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Research Article

Cite This: ACS Sustainable Chem. Eng. 2019, 7, 15311−15319 pubs.acs.org/journal/ascecg

Sustainable Bioleaching of Rare Earth Elements from Industrial

Waste Materials Using Agricultural Wastes
Hongyue Jin,†,$ David W. Reed,‡,$ Vicki S. Thompson,*,‡,$ Yoshiko Fujita,‡ Yongqin Jiao,§
Michael Crain-Zamora,‡ Jacob Fisher,‡ Katherine Scalzone,‡ Mike Griffel,∥ Damon Hartley,∥
and John W. Sutherland⊥
†
University of Arizona, Department of Systems & Industrial Engineering, 1127 E. James E. Rogers Way, Room 263A, Tucson,
Arizona 85721, United States
‡
Idaho National Laboratory, Department of Biological and Chemical Processing, P.O. Box 1625, Idaho Falls, Idaho 83415-2203,
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United States
§
Lawrence Livermore National Laboratory, Physical and Life Science Directorate, Biosciences and Biotechnology Division, 7000
East Ave, Livermore, California 94550, United States
∥
Idaho National Laboratory, Department of Bioenergy Technologies, P.O. Box 1625, Idaho Falls, Idaho 83415-2203, United States
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⊥
Purdue University, Environmental and Ecological Engineering, Potter Engineering Center, Room 364, 500 Central Drive, West
Lafayette, Indiana 47907-2022, United States
*
S Supporting Information

ABSTRACT: Agricultural waste was used as substrate for

fermentation by Gluconobacter oxydans to produce lixiviant for
rare earth element (REE) recovery from industrial waste
materials, i.e., spent fluid catalytic cracking (FCC) catalysts.
Biolixiviant generated from potato wastes performed comparably
to that generated from refined glucose (25.7% ±0.2 and 25.1%
±1.1 REE recovered, respectively). Corn stover yielded a slightly
less effective biolixiviant (23.3% ±0.3 REE recovered) but may
serve as a better industrial substrate since collection systems for
stover are already in development and have been implemented in
several locations. Techno-economic analysis indicated that the use
of agricultural waste carbon could lead to a more cost-effective
bioleaching process than refined glucose. Analyses suggested that
a corn stover-based bioleaching plant would have 22% lower total costs than a potato wastewater-based plant, and a potato
wastewater-based plant should have 17% lower total costs compared to a glucose-based plant. An environmental life cycle
analysis showed no clear winner among the three alternatives when ten impact categories were considered simultaneously.
However, a corn stover-based process generally showed less environmental impact than a potato wastewater-based process or a
refined glucose-based process. Our studies indicate that using agricultural wastes as substrates for biological production of
lixiviant provides a profitable means for recovering critical metals from recyclable waste materials.
KEYWORDS: Fluid catalytic cracking catalyst, Critical materials, Corn stover, Urban mining, Environmental life cycle analysis,
Techno-economic analysis, Gluconobacter oxydans, Potato wastewater

■ INTRODUCTION
Rare earth elements (REE) are a vital component in modern
electronics and green technology products such as computers,
smartphones, lighting, hybrid and electric vehicles, wind
turbines, and photovoltaic cells. They are also important in
glass polishing powders, optical glass, and petroleum refining
catalysts. REE are chemically similar metallic elements that
include the lanthanide series, as well as yttrium and scandium.
Although these elements are not really rare, it is challenging to
acquire them in usable quantities.1 Currently, China is
producing >70% of the global REE supply.2 To improve
environmental and safety conditions and to satisfy growing
domestic demand, China has recently clamped down on illegal
mining operations and tightened export quotas, which has the
potential to lead to supply risks as demand for these materials
continues to grow.3 Since metals are inherently recyclable,
recovery and reuse of these metals can reduce the negative
impact of disposal, save energy, and mitigate supply and
security risks.
Received: May 8, 2019
Revised: August 9, 2019
Published: August 20, 2019

© 2019 American Chemical Society 15311 DOI: 10.1021/acssuschemeng.9b02584

ACS Sustainable Chem. Eng. 2019, 7, 15311−15319
ACS Sustainable Chemistry & Engineering
One potentially environmentally and economically favorable
approach to recover REE is bioleaching. In bioleaching,
microbial activity results in metabolites that solubilize and
release metals from a solid matrix, which may be ore or
alternative sources. Such biohydrometallurgical practices are
established in the mining industries and offer lower costs and
improved environmental sustainability.4 These industrial
processes rely on microorganisms that oxidize sulfidic minerals
in the ore to produce acid for metal dissolution. In copper
bioleaching, microorganisms produce ferric iron and sulfuric
acid that promote solubilization of the metal. In gold recovery,
rather than direct dissolution of the target metal, micro-
organisms are utilized to dissolve the sulfidic mineral matrix
surrounding the gold, making it more accessible to chemical
leaching agents.5 However, as most REE ores and industrial
wastes do not contain reduced sulfur, an alternative
bioleaching approach utilizes heterotrophic microorganisms
grown on organic carbon compounds to produce organic acids.
These acids have been shown to successfully recover metals
such as REE from waste materials that do not contain
sulfur.6−9
In our previous work, we reported the leaching of REE from
end-of-life materials such as retorted phosphors and spent fluid
catalytic cracking (FCC) catalyst by several heterotrophic
microorganisms; from these we identified Gluconobacter
oxydans NRRL B5810 as a particularly promising strain.7 G.
oxydans is an industrially proven bacterium which oxidizes
carbohydrates to produce organic acids such as gluconic acid.11
Lixiviant (spent medium containing exudate) produced by G.
oxydans, containing predominantly gluconic acid when the
organism was grown with refined glucose, could recover about
half of the total REE content available in FCC catalyst.7 As
described previously, the biologically produced lixiviant was up
to 2-fold more effective at leaching than an abiotically prepared
solution containing a similar concentration of gluconic acid.7
Techno-economic analysis (TEA) and life cycle analysis
(LCA) for bioleaching of REE from spent FCC catalyst
indicated that a bioleaching plant based on G. oxydans lixiviant
production could be profitable and have a lower environmental
impact than a chemical leaching plant.12 The TEA also
revealed that the refined sugar used to feed the microorganisms
comprised 44% of the total cost of the plant and would
therefore be a good target for substitution in order to reduce
costs and increase profitability.
One potential option to lower substrate costs for G. oxydans
is to use agricultural and food waste products in place of the
sugar.13−15 Waste products such as corn stover, wheat straw,
sugar beet pulp, and potato wastes contain lignocellulose,
which consists of lignin, cellulose, and hemicellulose. When
hydrolyzed, the cellulose polysaccharides yield glucose while
hemicellulose generates a variety of sugar subunits but
primarily xylose. Corn stover has been successfully converted
to bioethanol and both corn stover and potato waste products
have been converted to gluconic acid by G. oxydans strains.15,16
Consequently, we evaluated the ability of G. oxydans B58 to
grow on these wastes and produce a lixiviant effective for
bioleaching. Along with laboratory experiments to quantify
organic acid production and REE recovery, we conducted TEA
and LCA to examine the impacts of exchanging refined glucose
for these wastes on the economic prospects of heterotrophic
bioleaching for REE recovery.
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■ MATERIALS AND METHODS
Gluconobacter Growth and Bioleaching. Preparation and
Analysis of Corn Stover and Potato Wastewater. Hot water
pretreated corn stover was kindly provided by Dr. Nate Mosier from
Purdue University and enzymatically hydrolyzed as described
elsewhere17 with the exception that the enzyme hydrolysis procedure
was in 20 mM sodium acetate buffer (pH 4.8) and Cellic enzymes
(Novozymes; Franklinton, NC) were loaded with Ctec2 at 40 mg and
Htec2 at 4 mg per gram dried corn stover (10% w/v).
Potato wastewater (Idaho Supreme Potatoes Inc., Firth, ID) was
dried at 50 °C for 2 days. A suspension of the dried material was
prepared (15% w/v) using nanopure water and adjusted to pH 7.0
using HCl. For enzyme hydrolysis, α-amylase (45 U; Sigma-Aldrich,
St. Louis, MO) was added and the solution (100 mL) was incubated
for 2 h at 80 °C and 200 rpm.18 The solution was then allowed to
cool, and following adjustment to pH 4.5 (using NaOH),
amyloglucosidase (9 U) was added and the mixture was incubated
for 24 h at 60 °C and 200 rpm. Finally, to remove solids, the solution
was centrifuged (7500g; 1 h) and filtered (0.22 μm pore size).
The sugar contents of the corn stover and potato waste
hydrolysates were determined using the National Renewable Energy
Laboratory (NREL) Laboratory Analytical Procedure for standard
biomass analysis.19 Released carbohydrates were measured with a
water mobile phase using a high performance liquid chromatography
(HPLC) instrument (Thermo Fisher Scientific, Ultimate 3000,
Waltham, MA, U.S.A.) equipped with an Aminex HPX-87P column
(Bio-Rad, 300 × 7.8 mm, Hercules, CA, U.S.A.) and a Refractive
Index (RI) detector (Thermo Fisher Scientific, Ultimate 3000,
Waltham, MA, U.S.A.). Standards for carbohydrate analysis included
cellobiose, glucose, xylose, galactose, arabinose, and fructose. At least
two parallel samples were used in all analytical determinations.
Biolixiviant Production from Corn Stover and Potato Waste-
water. A starter culture of G. oxydans was grown in Pikovskaya
phosphate modified (Pkm) medium containing 10 g/L refined
glucose.7 The cells were washed and used to inoculate fresh Pkm (3 ×
106 cells/mL) where the carbon source consisted of refined glucose or
treated corn stover or potato wastewater. The amount of corn stover
or potato hydrolysate added to the culture was based on the total
sugar content, with the goal of providing a sugar molar concentration
comparable to 40 g/L glucose. For these experiments, the final
concentration in the potato wastewater treatment was ∼43 g/L
glucose and those for corn stover were 32 g/L glucose with 8 g/L
xylose. Biolixiviant was produced at 30 °C by shaking the culture at
150 rpms in flasks for 42 h or with the Sixfors reactor system (Infors
HT, Laurel, MD) for 36 h.12 The spent medium containing the
biolixiviant was separated from the cells by centrifugation (6000g, 30
min) and filtration (0.22 μm pore size) prior to storage at 4 °C and
use for bioleaching.
Metal Leaching and Analysis. Spent FCC catalyst containing
approximately 1.5% REE (predominantly La, 13.6 mg/g and Ce, 0.7
mg/g) by mass7 was obtained from Valero (Houston, TX). The
catalyst was leached with the biolixiviant at 30 °C while shaking at
150 rpm for 24 h in 50 mL conical tubes at solid to liquid mass ratios
of 50%. Control bioleaching treatments were prepared to include
FCC catalyst incubated with sterile “fresh” media.
REE concentrations were measured using inductively coupled
plasma mass spectrometry (ICP-MS). The ICP-MS instrument
(Agilent 7900 with UHMI) was operated in accordance with
manufacturer recommendations. The filtered (0.22 μm) samples
and the commercial standard stock solutions were acidified with
ultrapure concentrated nitric acid to a concentration of 1% HNO3 (v/
v) prior to analysis.
Economic Analysis. Analysis Framework. A bioleaching plant
with an FCC catalyst processing rate of 19000 tons per year was
simulated and modified from our previous design12 which utilized
glucose as the carbon source. It was assumed that a corn stover-based
plant would be colocated in Joliet, IL next to a petroleum refinery
with corn stover sourced from rural Illinois, while a potato waste-
based plant would be colocated with petroleum refineries in Salt Lake
City, UT with potato waste sourced from southeastern Idaho. Figure
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S1 shows a process flow diagram for this system as well as material
and energy balances for the biolixiviant production portion of the
plant from Zhang16(Figure S2). The TEA was conducted using the
production and capital cost estimation procedure adapted from
Silla.20 The total cost consists of direct costs, fixed capital costs, and
other indirect and general costs, whereas the revenue is from REE
product sales and tipping fees received from oil refineries for the
disposal of spent FCC catalysts.
Direct Costs. Direct costs are by far the largest portion of costs for
the industrial bioleaching process and consisted of substrates,
electricity, utilities, agricultural waste collection, and other related
biolixiviant production and bioleaching expenses. In our previous
analysis, the costs for substrates totaled slightly less than half of the
overall REE recovery process cost, and glucose had the largest
economic impact (98% of nutrient cost).12 In this analysis, the cost of
refined glucose was eliminated, and instead, additional expenses were
incurred for pretreatment and enzymatic hydrolysis to generate
glucose and other monosaccharides from potato wastewater and corn
stover. The cost for gluconic acid production from corn stover by G.
oxydans reported previously by Zhang et al.,16 which includes the
costs of collection, pretreatment and enzymatic hydrolysis, liquid/
solid separation, fermentation, and product recovery of the gluconic
acid, was incorporated into the model. To treat potato wastewater to
obtain similar concentrations of glucose as the other carbon sources,
α-amylase and amyloglucosidase were required. These enzymes were
available for as little as $1−4/kg at the volumes needed for a full-scale
bioleaching plant (Alibaba.com, July 2, 2018). However, to obtain a
conservative estimate, the maximum prices found online (Hangzhong
Yanghong Bioengineering Co., Ltd.; early 2019) for α-amylase and
amyloglucosidase, $10/kg and $50/kg, respectively, were used in the
TEA. Since particulates remained after the enzymatic treatment of the
potato wastewater and would likely interfere with the bioleaching
process, a liquid/solid separation of vacuum filtration was added
based upon the 2015 NREL design report.21 Potato wastewater was
assumed to be available at no cost except for the transportation. This
is a conservative assumption since potato processers currently have to
pay for wastewater treatment of potato waste which is then applied to
local fields as irrigation water. However, in Idaho, the Department of
Environmental Quality limits the yearly application of this waste-
water22 which limits the amount of potatoes that can be processed
yearly. If another use for their waste stream was available, the potato
processers would avoid the wastewater treatment costs and would
have additional revenue, making this an attractive option. The
transportation cost of potato wastewater was estimated to be $0.14/
ton per mile23, and it was assumed that potato waste would be
sourced from Idaho potato processing plants such as Idaho Supreme
Potatoes (Firth, ID) and transported to oil refineries in Salt Lake City,
UT which would be the source of FCC catalysts.
Electrical costs were based on the rate of electricity usage for
equipment specific to the biolixiviant production and bioleaching of
REE.12,16,21 One key difference between the two feedstocks, corn
stover and potato wastewater, is that the combustion of lignin residue
from corn stover generated sufficient heat and electricity for gluconic
acid production. In addition, 251 kWh of excess electricity was
generated as a byproduct per ton of acid.16 Therefore, the net
electricity cost of corn stover-based bioleaching was negative, while
that of potato wastewater-based bioleaching was substantial
(approximately $520,000/year). The basis for operation costs
assumed a standard 8000 h in a working year, a reasonable
approximation of the number of working hours in a year, considering
holidays, system maintenance, and repair. The utilities included water
and steam used in the various processes, and other costs such as the
operating labor, operating supplies, maintenance, and quality control
of the plant were also considered.
Fixed Capital Expenses. Specific capital equipment for the
bioleaching plant included a bioreactor, compressor, sterilization
equipment, vacuum belt filter, and heat exchangers to heat and cool
the reactor feed. Heap leaching costs included piping, pumps, and
pads,24 which have been adjusted for inflation and working volume.
Additional capital costs consisted of the feasibility study, land use,
15313
Research Article
construction and installation costs for the bioleaching site, including
instrumentation and control, electrical materials, and service facilities
and improvements. Sixty percent of the capital cost was assumed to be
financed with a cost of capital at 8%.
Other Indirect and General Costs. Property taxes, insurance costs,
fringe benefits, and overhead, although not directly part of the
bioleaching process, were considered as inevitable costs of running a
business. Administration, marketing, financing, research and develop-
ment comprised the general expenses. Additional assumptions are
available in Supporting Information Table S1.
Revenue. One revenue for the bioleaching TEA was provided by
the REE that were leached and sold (Supporting Information Table
S2). As the recovered REE are mixed in aqueous solution, additional
concentration and separation processes are required to obtain pure
individual REO. Therefore, a discount rate of 60% was applied to the
prices of 99%+ pure individual REOs to estimate the revenue from
bioleached REE.12,25 In addition, a significant source of revenue was
the $200 per ton tipping fee (avoided cost for disposing the spent
FCC catalyst as hazardous waste). The bioleaching plant was assumed
to render the catalyst waste nonhazardous through the bioleaching
process, adding $200 to the revenue.12
Life Cycle Analysis (LCA). The goals of the LCA were to (1)
quantify the environmental impacts associated with bioleaching using
corn stover and potato waste based processes compared to refined
glucose and (2) identify the environmental hotspots that contributed
most to the environmental footprint. The LCA system boundary
started with media preparation, followed by biolixiviant production,
and subsequent leaching for REE recovery (Figure S3). The
functional unit was set at bioleaching 1 ton of spent FCC catalyst
with gluconic acid derived from 80 kg of refined glucose. As our
experimental data showed that metal recovery efficiencies varied
slightly by the process type, the functions delivered by bioleaching 1
ton of FCC catalyst were different. To compare the alternative
processes with the same basis, we adjusted the impacts of corn stover-
and potato wastewater-based bioleaching to achieve the same
economic value as the defined functional unit.
The unit processes used to model the environmental inputs and
outputs are summarized in Table 1 (for corn stover), Table 2 (for
potato waste), and Supporting Information Table S3 (for refined
glucose). Relevant data were collected from lab experiments, Zhang et
al.,16 Davis et al.,21 GREET,26 and Thompson et al.12 Although the
transportation distance was assumed to be the same (200 miles) for
both types of agricultural wastes, more potato wastewater was
required than corn stover to process one ton of spent FCC catalysts
(i.e., 450 tkm vs 68 tkm; tkm = ton*km), which increased the
transportation impact of potato wastewater-based bioleaching. With
this information, TRACI (Tool for Reduction and Assessment of
Chemicals and Other Environmental Impacts), developed by the U.S.
Environmental Protection Agency,27 was used to classify and
characterize the environmental impacts.
■
RESULTS AND DISCUSSION
Comparison of Carbon Sources for G. oxydans
Cultivation and Lixiviant Production. Following enzymatic
hydrolysis, approximately 440 mg of glucose was obtained per
gram of dried corn stover, representing roughly 70 percent of
the available glucose.28 With corn stover, xylose is also an
important hydrolysis product; under the tested conditions, the
xylose yield was 130 mg/g. The potato wastewater hydrolysate
contained 430 mg of glucose per gram of dried material.
The highest REE recovery from FCC catalyst had been
obtained using lixiviant from G. oxydans grown on refined
glucose at about 40 g/L in Pkm media.12 To compare the
biolixiviant derived from agricultural wastes to the biolixiviant
derived from glucose, the hydrolysates were amended into the
growth medium at similar concentrations. For the potato
wastewater hydrolysate, since the carbohydrate composition
consisted almost entirely of glucose, this was straightforward.
DOI: 10.1021/acssuschemeng.9b02584
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Table 1. Life Cycle Inventory Data for Leaching One Ton of Table 2. Life Cycle Inventory Data for Leaching One Ton of
Spent FCC Catalysts Using Biolixiviant from Corn Stovera Spent FCC Catalysts Using Biolixiviant from Potato
Wastewater
Unit Process Value Unit
Inputs to Product System Unit Process Value Unit
Corn stover, at field/kg/US 163 kg Inputs to product system
Sulfuric acid {GLO}| market for | APOS, U 3.47 kg Alpha amylase 60 g
Steam, in chemical industry {RoW}| production | 27.89 kg Amyloglucosidase 0.92 g
APOS, U Ammonium sulfate, as N {GLO}| market for | 1 kg
Lime {GLO}| market for | APOS, U 2.66 kg APOS, U
Oxygen, liquid {RoW}| market for | APOS, U 2.59 kg Magnesium sulfate {GLO}| market for | APOS, U 0.2 kg
Protein pea {GLO}| market for | APOS, U 1.35 kg Manganese sulfate {GLO}| market for | APOS, U 0.0002 kg
Phosphate fertilizer, as P2O5 {RER}| diammonium 0.10 kg Iron sulfate {GLO}| market for | APOS, U 0.0002 kg
phosphate production | APOS, U Potassium chloride, as K2O {GLO}| market for | 0.4 kg
Corn steep liquor/kg/RNA 0.23 kg APOS, U
Sodium hydroxide, without water, in 50% solution 13.53 kg Yeast paste, from whey, at fermentation/US* US- 1 kg
state {GLO}| market for | APOS, U EI U
Compressed air, 800 kPa gauge {GLO}| market for 37.41 m3 Calcium chloride {GLO}| market for | APOS, U 0.14 kg
| APOS, U Compiled | Potassium phosphate {GLO}| market 0.74 kg
Activated carbon, granular {RoW}| activated 1.85 kg for | APOS, U
carbon production, granular from hard coal | Water, completely softened, from decarbonised 6.50 ton
APOS, U water, at user {RoW}| production | APOS, U
Water, completely softened, from decarbonized 3.63 ton Electricity, medium voltage {US}| market group for 393 kWh
water, at user {RoW}| production | APOS, U | APOS, U
Electricity, biomass, at power plant NREL/US 141.54 kWh Steam, in chemical industry {GLO}| market for | 148.77 kg
Transport, freight, lorry, unspecified {GLO}| 68.28 tkm APOS, U
market group for transport, freight, lorry, Transport, freight, lorry, unspecified {GLO}| 450.7 tkm
unspecified | APOS, U market group for transport, freight, lorry,
Avoided Products unspecified | APOS, U
Electricity, medium voltage {US}| market group for 17.60 kWh Outputs
| APOS, U Yttrium oxide 4.67 × 10−03 kg
Emissions to Air Europium oxide 1.22 × 10−04 kg
Carbon dioxide 4.47 kg Terbium oxide 7.91 × 10−05 kg
Oxygen 9.98 kg Lanthanum oxide 3.54 kg
Nitrogen 33.15 kg Cerium oxide 1.16 × 10−01 kg
Water 0.57 kg Praseodymium oxide 2.89 × 10−03 kg
Emissions to Water Neodymium oxide 7.16 × 10−03 kg
Glucose 9.92 kg Dysprosium oxide 3.77 × 10−04 kg
Calcium compounds, unspecified 4.79 kg Vanadium 7.59 × 10−02 kg
Water 31.20 kg
Wastewater 453.5 kg
the expectation that it would convert glucose to gluconic acid
Emissions to Soil
and convert xylose to xylonic acid.29
Lignosulfonic acid, sodium salt 21.74 kg
G. oxydans was able to grow on each of the carbon sources.
Outputs
After growth, the lowest average pH (2.2) was generated in the
Yttrium oxide 4.48 × 10−03 kg
medium amended with glucose. The average pH values of the
Europium oxide 1.13 × 10−04 kg
spent media from the cultures grown in potato wastewater and
Terbium oxide 7.32 × 10−05 kg
corn stover were 2.4 and 2.6, respectively (Figure 1). Although
Lanthanum oxide 3.22 kg
they are not the focus of this paper, other agricultural waste
Cerium oxide 1.06 × 10−01 kg
materials were also tested and had pH up to 3.1 (Table S4).
Praseodymium oxide 2.67 × 10−03 kg
Bioleaching with Lixiviant from Agriculture Waste.
Neodymium oxide 6.67 × 10−03 kg
REE and metal recovery with media controls were marginal
Dysprosium oxide 3.70 × 10−04 kg
(data not shown). Our previous work with biolixiviants
Vanadium 6.96 × 10−02 kg
a
generated from refined glucose indicated that the concen-
The environmental input and output values for gluconic acid tration of gluconic acid was an important factor for metal
production were derived from Zhang et al.,16 whereas those for leaching, but perhaps the pH was a better predictor of leaching
bioleaching were from Thompson et al.12 and additional experiments
efficiency.7 In this study, the leaching results suggested that the
conducted in this study. Ecoinvent 3.4 and UCLCI databases were
used to model the relevant unit processes. “GLO” represents global, potato wastewater biolixiviant was similarly efficient to refined
“RoW” represents rest of the world, and “US” represents the United glucose (25.7% and 25.1%, respectively). Each had similar
States. gluconic acid concentrations, although the pH differed by 0.2
units (Figure 1). They both out-performed the corn stover
biolixiviant in leaching REE from the spent FCC catalyst; the
In the case of the corn stover hydrolysate, glucose and xylose corn stover had a much lower gluconic acid (104 mM) and
were present at about a 4:1 ratio in terms of mass. Therefore, higher pH (2.6). A similar trend was observed for REE
the total sugar derived from corn stover that was added to the leaching efficiencies using refined glucose, corn stover, and
growth medium consisted of approximately 32 g of glucose/L potato wastewater derived biolixiviants when leached at a solid
and 8 g of xylose/L. This was provided to the G. oxydans with to liquid mass ratio of 1.5% (Figure S4). Leaching efficiency
15314 DOI: 10.1021/acssuschemeng.9b02584
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Figure 1. REE leached from FCC catalyst at 24 h using lixiviant produced by G. oxydans grown on refined glucose, corn stover, or potato
wastewater. Results from leaching 5 g of FCC catalyst with 10 g of biolixiviant. Primary Y-axis, bars, percent of Ce and La leached from total
available in solid FCC catalyst. La and Ce were selected, as they are the major REE present in spent FCC catalyst. Secondary Y-axis, circles, average
pH of biolixiviant prior to leaching. Error bars indicate standard deviations for 3−9 replicates.

Figure 2. Total cost, revenue, and net profit for the bioleaching process using refined glucose versus potato waste or corn stover. All values are from
income statement, considering time value of money, interest payments, depreciation, and taxes. Two major differences between corn stover and
potato waste based bioleaching are collection cost and energy cost. Corn stover has a lower collection cost than potato wastewater, and it also has a
lower electricity cost due to the offset from electricity generation from the burning of lignin residues.

with other agricultural wastes also showed this trend with
lower efficiencies observed at higher pH (Table S4). Overall,
the data suggest that the alternative carbon sources could
effectively replace refined glucose as a substrate to support G.
oxydans for the production of lixiviant.
Techno-Economic and Life Cycle Analyses. The costs
for using agricultural wastes (i.e., corn stover and potato
wastewater) as a microbial substrate were much lower than the
costs for using refined glucose (Figure 2). Utilizing these waste
resources did however incur new costs: feedstock pretreatment
and the addition of enzymes. Many of the expenses related to
the remaining industrial processing steps remained unchanged
since the microbial growth and bioleaching would be
performed in the same manner, regardless of which carbon
source was used. For corn stover, a TEA was reported on the
conversion of corn stover to sugars via acid pretreatment and
enzymatic hydrolysis and subsequent fermentation to gluconic
and xylonic acid by G. oxydans.16 Consequently, the
production cost of gluconic acid from a biorefinery ($0.404/
kg for glucono-xylonic acid16) was utilized and updated to
reflect the capacity, electricity rate, and business costs of our
theoretical plant. It should be noted that the Zhang TEA
15315
utilized a different pretreatment (dilute acid) compared to the
hot water pretreated corn stover used to generate the
experimental data for this study. Our experience has shown
that biolixiviant leaching performance is best predicted by the
amount of sugar utilized in the fermentation.12 While the
Zhang pretreatment produced higher yields of glucose and
xylose compared to our hot water pretreated corn stover, our
TEA assumed that we would dilute those sugars to the same
levels that were utilized in this study. Therefore, the impact to
the TEA results presented here is minimal.
The potato wastewater did not need pretreatment, and for
determining glucose yield and leaching efficiency, it was dried
and the starch was enzymatically hydrolyzed with α-amylase
and amyloglucosidase to produce glucose. In this laboratory
study, the hydrolysis step was completed at elevated temper-
atures. In industrial use, however, the solids would not be dried
prior to use but would be mixed directly with growth medium,
and the enzymatic hydrolysis could be coordinated simulta-
neously with microbial culturing and without pH adjustments,
temperature control, or centrifugation steps. A key difference
between corn stover and potato wastewater is the collection
mass: to process 1 ton of FCC catalyst, 163 kg of corn stover is
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Figure 3. Sensitivity analysis on the effect of changing gluconic acid cost on the net present value of corn stover-based bioleaching.

Figure 4. Sensitivity analysis on the effect of changing tipping fee on the net present value of the bioleaching projects.

Table 3. Life Cycle Impacts for Leaching One Ton of Spent FCC Catalysts Using Biolixiviant Produced from Corn Stovera
Impact category Unit Total NaOH Activated carbon Electricity Electricity credit Compressed air
Ozone depletion kg CFC-11 eq 1.3 × 10−05 78% 2% 0% −7% 2%
Global warming kg CO2 eq 5.8 × 1001 28% 28% 11% −20% 9%
Smog kg O3 eq 3.7 × 1001 2% 2% 91% −1% 1%
Acidification kg SO2 eq 3.9 × 10−01 20% 26% 30% −8% 6%
Eutrophication kg N eq 9.8 × 10−02 64% 54% 6% −96% 23%
Carcinogenics CTUh 1.5 × 10−06 55% 50% 14% −65% 20%
Non carcinogenics CTUh 8.7 × 10−06 52% 29% 0% −37% 11%
Respiratory effects kg PM2.5 eq 2.4 × 10−02 97% 56% 4% −148% 32%
Ecotoxicity CTUe 1.6 × 1002 45% 39% 0% −56% 16%
Fossil fuel depletion MJ surplus 5.0 × 1001 24% 12% 0% −16% 7%
a
The third column, “Total”, shows the environmental impacts of the entire bioleaching process, whereas the columns 4-8 indicate the percentages
of impacts from each major environmental input or output. For example, sodium hydroxide contributes to 28% of the total global warming effect of
bioleaching. The impacts of energy generated from combustion of lignin residue were shown in the “Electricity” column. The bonus electricity that
would be sent to the electricity grid was modeled as avoided burden (as shown in Table 1), which represents the “electricity credit”.

required, while 1408 kg of potato wastewater is required.
Therefore, the collection cost reduces substantially for corn
stover (by approximately $730,000/year). More detailed cost
comparison is available in Supporting Information Table S5.
The revenue for the bioleaching process came from two
main sources: the elimination of the $200/ton tipping fee for
disposal of hazardous spent FCC catalyst and the sales of REE
and other metals obtained from the FCC catalyst bioleaching.
The experimental data presented in the preceding section
showed that the biolixiviants produced using agriculture waste
were almost as effective in leaching REE as biolixiviant
produced from refined glucose (Figure 1). Consequently, the
revenue from REE recovery was not reduced substantially by
the use of corn stover or potato wastewater as microbial
growth substrates (Figure 2). Following adjustments for the
15316
different REE recovery and process expenses, the net profits
were increased by nearly 4 times for the corn stover-based
plant and 2 times for the potato wastewater-based plant,
compared to the net profit from a glucose-based bioleaching
plant.
For sensitivity analysis, two main factors that significantly
affected the profitability were investigated: the cost of gluconic
acid production from corn stover (Figure 3) and the tipping
fee (Figure 4). When using refined glucose, the high cost (44%
of total costs) meant that any fluctuation in glucose price could
result in significant changes in profit (or loss). Sensitivity
analysis showed that gluconic acid production costs from corn
stover would increase more than 3-fold to $1.5/kg before net
present value would become negative (Figure 3). Similarly, as
the tipping fee constitutes 97−98% of the total revenue,
DOI: 10.1021/acssuschemeng.9b02584
ACS Sustainable Chem. Eng. 2019, 7, 15311−15319
ACS Sustainable Chemistry & Engineering Research Article

Table 4. Life Cycle Impacts for Leaching One Ton of Spent FCC Catalysts Using Biolixiviant Produced from Potato
Wastewatera
Impact category Unit Total Electricity Transportation Steam Others
Ozone depletion kg CFC-11 eq 3.88 × 10−05 54% 30% 14% 1%
Global warming kg CO2 eq 3.55 × 1002 72% 13% 13% 1%
Smog kg O3 eq 1.41 × 1001 44% 45% 9% 2%
Acidification kg SO2 eq 1.12 × 1000 64% 20% 13% 3%
Eutrophication kg N eq 2.18 × 1000 96% 1% 2% 1%
Carcinogenics CTUh 2.24 × 10−05 94% 0% 3% 3%
Non carcinogenics CTUh 8.40 × 10−05 85% 9% 5% 1%
Respiratory effects kg PM2.5 eq 8.29 × 10−01 95% 3% 2% 1%
Ecotoxicity CTUe 2.22 × 1003 89% 7% 3% 2%
Fossil fuel depletion MJ surplus 3.73 × 1002 49% 28% 21% 2%
a
The third column, “Total”, shows the environmental impacts of the entire bioleaching process, whereas the columns 4-6 indicate the percentages
of impacts from each major environmental input or output. For example, electricity contributes to 72% of the total global warming effect of
bioleaching.

Table 5. Life Cycle Impact Comparison for Bioleaching from Corn Stover, Potato Wastewater, and Refined Glucosea
Impact category Unit (A) Corn stover (B) Potato wastewater (C) Refined glucose (A)/(C) (B)/(C)
−05 −05 −05
Ozone depletion kg CFC-11 eq 1.29 × 10 3.87 × 10 2.70 × 10 48% 143%
Global warming kg CO2 eq 5.78 × 1001 3.54 × 1002 2.79 × 1002 21% 127%
Smog kg O3 eq 3.69 × 1001 1.41 × 1001 1.03 × 1001 357% 137%
Acidification kg SO2 eq 3.88 × 10−01 1.12 × 1000 1.20 × 1000 32% 93%
Eutrophication kg N eq 9.65 × 10−02 2.18 × 1000 2.41 × 1000 4% 90%
Carcinogenics CTUh 1.44 × 10−06 2.24 × 10−05 1.80 × 10−05 8% 124%
Non carcinogenics CTUh 8.65 × 10−06 8.39 × 10−05 1.55 × 10−04 6% 54%
Respiratory effects kg PM2.5 eq 2.35 × 10−02 8.28 × 10−01 5.63 × 10−01 4% 147%
Ecotoxicity CTUe 1.56 × 1002 2.22 × 1003 1.67 × 1003 9% 133%
Fossil fuel depletion MJ surplus 4.92 × 1001 3.72 × 1002 2.67 × 1002 18% 140%
a
The functional unit was defined as bioleaching 1 ton of spent FCC catalysts with gluconic acid derived from 80 kg of refined glucose. As
biolixiviants from agricultural wastes have different REE recovery rates, the impacts of corn stover- and potato wastewater-based bioleaching were
adjusted to recover the same value as the defined functional unit.

changes in tipping fee have significant effects on the resulting
net present value of the project. The potato waste-based
bioleaching would not be worthy of investment if the tipping
fee was reduced to $140/ton of spent FCC catalyst, whereas
the corn stover-based bioleaching would still be favorable even
if the tipping fee was reduced to $110/ton (Figure 4).
Life Cycle Analysis. The major contributors to the
environmental impacts for bioleaching one ton of spent FCC
catalysts were identified by LCA (Tables 3 and 4 for corn
stover- and potato wastewater-based bioleaching; Supporting
Information Table S6 for refined glucose-based bioleaching).
For leaching using biolixiviant derived from corn stover, the
environmental hotspots were sodium hydroxide, activated
carbon, electricity, and compressed air. Notably, sodium
hydroxide contributed 97% of the respiratory effects
(measured by kg PM2.5 equiv), electricity from combustion
of lignin residue contributed 91% of the smog effect (measured
by kg O3 eq.), and the credits from selling net electricity
generated by combustion of lignin residue reduced 60% of the
respiratory effect (i.e., respiratory effects before and after
electricity credit were 0.059 and 0.024 kg of PM2.5 equiv)
(Refer to Table 3 and Figure S2). For leaching using
biolixiviant derived from potato wastewater, the environmental
hotspots were electricity, transportation, and steam for
bioreactor operation. Electricity generated the highest impacts
for nine out of ten impact categories (excluding smog),
whereas transportation had the highest impact on smog
generation. Adoption of renewable energy could play an
15317
important role in reducing the environmental impacts of this
bioleaching process.
Overall, the environmental footprint of leaching using
biolixiviant derived from corn stover was lower than that of
bioleaching based on potato wastewater or refined glucose as
shown in Table 5. The only impact category that was an
exception was smog, where corn stover-based bioleaching was
higher than that of the two alternatives, largely due to the
energy generation from the combustion of lignin residue.
Therefore, to lower the smog effect, focus should be placed on
reducing the direct emissions from biomass combustion.
■ CONCLUSIONS
The demand for materials necessary to produce high
technology products is likely to increase in the foreseeable
future, making more critical than ever the need to develop
economically and environmentally viable means to recycle and
refine them. On the basis of the research documented in this
and previous papers,7,12 bioleaching to recover REE represents
a promising solution. While a standard heterotrophic
bioleaching process can be successful, the use of agricultural
waste products as alternative substrates for microbial
metabolism was shown to be more profitable and environ-
mentally friendly for several impact categories, with leaching
efficiency remaining largely unchanged but the processing costs
and impacts being greatly reduced. Corn stover, in particular, is
produced in high volumes, and the infrastructure for material
collection and transport toward the production of biofuels and
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ACS Sustainable Chem. Eng. 2019, 7, 15311−15319
ACS Sustainable Chemistry & Engineering
biochemicals already exists.30,31 Our analyses indicate that a
bioleaching plant using agricultural or food wastes is an
economically and environmentally viable option for future REE
recovery efforts.
■ ASSOCIATED CONTENT
*
S Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acssusche-
meng.9b02584.
Tables documenting additional assumptions for TEA,
prices for REE metals, life cycle inventory for refined
glucose, additional leaching and pH data for agricultural
residues, cost breakdown comparison between corn
stover and potato wastewater plants, life cycle impacts
for refined glucose and figures providing information on
process flow diagram, material, and energy balances for a
plant producing gluconic and xylonic acids from corn
stover, life cycle system boundaries and additional
leaching and pH data (PDF)
■
AUTHOR INFORMATION
Corresponding Author
*E-mail: Vicki.Thompson@inl.gov.
ORCID
Hongyue Jin: 0000-0002-9531-340X
David W. Reed: 0000-0003-4877-776X
Vicki S. Thompson: 0000-0003-4975-392X
Yoshiko Fujita: 0000-0002-4472-4102
Yongqin Jiao: 0000-0002-6798-5823
John W. Sutherland: 0000-0002-2118-0907
Author Contributions
$
These authors contributed equally (Hongyue Jin, David W.
Reed, Vicki S. Thompson)
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
We thank J. Hude (Valero) for the spent FCC catalyst, Nathan
Mosier (Purdue University) for the pretreated corn stover, and
Ron Kulow (Idaho Supreme Potatoes, Inc.) for the potato
wastewater. We thank the Agricultural Research Service, US
Department of Agriculture (Peoria, IL) for the G. oxydans
strain. We thank Idaho National Laboratory scientists D.
Daubaras and K. Schaller for assistance with HPLC, and D.
Lacroix and J. Taylor (University of Idaho; Center for
Advanced Energy Studies) for ICP analysis. We also
acknowledge the Department of Energy’s Science Under-
graduate Laboratory Internship program for providing funding
to Michael Crain-Zamora, Jacob Fisher, and Katherine
Scalzone. Finally, we thank David Combs, Idaho National
Laboratory, for production of the TOC graphic. This research
was supported by the Critical Materials Institute, a Department
of Energy Innovation Hub led by the U.S. Department of
Energy’s Ames Laboratory and supported by DOE’s Office of
Energy Efficiency and Renewable Energy’s Advanced Manu-
facturing Office, which supports early stage research to advance
innovation in U.S. manufacturing and promote American
economic growth and energy security. CMI seeks ways to
reduce supply risks on rare-earth metals and other materials
critical to the success of clean energy technologies. Work is
15318
Research Article
conducted under DOE Idaho Operations Office Contract DE-
AC07-05ID14517 and Lawrence Livermore National Labo-
ratory Contract DE-AC52-07NA27344. Accordingly, the U.S.
Government retains a nonexclusive, royalty-free license to
publish or reproduce the published form of this contribution
and allow others to do so for U.S. Government purposes.
■
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