficial for Co batteries.
recovery
Co high pressure Acidithiobacillus caldus S2, Leptospirillum 50 0.2 15 d 87.9 citric acid and sulfate dissolve Lab scale, industrial application of (Liu et al., 2019b)
acid leaching ferriphilum DX, Sulfobacillus acidophiles CoFe3(SO4)2(OH)6, Co (II) dissolved at the trace heavy metals removal
residue TPY, Ferroplasma thermophilum L1 low pH from high-pressure acid leaching
residue
In discarded LCDs Acidithiobacillus thiooxidans 16 0.4 12 d 100 NA Lab scale, recover In from (Jowkar et al., 2018)
discarded LCDs
In discarded LCDs Microbial community dominated by 15 0.4 8d 100 secrete enzymes and extracellular Lab scale, potential biological (Xie et al., 2019)
Acidithiobacillus polymeric substances leaching of In from liquid crystal
displays
PCBs: Printed Circuit Boards; FP: fluorescent phosphor; EPs: Egyptian Phosphorites; GaAs: gallium arsenide; LED: Light Emitting Diode; EV LIBs: electric vehicle Li-ion batteries; LCDs: liquid crystal displays; NA: Not
available. The estimated costs were calculated based on medium, instruments and other chemicals used in researches.
2016). The high concentration of metals from bioleaching process in- enhanced leaching efficiency, which is consistent with previous re-
hibited bacterial growth and activity (Natarajan and Ting, 2015), while search (Tran et al., 2011). Furthermore, pretreatment with a mixed
fungus exhibited a high metal-tolerance capacity (Xin et al., 2012; Zotti culture (e.g., A. ferrivorans and A. thiooxidans, or P. fluorescens and P.
et al., 2014). In contrast to bacterial bioleaching, fungal bioleaching has putida) yielded a 1.6-fold improvement in gold recovery from waste
several advantages, such as bioleaching at high pH, short lag phase PCBs (Işıldar et al., 2016). A novel step-wise indirect bioleaching
(Moore et al., 2008), and secreting organic acids (Jadhav et al., 2016). method was proposed by addition of biogenic ferric to improve re-
Some fungus, such as Aspergillus genus, exhibited a high recovery of covery efficiency of copper, nickel, and gallium from waste light-
90–95% from Zn–Mn battery and Ni–Cd battery via the formation of emitting diodes (LED) using adapted A. ferrooxidans. Compared to di-
citric and oxalic acids (Kim et al., 2016), which was highly comparable rect bioleaching, step-wise indirect bioleaching achieved 83, 97, and
or even better than bacterial or acid leaching (Biswal et al., 2018). In 84% recovery efficiency for copper, nickel, and gallium respectively at
addition, a fungus strain Penicillium expansum can bioconcentrate Lan- a pulp density of 20 g/ L and the leaching time reduced from 30 days to
thanum (up to 390 ppm) and Terbium (up to 1520 ppm) from WEEE 15 days (Pourhossein and Mousavi, 2019).
after three weeks of cultivation (Di Piazza et al., 2017), its relative Bioleaching has been widely used for commercial metal extraction
mechanism affecting this process needs further studies. These evidence from mining ores (Panda et al., 2015). Recently, this technology was
indicate that the exploration of novel strain resources is an effective developed to recover metals from solid wastes. Various mature ex-
strategy for improving bioleaching rates. perience in commercial metal extraction can be used for metal re-
During bioleaching, forming critical metals in the leaching solution covery. Nevertheless, the relative low metal concentration and multiple
can cause potential toxicity to microorganisms, thus adaptation strategy metal toxicity exist in solid wastes hinder the application of bioleaching
can contribute to improving microbial resistance (Ma et al., 2019). and decrease recovery efficiency. Different strategies were developed to
Some membrane proteins (transporter) and EPS alleviate the toxicity of solve these problems, while these strategies only focus on specific me-
metals via adsorbing on the surface of cell or increasing extracellular tals. For other critical metals, the feasibility of similar strategies should
efflux. The adaptation of Acidithiobacillus ferrooxidans treated with be investigated for more broad applications.
varied concentrations of LED powder (5–25 g/L) resulted in higher Fe
(III) levels, cell amounts, oxidation-reduction potential, and lower pH 5. Recovery of critical metals through biomineralization
vs. the non-adapted group (Pourhossein and Mousavi, 2018). The
adapted A. ferrooxidans exhibited an increase of 1.6-fold leaching rate 5.1. Biomineralization
of nickel and gallium when compared to that non-adapted A. ferroox-
idans. Such adaptation strategy achieved a recovery rate of 100% of Biomineralization of critical metals is performed by microorgan-
indium from discarded liquid crystal displays by A. thiooxidans (Jowkar isms, usually via detoxification process. As shown in Table 4, the Pho-
et al., 2018). Similarly, adapted fungi A. niger improved the organic mopsis sp. XP-8 fungus selectively recovered around 80% of Au from
acid production and leaching efficiency (Bahaloo-Horeh et al., 2018), electronic wastewater without any pretreatment. In simulated elec-
the high metals recovery was achieved by leaching using biogenic acids tronic water containing different concentrations of Au (III), K (I), Na (I),
rather than chemical leaching (Bahaloo-Horeh et al., 2016). A novel Ni (II), Ca (II), Co (II), Al (III), and Fe (III), this fungus exhibited a
strategy of three-step (consortium construction, directed evolution, and recovery ability of 68.07% (Xu et al., 2019). Moreover, the metal-re-
chemostat selection) adaptive laboratory evolution was proposed to ducing bacterium Shewanella algae recovered three PGMs (platinum
improve bioleaching efficiency. The results showed that iron recovery (IV), palladium (II), and rhodium (III)) from the aqua regia leachate of
rate increased by 26 and 55% at pH 1.5 and 0.75 respectively by using spent automotive catalysts simultaneously (Saitoh et al., 2017). Two Fe
developed consortium than original consortium (Liu et al., 2019a). (III)-reducing bacteria, Acidocella aromatica sp. PFBCT and Acidiphilium
Pathak et al. proposed addition of catalysts can improve the dissolution cryptum sp. SJH, were applied to recover palladium (Pd) from acidic Pd
and bioleaching rate (Pathak et al., 2017). With the addition of citric (II) solutions and spent catalyst leachates via bionanoparticles (Okibe
acid, Fe (II) and elemental sulfur, recovery rate of cobalt and copper by et al., 2017).
moderate thermophiles (A. caldus S2, Leptospirillum ferriphilum DX,
Sulfobacillus acidophiles TPY, Ferroplasma thermophilum L1) from high 5.2. Recent progress in the mechanistic study of biomineralization
pressure acid leaching residue reached to 87.91 and 58.52% with pulp
density of 50 g/L (Liu et al., 2019b). Subsequently, aerobic activated Despite the wide application of biomineralization to waste treat-
sludge was domesticated for leaching indium by incubation with Starky ment and nanoparticle formation, the underlying mechanisms remain
medium, 9 K medium, and a mix of the two media for 7 days, to induce elusive. Research has confirmed the crucial role of nitrate reductase in
microbial communities via the S-mediated pathway, Fe-mediated the extracellular bioreduction of silver by P. aeruginosa JP1 (Ali et al.,
pathway, and mixed S- and Fe-mediated pathway (Xie et al., 2019). The 2017). Purified nitrate reductase treatment accompanied by AgNO3 can
bioleaching efficiencies of the S-mediated pathway reached approxi- transfer electrons from the nitrate molecule to silver, resulting in the
mately 100%, which was the highest among these three pathways (0% formation of nanoparticles. A novel molybdoprotein-mediated me-
for the Fe-mediated pathway and 78% for the mixed pathway). A rea- chanism was involved in aerobic Pd (II) reduction by E. coli mutants
sonable explanation for this observation is that Acidithiobacillus was the deficient in different oxidoreductase processes, using formate as the
dominant genus in the S-mediated pathway communities, based on electron donor (Foulkes et al., 2016); this was distinct from the hy-
sequencing data of 16S rRNA gene. drogenase-mediated Pd (II) reduction pathway of anaerobic E. coli
The two-step method is a more efficient metal mobilization process cultures described previously. Recently, the mechanism of gold biomi-
when bacteria attains its logarithmic phase in pure culture (Heydarian neralization associated with extracellular polymeric substances (EPSs)
et al., 2018). This method was proposed for gold recovery from waste of E. coli was elucidated (Kang et al., 2017), the Au (III) reduction
PCBs using Chromobacterium violaceum (Li et al., 2015a). Regardless of process was mediated by the hemiacetal groups of the reducing sac-
the high Cu content (268.17 mg/g) and low Au content (0.050 mg/g), charides of EPSs via the identification of the relevant functional groups.
pretreatment of waste PCBs with Acidithiobacillus ferrooxidans can re- Such EPSs-mediated U (VI) reduction also exists in Shewanella sp.
move 80% of Cu and other base metals at optimum conditions. More- HRCR-1 (Cao et al., 2011).
over, pretreatment increased the Au content of waste PCBs by
0.114 mg/g, accompanied by a biorecovery rate of Au that was two 5.3. Novel biomineralization isolates and processes
times higher than that of the control group. In addition, oxygen sup-
plementation and the addition of nutritive salts (NaCl and MgSO4) Recently, novel microorganisms for the reduction of critical metals
8
Z. Yu, et al.
Table 4
Biomineralization of critical metals.
Critical Sources Microorganisms Concentration mg/ Recovery rate Estimated Costs Duration Mechanisms Potential applicability References
metals L % ($/L)
Au HAuCl4 Shewanella xiamenensis 300 36 0.64 24 h sodium lactate as electron donor Lab scale, the recovery of Au ions from (Wu and Ng, 2017)
BC01 industrial waste
Au HAuCl4 Shewanella oneidensis 300 19.6 0.64 24 h sodium lactate as electron donor Lab scale, the recovery of Au ions from (Wu and Ng, 2017)
MR-1 industrial waste
Au HAuCl4 Aspergillus foetidus 197 NA 0.5 4h certain protein molecules Lab scale. (Roy et al., 2016)
Au HAuCl4 Phomopsis sp. XP-8 100 68 0.4 6h Adsorb and reduce Au (III) to Lab scale, complex aqueous solutions, AuNPs (Xu et al., 2019)
immobilized AuNPs can degrade toxic dyes
Ag AgNO3 Pseudomonas aeruginosa NA NA 0.5 NA nitrate reductase mediated biomineralization and biotransformation (Ali et al., 2017)
mechanism processes and biogeochemical cycles for silver
and other heavy metals.
Pt PtCl4 Escherichia coli 1950 74 0.4 112 day Bacterial biomineralization biomineralize platinum (Shar et al., 2019)
Pt K2PtCl4 halophilic cultures 100 98 0.72 3–21 h Reduction to Pt (0) recovery of platinum from process and waste (Maes et al.,
streams 2016b)
Pt K2PtCl6 halophilic cultures 100 97 0.72 3–21 h Possible thinner peptidoglycan Lab scale (Maes et al.,
layer 2016b)
Pt industrial process halophilic microbial 80 99 0.72 24 h NA Lab scale, from process stream (Maes et al.,
streams community 2016a)
Pd Pd(II) Escherichia coli 100 100 0.64 0.5 h molybdoprotein-mediated Lab scale (Foulkes et al.,
9
mechanism, using formate as the 2016)
electron donor
Pt, Pd, platinum(IV), Shewanella algae 0.2 wt% PGMs > 95 NA 2h oxidation of organic acid salts such Lab scale, from spent automotive catalysts (Saitoh et al.,
palladium (II) and aslactate and formate 2017)
rhodium (III)
Pd Pd2+ Enterococcus faecalis 210 100 0.64 48 h sodium formate as electron donor Lab scale (Ha et al., 2016)
Pd spent catalyst Acidocella aromatica 100 100 0.5 95 h Monosaccharides or formate as Lab scale, leaching lixiviant (Okibe et al., 2017)
leachate PFBCT electron donor
Pd K2PdCl6 Phanerochaete 48 81.5 0.4 48 h Amide groups Lab scale, catalyze Heck reaction of styrene (Tarver et al.,
chrysosporium and iodobenzene 2019)
Eu Thermus scotoductus 76 100% 0.5 10 h Produce Eu2(CO3)3 Lab scale (Maleke et al.,
SA-01 2019)
Te sodium tellurite Phoma glomerata 10 98.5 2.6 30 d intracellular uptake or interaction Lab scale (Liang et al., 2019)
with surface biomolecules
Te tellurite anaerobic granular 10 98 110 42 d loosely-bound EPS of granular Lab scale, synthetic wastewater (Mal et al., 2017)
sludge sludge
Te tellurite Phanerochaete 10 39.8 1.2 8d NA Lab scale (Espinosa-Ortiz
chrysosporium et al., 2017)
Te tellurite Shinella sp. WSJ-2 63.8 96.4 0.64 44 h NA Lab scale, simulated lake water (Wu et al., 2019a)
Mo Na2MoO4 Clostridium 100 88 0.5 4–5 h NA Lab scale, degradation of MeO (Nordmeier et al.,
pasteurianum BC1 2018)
were isolated. The isolated Raoultella ornithinolytica and Raoultella 6.2. Future prospects
planticola strain MoI showed optimal molybdate reduction ability when
using glucose as the electron donor (Saeed et al., 2019). Moreover, The combination of two or three technologies might be more effi-
tellurite reduction was observed intracellularly and extracellularly in cient in terms of biorecovery. Combination of bioleaching with a bio-
the genus Raoultella and Escherichia isolated from wastewater (Nguyen sorbent strategy yielded a > 86% Cu recovery from waste PCBs using
et al., 2019). Tellurite-reducing photosynthetic bacterium, Rhodopseu- USCT-R010 isolates for bioleaching and the dead biomass of A. oryzae
domonas palustris strain TX618, exhibited a high recovery efficiency and Baker’s Yeast as biosorbents (Sinha et al., 2018). The hybrid of
with wide variations in pH, temperature, light intensity, and initial ammonium thiosulfate (AT) and Lactobacillus acidophilus (LA) achieved
tellurium concentration (Xie et al., 2018). In addition, the potential 85% gold recovery from waste PCBs, the π-π interaction between AT
functions of biorecovery of critical metals in previously isolated mi- and LA enhanced amide absorption bond and then lead to improvement
croorganisms were explored. A keratin-degrading Bacillus sp. strain of gold recovery (Sheel and Pant, 2018). MFC and bioleaching hybrid
(khayat) was able to reduce molybdate to molybdenum in optimal technologies also significantly improved the recovery rate of Cu, with
conditions (pH, 5.8–6.8; temperature, 25–34 °C) (Khayat et al., 2016). 54% leaching and 78% recovery of Cu from the secondary copper
Moreover, Shinella sp. WSJ-2 was also found in the reduction of Te (IV) tailings (Huang et al., 2019b). A similar concept was used for the re-
(Wu et al., 2019a). covery of Cu from copper sulfide minerals and enhanced Cu recovery,
Several novel biomineralization processes of critical metals have which was attributed to an MFC-mediated decrease in the pH value
been reported. The extracellular formation of Pd nanoparticles was derived from the anodic sulfide/sulfur oxidation process (Huang et al.,
observed after supplementation of Pd (II) (12–48 ppm) into the fer- 2019d). The successful biorecovery of Cu provides a potential for re-
mentation medium during the growth of Phanerochaete chrysosporium cycling of critical metals from wastes via a combination of these tech-
(Tarver et al., 2019). This extracellular biosynthesis of gold nano- nologies. Researchers investigated the integration of two stages, i.e.,
particles exists in A. foetidus-mediated biomineralization (Roy et al., bioleaching and electrochemical extraction, for the recovery of Nd and
2016). As reported, a UASB reactor was used to perform tellurium re- La from monazite rock ore (Maes et al., 2017). The results showed that
covery continuously from tellurite-containing wastewater (Mal et al., Nd was concentrated from 392 mg/L in the lixiviants to 880 mg/L after
2017). The exploration of the mechanisms of biomineralization of dif- the electrochemical extraction process through utilization of a CEM
ferent critical metals provides insight on improving the production of under the effect of an electric field. Thus, the combination of these
metal nanoparticles and preferable applications in industry. technologies might be a promising way to recover critical metals from
The application of biomineralization for biorecovery of critical wastes in the future. The exponential growth of emerging materials
metals offer an effective way to produce nanoparticles. The metal na- (e.g., nanomaterials) in a wide range of potential applications implies
noparticles showed good performance in application, such as Pd na- that various types of waste would become an additional secondary
noparticles in chromate reduction (Ha et al., 2016) and azo dyes bior- source of critical metals (Tan et al., 2017). The interactions between
eduction (Wang et al., 2018a), Au nanoparticles in degradation of toxic fungi and bacteria occurred in various environments (Deveau et al.,
dyes (Xu et al., 2019), etc. With exploration of novel biomineralization 2018), new metal-reducing bacteria could be isolated through the uti-
isolates and processes, more pathways of critical nanoparticles gen- lization of fungi (Furuno et al., 2012). Furthermore, the co-culture of
eration are elucidated. However, the detailed mechanisms are not clear. bacteria and fungi might be a potential way to deal with critical metals
Therefore, mechanisms for better performance of nanoparticle pro- for high recovery rate (Deveau et al., 2018), such as REEs (Hopfe et al.,
duction need be to be explored. 2017).
6. Challenges and future prospects 7. Conclusions
6.1. Gaps and challenges in knowledge The biorecovery of critical metals through biosorption, BESs, bio-
leaching, and biomineralization are potential approaches for waste
The application of biosorption, BESs, bioleaching, and biominer- management and metals’ recycling. The biosorption technique showed
alization into the recovery of critical metals provides a potential for the better efficiency and low-cost in recovery of metals from wastewaters as
recycling of these metals from different kinds of wastes. Although great compare to other treatments while bioleaching is appropriate for solid
improvements have been achieved using these strategies, gaps and wastes. The combination of these technologies has emerged as a pro-
challenges remain regarding their practical applications to the recovery mising application in biorecovery processes. Developments and mod-
of critical metals. The metal-binding protein exhibits high adsorption ifications of biological strategies will provide high-efficient way to re-
ability and selectivity. However, only few metal-binding proteins have cover metals selectively from wastes. A better understanding of the
been applied to biorecovery. Thus, more attention should be focus on mechanisms underlying these technologies will lead to the generation
the explorations and mechanisms of novel metal-binding proteins. The of more accurate technologies for the biorecovery of metals.
MFC and MEC exhibited high efficiencies for simultaneous recovery of
critical metals and removal of organic pollutants, which is suitable for
wastewater treatment. However, most of the applications of BESs on Declaration of Competing Interest
wastewater treatment are still in lab-scale. The functional microbial
communities in biorecovery processes of critical metals are not clear. In The authors declare that they have no known competing financial
addition, more studies are needed to explore the mechanisms under- interests or personal relationships that could have appeared to influ-
lying the exploitation of the electron transfer rate of BES. The me- ence the work reported in this paper.
chanisms of biomineralization should be explored further in future
studies. A better understanding of the mechanisms that link micro-
organisms to the reduction of critical metals would lead to the gen- Acknowledgments
eration of nanoparticles with high quality in short time. The possibility
of applying novel isolates to the biorecovery of critical metals needs to The work was supported by National Natural Science Foundation
be verified. grant (31870082); Gansu province major science and technology pro-
jects (No: 17ZD2WA017); Central Universities grant [grant number
lzujbky-2018-103].
10
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Bioresource Technology 297 (2020) 122416

Contents lists available at ScienceDirect

Recent advances in the recovery of metals from waste through biological T

(Esmaeili and Beni,

(Ogi et al., 2016)

developments and modiﬁcations of biosorbents overcoming these

2.2. Improvements on adsorption capacity and selectivity

Various biosorbents were developed recently to adsorb critical

metals (Table 1). For non-living biosorbents, the introduction of func-

metal sorption (Wang and Chen, 2009). So, improvements on the

60 ppm (Páez-Vélez et al., 2019). In some cases, NaOH- or hexadecyl-

trimethylammonium bromide (CTAB)-modiﬁed bark powder of Man-

solution (Devi and Mishra, 2019), with a resulting maximum adsorption

ment provides additional active binding sites (eCOOH and eOH) on

served for CTAB modiﬁcation. A heat-treated E. coli cell suspension (90-

which increased from 5 mV (un-treated) to 19–24 mV (heat-treated),

contributed to the improved biosorption performance. Further analysis

increase density of amino and carboxyl groups on the surface of E. coli

iﬁed cellulose nanoﬁbril from tunicate showed the highest Pt adsorp-

PEI modiﬁed cellulose nanocrystals obtained from hardwood pulp,

modiﬁed cellulose nano-ﬁbril from tunicate (Hong et al., 2019). Also,

novel magnetic biosorbent was generated by immobilizing persimmon

tannin (PT) onto Fe3O4@SiO2 microspheres (Fe3O4@SiO2@PT) showed

pation of phenolic hydroxyl group. The high selectivity of Fe3O4@

Cu (II) and Fe (III) coexist in solution. The reduction of Au (III) to

metallic gold by Fe3O4@SiO2@PT realizes the convenient and eﬃcient

In contrast, extracellular proteins play a crucial role in the bio-

sorption process of living-cell biosorbents. Similarly, an extracellular

protein from Tepidimonas fonticaldi sp. AT-A2, displayed an outstanding

treatment of industrial wastewater obtained from a manufacturing

based biosorbent also achieved a high adsorption capacity (1.45 mg

sequently, the overexpression of the CueR protein on the surface of

Saccharomyces cerevisiae cells signiﬁcantly enhanced the silver (Ag) (I)

binding capacity (Tao et al., 2016). The surface-engineered cells can

similar phage surface display technique also exhibited an aﬃnity for Te

(Huang et al., 2015a)

(Huang et al., 2019a)

(Wang et al., 2018b)

(Wang et al., 2015)

(Liu et al., 2019c)

(Kim et al., 2018)

(Ali et al., 2019)

(Tan et al., 2019). In this regard, the expression of speciﬁc metal-

It is worth mentioning that the surface display technology oﬀers

dical, Round Top Mountain, and Togo leachates), an enhancement of

0.5% REEs by mass of the total metals, respectively. Little to no ad-

protein (CsgA-LBT) for REE recovery via the secretion of functionalized

curli ﬁbers (Tay et al., 2018). This extracellular display of curli-LBT

at thetreat conditions that might compromise the viability of cell-based

Overall, pretreatment of biosorbents contributes to the availability

capacity, while ﬁlters generated using the surface display technology

sorption capacity, while the relatively low selectivity is its short-

comings. Expressing metal-binding protein in living cells could improve

the selectivity, while there are only a few metal-binding proteinsre-

industrial application would be the main challenges in future studies.

3. Recovery of critical metals through bioelectrochemical systems

3.1. Bioelectrochemical systems

The bioelectrochemical systems (BESs) usually contains MFC, MEC,

derived during microorganism metabolism can reduce some metal ions