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org/est Article

Transformation and Mobility of Cu, Zn, and Cr in Sewage Sludge

during Anaerobic Digestion with Pre- or Interstage Hydrothermal
Treatment
Qian Wang, Chiqian Zhang, Haesung Jung, Pan Liu, Dhara Patel, Spyros G. Pavlostathis,
and Yuanzhi Tang*
Cite This: Environ. Sci. Technol. 2021, 55, 1615−1625 Read Online
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sı Supporting Information

ABSTRACT: Anaerobic digestion (AD) combined with hydrothermal treatment (HT) is

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an attractive technology for sewage sludge treatment and resource recovery. The fate and
distribution of heavy metals in the sludge during combined HT/AD significantly affect the
sludge final disposal/utilization options, yet such information is still lacking. This study
systematically characterizes the transformation of important heavy metals Cu, Zn, and Cr
in sewage sludge during AD with pre- or interstage HT (i.e., HT-AD or AD-HT-AD,
respectively). Complementary sequential chemical extraction and X-ray absorption
spectroscopy were used to characterize the speciation and mobility of metals. For the
HT-AD system, both Cu and Zn predominantly occur as sulfides in HT hydrochars.
Subsequent AD favors the formation of Cu2S and partial transformation of nano-ZnS to
adsorbed and organo-complexed Zn species. HT favors the formation of Cr-bearing
silicates in hydrochars, whereas Fe(III)-Cr(III)-hydroxide and Cr(III)-humic complex are
the predominant Cr species in AD solids. Similar reaction pathways occur in the AD-HT-AD system with some minor differences in
metal species and contents, as the first-stage AD changed the sludge matrix. These findings have important implications for
understanding the fate and mobility of heavy metals in sludge-derived hydrochars and AD solids.

1. INTRODUCTION explored HT as an interstage process (i.e., sequential AD-HT-

Activated sludge process is commonly used for treating AD) to enhance the biodegradation of recalcitrant particulate
municipal wastewater at water resource recovery facilities organic matter and maximize biogas production and energy
(WRRFs). WRRFs in the US produce millions of tons of recovery.10,11
sewage sludge as a byproduct annually,1 among which ∼55% is Overall, the above discussed combined HT and AD
land applied and the remaining is disposed by landfill or processes (including HT-AD and AD-HT-AD, hereinafter
incineration.2 Sewage sludge contains a wide range of collectively referred to as combined HT/AD) can facilitate
contaminants, such as heavy metals, pesticides, herbicides, sludge dewatering, reduce sludge volume, and improve sludge
and pathogens,3,4 posing significant environmental and public quality as a soil amendment.12,13 Considering the important
health risks during land application or disposal. Thus, proper roles of heavy metals in regulations for sludge utilization and
treatment before its final utilization or disposal is needed. On disposal, as well as the significant correlation between metal
the other hand, sewage sludge contains high contents of speciation, mobility, and bioavailability, an in-depth under-
organic matter, which can be converted to biomethane standing of metal speciation evolution during combined HT/
(renewable bioenergy) via anaerobic digestion (AD), making AD is highly desired. Two common methods for investigating
it a good candidate for the energy recovery.1,5 AD consists of the fate of metals in solid samples are sequential chemical
four key steps: hydrolysis, acidogenesis, acetogenesis, and extraction (SCE) and X-ray absorption spectroscopy (XAS).
methanogenesis.6 Hydrolysis, the conversion of particulate SCE is an empirical chemical method for indirect identification
polymeric materials to bioavailable substrates for subsequent of metal species. For the three-stage Community Bureau of
acidogenesis and acetogenesis, is the rate-controlling step of
AD of particulate organic waste.7 Hydrothermal treatment
(HT) as a prestage process for AD (i.e., sequential HT-AD) is Received: August 3, 2020
effective in accelerating hydrolysis, increasing organic matter Revised: January 1, 2021
biodegradability, and promoting biogas (biomethane and Accepted: January 4, 2021
CO2) production during AD.8 Moreover, the preheated Published: January 19, 2021
feedstock stream reduces the energy input for maintaining
the subsequent AD at 35 °C.9 Recent studies have also

© 2021 American Chemical Society https://dx.doi.org/10.1021/acs.est.0c05164

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Reference (BCR) procedure14 used in this study, metal species were stored in the dark at 4 °C before use. A portion of raw
are categorized to four fractions: water-/acid-soluble and sludge was separated by centrifugation and freeze-dried for
exchangeable (i.e., carbonates), reducible (i.e., bound to Fe chemical composition and structure analyses as detailed below.
and Mn oxyhydroxides), oxidizable (i.e., bound to organic 2.2. Combined HT/AD of Sewage Sludge. Combined
matter and sulfides), and residual fractions.14,15 The metals in HT/AD of raw sludge was conducted in the sequences of HT-
the acid-soluble fraction are considered to be the most mobile AD or AD-HT-AD. The treatment conditions and sample
and readily bioavailable, whereas metals in the other fractions labels are summarized in Table 1 and discussed below.
are considered to be relatively stable and less mobile.16 XAS is
an in situ and nondestructive method for obtaining direct Table 1. Hydrothermal Treatment (HT) and Anaerobic
molecular level structure information on metal speciation (e.g., Digestion (AD) Conditions and Sample Labels
oxidation state, coordination structure, and mineral phase) in
heterogeneous matrices such as environmental samples.15,17 sample
system treatment reaction conditions and pHa label
Previous studies characterizing the contents and speciation
of heavy metals in sewage sludge mainly focused on AD or HT raw pH 6.34 raw sludge
sludge
alone. The speciation of Cu and Zn in anaerobically digested AD alone AD of raw sludge, 35 °C, 79 days, and pH A79
sludge was dominated by sulfides based on XAS analyses.18 7.69
However, Dong et al. reported that AD increased the HT alone 90 °C, 4 h, and pH 6.04 H90
bioavailability of Cu and Zn using the SCE method.19 AD HT-AD AD of H90-derived slurries, 35 °C, 79 H90A
can also increase the bioavailability of Cr, a common heavy HT- days, and pH 7.49
AD
metal contaminant in sludge.19 Similarly, HT alone can HT alone 155 °C, 4 h, and pH 5.67 H155
significantly affect metal speciation in sewage sludge.15,20 Our HT-AD AD of H155-derived slurries, 35 °C, 79 H155A
days, and pH 7.47
recent study revealed that the transformation of Cu and Zn in
HT alone 185 °C, 4 h, and pH 5.41 H185
sewage sludge during HT was highly dependent on treatment
HT-AD AD of H185-derived slurries, 35 °C, 79 H185A
temperature.15 Cr exists predominantly as an organo-Cr(III) days, and pH 7.46
complex in activated sludge,21,22 and HT can convert
bioavailable Cr fractions into more stable fractions23,24 as raw pH 6.34 raw sludge
oxidizable and residual fractions in HT hydrochars.20,25 A sludge
recent study reported that HT under alkaline conditions favors AD alone AD of raw sludge, 35 °C, 15 days, and pH A15
the immobilization of Cr, while it is the opposite under acidic 7.60
conditions.26 To the best of our knowledge, no study has AD-AD AD of A15-derived slurries, 35 °C, 74 A89
days (89 days in total), and pH 8.44
systematically investigated Cu, Zn, and Cr speciation evolution
AD-HT HT of A15 solids, 90 °C, 4 h, and pH 7.53 AH90
in sewage sludge during combined HT/AD. In addition,
AD-HT- AD of AH90-derived slurries, 35 °C, 74 AH90A
previous studies investigating Cr speciation during AD or HT AD days, and pH 8.45
alone mainly used SCE analysis, which is an empirical method AD- AD-HT HT of A15 solids, 125 °C, 4 h, and pH AH125
that does not provide direct in situ information on the HT- 7.26
speciation of metals.17,27 AD AD-HT- AD of AH125-derived slurries, 35 °C, 74 AH125A
This study aims to (1) characterize the transformation of AD days, and pH 8.38
representative heavy metals Cu, Zn, and Cr during the AD-HT HT of A15 solids, 155 °C, 4 h, and pH AH155
7.24
combined HT/AD of sewage sludge using complementary AD-HT- AD of AH155-derived slurries, 35 °C, 74 AH155A
SCE and synchrotron XAS analyses; (2) compare the effects of AD days, and pH 8.37
HT as a pre- or interstage process (i.e., HT-AD versus AD- AD-HT HT of A15 solids, 185 °C, 4 h, and pH AH185
HT-AD) on metal speciation evolution; and (3) explore the 6.91
underlying mechanisms and the controlling factors such as HT AD-HT- AD of AH185-derived slurries, 35 °C, 74 AH185A
AD days, and pH 8.23
temperature on metal speciation. HT was conducted at 90, a
155, 125, or 185 °C to evaluate different thermal hydrolysis pH values were measured after HT/AD.
conditions. This study fills the knowledge gap in the speciation
evolution of heavy metals during combined HT/AD of sewage 2.2.1. HT-AD System. HT of raw sludge (130 mL per
sludge and provides fundamental knowledge for sustainable reactor) was performed using 200 mL polypropylene-lined
management of sewage sludge and other biowastes. stainless-steel hydrothermal reactors (COL-INT TECH, SC,
USA). The reactors were tightly sealed and heated in an oven
2. MATERIALS AND METHODS at 90, 155, or 185 °C for 4 h (3 h ramping and 1 h holding
2.1. Sludge Sample Collection. Sludge samples were time at the target temperature; six replicates) and then
collected from a municipal WRRF near Atlanta, Georgia, USA. naturally cooled down to room temperature. A portion of the
The WRRF has primary (physical) and secondary (activated HT-treated sludge (HT-derived slurry hereinafter) was
sludge) treatment units and anaerobic digesters. The sludge separated by centrifugation into solids (hydrochars hereinafter,
mixture, a blend of primary and waste activated sludges, was although HT at 90 °C did not readily convert biomass to
collected as raw sludge. Raw sludge has a total solids (TS) chars) and supernatants (HT process water hereinafter). The
concentration of approximately 60 g/L. In addition, secondary hydrochars were freeze-dried and used for composition and
wastewater effluent and anaerobic digestate were collected structure analyses.
from the secondary clarifier and an anaerobic digester of the HT-derived slurry that was not separated was transferred to
WRRF, respectively. The digestate was further anaerobically 600 mL glass AD reactors to achieve a final concentration of 2
preincubated at 35 °C in the lab until no significant biogas g volatile solids (VS)/L. The total sludge suspension volume
production and served as the anaerobic inoculum. All samples was 400 mL in each AD reactor, which also contained
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Figure 1. (a−f) Distribution of Cu, Zn, and Cr in the extracts/residue from sequential extraction of raw sludge, hydrochars, and AD solids. The
relative abundance of each metal in the extracts/residue was calculated by its content in the extracts/residue divided by its total content in the
solids before sequential chemical extraction (SCE). Error bars indicate the standard deviation of measurements (n = 4). Panels (a), (c), and (e) are
for the HT-AD system; panels (b), (d), and (f) are for the AD-HT-AD system.

NaHCO3 (1.4 g/L), anaerobic inoculum (2 g VS/L), and under magnetic stirring. The total suspension in the reactor
secondary wastewater effluent. The AD reactors were was 6 L, containing raw sludge (10 g VS/L), NaHCO3 (1.4 g/
maintained at 35 °C for 79 days while being shaked at ∼220 L), anaerobic inoculum (1 g VS/L), and secondary wastewater
rpm. A control AD experiment was set up to digest raw sludge effluent.
without HT. The 15-day digested sludge suspension without centrifuga-
At the end of AD, an aliquot of the final suspension was tion was further treated by sequential HT and a second-stage
immediately transferred to an anaerobic chamber (COY) filled AD using the same procedures as in the HT-AD system. To
with 95% N2/5% H2, where the solids (AD solids hereinafter) investigate the effect of low-temperature thermal hydrolysis, an
and supernatant (AD process water hereinafter) were additional interstage HT was conducted at 125 °C. The
separated using 0.45 μm membrane filters. The AD solids second-stage AD lasted 74 days. The 15-day digested sludge
were air-dried in the anaerobic chamber and used for suspension without HT was anaerobically incubated with the
composition and structure analyses. same procedure and used as the control.
2.2.2. AD-HT-AD System. Raw sludge was first anaerobically No medium was used in all AD incubations to avoid
digested for 15 days at 35 °C in a capped 9 L glass reactor introducing metals into the sludge. Total biogas volume and
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composition were monitored periodically throughout each AD as compared to their corresponding hydrochars. The acid-
stage; the results will be presented in a parallel study. AD soluble, reducible, and oxidizable fractions of Zn in sample
lasted over 70 days till the production of biomethane reached a H185A are 13.9, 60.2, and 21.2%, respectively.
plateau. The detailed experimental procedures for the two For the AD-HT-AD system, after the first-stage AD, the Zn
systems were also described in our previous studies.28,29 fractions are similar to those in raw sludge. The acid-soluble,
2.3. Sample Characterization. The dried raw sludge, reducible, and oxidizable fractions of Zn in sample A15 are
hydrochars, and AD solids were characterized using SCE (Text 36.7, 53.2, and 10.9%, respectively. Similar trends for HT
S1 in the Supporting Information), bulk XAS, and micro-X-ray hydrochars and final AD solids are observed as those in the
fluorescence microscopy (μ-XRF) coupled with μ-XAS (Text HT-AD system. Compared to the HT-AD system at high HT
S2). A portion of each solid sample was ashed and digested by temperatures (155 and 185 °C), more soluble but less
aqua regia for total metal concentration analysis. The changes reducible fractions of Zn in the final AD solids are observed
in the total concentrations of Cu, Zn, and Cr are provided in in the AD-HT-AD system.
Text S3. For bulk XAS, both Cu and Zn K-edge extended X- 3.1.3. Cr Fraction. As shown in Figure 1e and f, Cr fractions
ray fine structure (EXAFS) and X-ray absorption near edge in raw sludge are 5.5% acid-soluble, 21.4% reducible, 53.3%
structure (XANES) analyses were conducted on dried sludge oxidizable, and 27.8% residual. For the HT-AD system,
samples and corresponding reference compounds. Due to the compared with raw sludge, HT decreased both acid-soluble
low content of Cr (<100 ppm) in the samples, μ-XANES and reducible fractions while increased the residual fraction of
analysis was conducted for Cr analysis. Cr. The change in the oxidizable fraction is subtle after HT.
XAS data analysis used software Ifeffit. 30 Principal For instance, the acid-soluble, reducible, oxidizable, and
component analysis (PCA) in combination with target residue fractions of Cr in sample H185 are 2.9, 6.6, 53.6,
transformation (TT) was conducted on the processed spectra and 39.9%, respectively. After the subsequent AD, the changes
using a suite of reference compounds to determine the number in the acid-soluble and reducible fractions are insignificant.
and identity of end member components for the subsequent However, the residue fraction significantly decreased (e.g.,
linear combination fitting (LCF). The goodness of fitting was from 39.9% in sample H185 to 26% in sample H185A), while
determined by an R-factor, and the fits with the smallest R- the oxidizable fraction increased (e.g., from 53.6% in sample
factors are reported. Details on the Cu, Zn, and Cr reference H185 to 61.2% in sample H185A).
compounds for LCF analyses are in Table S1 and Figure S1. For the AD-HT-AD system, after the first-stage AD, the Cr
fractions are similar to those in raw sludge. The acid-soluble,
3. RESULTS reducible, oxidizable, and residue fractions of Cr in sample A15
3.1. Cu, Zn, and Cr Fractions by SCE Analysis. 3.1.1. Cu are 4.3, 11.7, 58.9, and 20.0%, respectively. Similar trends for
Fraction. As shown in Figure 1a and b, Cu predominantly HT hydrochars and final AD solids are observed to the HT-AD
exists in the reducible (25.8%) and oxidizable (63.5%) system. Compared with the HT-AD system conducted at high
fractions in raw sludge. For the HT-AD system, Cu speciation HT temperatures (155 and 185 °C), the residue fraction of Cr
in sample HT90 is similar to raw sludge. However, HT at high in HT hydrochars and the fractions of acid-soluble and
temperatures (155 and 185 °C) decreased the reducible reducible Cr in the final AD solids are higher in the AD-HT-
fraction and increased the oxidizable fraction of Cu. This AD system.
change is more significant at higher HT temperatures. The 3.2. Cu Speciation by XAS. Cu XANES is used to probe
reducible and oxidizable fractions of Cu in sample H185 are in situ speciation information. For the HT-AD system (Figure
8.1 and 83.9%, respectively. After the subsequent AD (sample S4a), a shoulder at 8982 eV in the spectra of HT hydrochars
H185A), the reducible fraction of Cu increased slightly to became pronounced as compared to raw sludge, indicating the
14.1%, whereas the oxidizable fraction decreased to 73.8%. presence of Cu(I) in the samples. Meanwhile, the shoulder at
For the AD-HT-AD system, Cu speciation is similar to raw 8992 eV became weaker (Figure S4) due to less Cu(II) in HT
sludge after the first-stage AD. The trends in the subsequent hydrochars. These changes are consistent with a previous study
HT and second-stage AD are similar to those in the HT-AD showing the absorption features of Cu(I, II) compounds.31
system. Compared with the HT-AD system, HT hydrochars in The presence of the shoulder at 8982 eV in the spectra of
the AD-HT-AD system have less reducible fraction but more sample A79 was also observed as compared to raw sludge
oxidizable fraction of Cu. The second-stage AD solids have (Figure S4). Moreover, the main peak and pre-edge peak of
more reducible fraction but less oxidizable fraction of Cu than sample A79 significantly shifted to lower energy as compared
those derived from the HT-AD system. to raw sludge, suggesting the reduction of Cu(II) to Cu(I)
3.1.2. Zn Fraction. As shown in Figure 1c and d, Zn during AD. The first derivative of Cu K-edge XANES spectra
predominantly exists in reducible (62.2%), acid-soluble of solid samples is also provided in Figure S5. The peak
(26.0%), and oxidizable (12.6%) fractions in raw sludge. For maximum of the first derivative of sample A79 slightly shifted
the HT-AD system, HT increased the oxidizable fraction and to lower energy as compared to raw sludge, confirming the
decreased the soluble and reducible fractions of Zn as reduction of Cu(II) during AD. Similar changes are observed
compared to raw sludge. For instance, the acid-soluble, for samples H90A, H155A, and H185A as compared to their
reducible, and oxidizable fractions in sample H185 are 6.4, corresponding HT hydrochars. Such energy shifting is less
34.8, and 51.7%, respectively. After AD, the acid-soluble significant for the AD solids after high-temperature HT,
fraction in samples A79 and H90A increases significantly, while suggesting that high-temperature HT inhibited the degree of
the reducible and oxidizable fractions decrease. For instance, Cu(II) reduction during the subsequent AD.
the acid-soluble, reducible, and oxidizable fractions of Zn in For the AD-HT-AD system (Figure S4b), in addition to the
sample H90A are 63.9, 34.2, and 6.9%, respectively. However, absence of a shoulder at 8982 eV, the main peak and pre-edge
for samples H155A and H185A, the acid-soluble and reducible peak of sample A15 did not shift as compared to raw sludge,
fractions of Zn increase, while the oxidizable fraction decreases suggesting that the 15-day duration of the first-stage AD did
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Figure 2. Relative abundance of Cu species determined from linear combination fitting (LCF) analysis of Cu K-edge XANES of the solid samples
from (a) HT-AD and (b) AD-HT-AD systems. Fitting results are also reported in Table S2.

Figure 3. Relative abundance of Zn species determined from linear combination fitting (LCF) analysis of Zn K-edge XANES of the solid samples
from (a) HT-AD and (b) AD-HT-AD systems. Fitting results are also reported in Table S4.

not induce Cu(II) reduction. The trends of energy shifting in chalcopyrite 34.5%) and Cu(OH)2 (11.2%) in raw sludge
Cu XANES spectra (and related redox state of Cu) for the (Figure 2a and Table S2).
subsequent HT hydrochars and final AD solids are similar to For the HT-AD system (Figure 2a, Figure S6a, and Table
those in the HT-AD system. S2), Cu sulfides are the predominant species in the hydrochars
We further conducted LCF analysis of Cu XANES using a similar to raw sludge. However, CuS slightly increases and
large library of reference compounds to quantify Cu speciation chalcopyrite decreases in fractions in the HT hydrochars. For
in the solids. Based on previous studies on Cu speciation in instance, the fractions of CuS, chalcopyrite, and Cu(OH)2 in
sludge,15,18,31,32 our reference compounds included Cu sample H185 are 79.8, 11.0, and 9.2%, respectively. Cu sulfides
sulfides, Cu(OH)2, Cu-phosphate, Cu adsorbed on ferrihydrite still dominate in the subsequent AD solids, but only Cu2S is
(Cu_ad_Fhyd), a Cu-humic complex, etc. (Table S1 and present. The fraction of Cu2S decreases in the AD solids
Figure S1). Our fitting results revealed that the Cu-humic following high-temperature HT. For instance, the fractions of
complex, Cu-phosphate, and Cu adsorbed on ferrihydrite were CuS (66%) and Cu2S (27.3%) in sample A79 decrease to CuS
not significant components. The use of reference compounds (93.7%) and Cu2S (6.3%) in sample H185A.
Cu2S, CuS, chalcopyrite, and Cu(OH)2 yielded the best fitting For the AD-HT-AD system (Figure 2b, Figure S6b, and
results. Note that the oxidation state of Cu in chalcopyrite is Table S2), after the first-stage AD, Cu sulfide is the
best considered to be CuIIFeIIS2 based on XAS analysis.33,34 Cu predominant species in sample A15, similar to raw sludge.
is present predominantly as sulfides (CuS 54.3% and However, 11.4% of ferrihydrite-adsorbed Cu is also present.
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Figure 4. Relative abundance of Cr species determined from linear combination fitting (LCF) analysis of Cr K-edge μ-XANES data of the solid
samples from (a) HT-AD and (b) AD-HT-AD systems. The value for each sample is averaged over two or three hot spots reported in Table S6.

The transformation of Cu for the subsequent HT hydrochars Zn predominantly exists as nano-ZnS (63%), sphalerite (31%),
and AD solids is similar to those in the HT-AD system. and a minor amount of Zn_ad_Fhyd (6%) (Figure 3a, Figure
Cu EXAFS spectra are generally noisy due to the low S9a, and Table S4). For the HT-AD system (Figure 3a, Figure
concentration of Cu in the solid samples (Figure S7), but we S9a, and Table S4), HT did not change Zn speciation even at
still observed the transformation of chalcopyrite into CuS and 185 °C. After the subsequent AD, Zn sulfides remain as the
Cu2S, as well as the inhibitory effect of high-temperature HT dominant Zn species in the AD solids. However, the total
on Cu2S formation during the subsequent AD (Table S3). fractions of ferrihydrite-adsorbed Zn and the Zn-humic
Note that some Cu species with fractions below 10% are kept complex increase from ∼6% in the hydrochars to 38% in the
for XAS LCF analyses, in order to comparatively evaluate the AD solids, whereas nano-ZnS decreases from ∼60% in the
trends of the Cu speciation change in the sludge during HT/ hydrochars to ∼30% in the AD solids. Compared with raw
AD using the same combination of reference compounds. sludge, AD alone partially converted Zn sulfides to
Considering that the error of XAS LCF analyses is typically Zn_ad_Fhyd. The fractions of nano-ZnS, sphalerite, and Zn-
∼10%, Cu species with a low fraction might exist in the solid adsorbed ferrihydrite in sample A79 are 48.8, 19.5, and 31.7%,
samples. These same considerations were also applied to Zn respectively. Compared with sample A79, samples H90A,
and Cr XAS LCF analyses below. H155A, and H185A contain lower fractions of nano-ZnS but
3.3. Zn Speciation by XAS. For the HT-AD system higher fractions of sphalerite, suggesting that prestage HT at
(Figure S8a), the Zn XANES spectra of hydrochars are 90−185 °C induced the dissolution of nano-ZnS during the
comparable to that of raw sludge. However, the main peak of
subsequent AD.
the subsequent AD solids was flattened as compared to their
For the AD-HT-AD system (Figure 3b, Figure S9b, and
corresponding hydrochars. For the AD-HT-AD system (Figure
Table S4), the first-stage AD did not significantly change Zn
S8b), the spectra of the A15 sample are similar to that of raw
speciation in sample A15 as compared to raw sludge. The
sludge, suggesting that the first-stage AD did not change Zn
changes in Zn speciation in the subsequent hydrochars and the
speciation. The changes of Zn XANES spectra for the
subsequent hydrochars and final AD solids are similar to the final AD solids in the AD-HT-AD system are similar to the
HT-AD system. A large library of reference compounds based HT-AD system. LCF analysis of Zn EXAFS (Figure S10 and
on previous studies15,18,32,35 was employed for LCF analysis, Table S5) shows slightly different values as compared to those
including Zn sulfides, hopeite (Zn3(PO 4)2 ·4H2 O), Zn derived from LCF analysis of XANES data (Table S4) but
adsorbed on ferrihydrite (Zn_ad_Fhyd), a Zn-humic complex, overall similar trends on the relative abundance of nano-ZnS
etc. (Table S1 and Figure S1). The use of reference and sphalerite. The differences in fitted nano-ZnS and
compounds nano-ZnS, sphalerite, Zn_ad_Fhyd, and a Zn- sphalerite fractions are possibly due to the EXAFS spectral
humic complex yielded the best fitting results. Note that nano- similarities of nano-ZnS and sphalerite (Figure S1).
ZnS was used for fitting as previous studies suggested it to be 3.4. Cr Speciation by XAS. The μ-XRF images of selected
the main Zn sulfide phase in the sludge.18,35 Sphalerite was Cr hot spots are provided in Figure S11, showing that
chosen as a reference compound, as our previous studies micrometer-sized Cr-containing particles/aggregates in the
showed that Fe content in raw sludge (same sludge used for solids are distributed heterogeneously and preferentially
this study) was much higher than other metals (i.e., Cu, Zn, associated with Fe and/or Si in hydrochars and AD solids.
and Cr) and Fe sulfides were the main inorganic S species in The corresponding Cr μ-XANES spectra are shown in Figure
the hydrochars and AD solids.28,29 Fe is also a common S12. For the HT-AD system, Cr XANES spectra of HT
impurity in Zn sulfide phases. The choice of chalcopyrite as a hydrochars and AD solids differ significantly from raw sludge.
reference compound for Cu XAS LCF analyses was for similar For the AD-HT-AD system, the spectra of sample A15, HT
reasons. LCF analysis of Zn XANES shows that in raw sludge, hydrochars, and AD solids are all different from sample A15.
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To better represent Cr speciation in the bulk sample, we Cu 2 + + S2 − → CuS (2)

averaged the LCF results of μ-XANES from multiple hot spots
(Figure 4). A large library of reference compounds based on
Fe2 + + S2 − → FeS (3)
previous studies36−38 was employed for the LCF analysis,
including a Cr(III)-humic complex, Cr(III) (oxy)hydroxides, In addition, the produced Cu2+ can also be reduced by
mixed Cr(III)-Fe(III) (oxy)hydroxides, Cr(III)-bearing silicate hydroxymethylfurfural (5-HMF)43 or hydroquinones of fulvic
minerals, CaCrO4, K2CrO4, etc. (Table S1 and Figure S1). The acid,44,45 producing Cu+ that can precipitate as Cu2S. In the
Cr(III)-humic complex (∼90%) is the predominant species in AD-HT-AD system, little conversion of chalcopyrite into CuS/
raw sludge, with the rest being FexCr1 − x(OH)3 (sum of Cu2S was observed at 90−155 °C HT due to the alkaline
Fe0.9Cr0.1(OH)3 and Fe0.2Cr0.8(OH)3) (Figure 4a). No environment during reaction (Table 1) as well as the presence
CaCrO4 or K2CrO4 was fitted in raw sludge, consistent with of little amount of Fe3+ (the first-stage AD induced Fe(III)
previous studies showing that Cr(III) phases are the main Cr reduction to Fe(II)) available for chalcopyrite dissolution
species in sewage sludge samples.21,22 Cr(VI) compounds can through eq 1.29 We also observe partial replacement of CuS by
also be readily reduced to Cr(III) by organics and bacteria in chalcopyrite at HT 185 °C, possibly due to the reaction
the activated sludge process.39,40 For the HT-AD system between FeS and CuS.
(Figure 4a), no Cr(III)-humic complex was fitted in the 155 For Cr speciation, the Cr(III)-organic complex is the
°C HT hydrochars, whereas the fractions of Cr 2 O 3 , predominant Cr species in raw sludges.22 Cr2O3 is previously
FexCr1− x(OH)3, and Cr(III)-bearing silicates (fuchsite and observed to occur during HT at 100−180 °C through the
uvarovite) are high. The fraction of Cr2O3 also increases decomposition of the Cr(III)-organic complex.46 Sewage
significantly with increasing HT temperature. For example, the sludge, rich in Si and Al,4,47 can also enable the formation of
dominant Cr species in sample H185 are Cr-bearing silicates low-solubility Cr-bearing silicate phases during HT, such as the
(27%) and Cr2O3 (73%). The fraction of Cr-bearing silicates is fuchsite and uvarovite observed in this study (Table S6). A
very low in the AD solids, and the predominant Cr species are recent study showed that Cr(III)-bearing silicates can
the Cr(III)-humic complex, Cr 2 O 3 , Cr(OH) 3 , and accumulate during Cr phase transformation in hydrothermal
FexCr1 − x(OH)3. For the AD alone sample, a portion of the slurries.48 We also observed the precipitation of FexCr1 −
Cr(III)-humic complex in raw sludge is converted to Cr2O3, x(OH)3, which is a common environmental sink phase of
Cr(OH)3, and FexCr1 − x(OH)3 for sample A79. Cr(III) and has lower solubility than pure Cr(OH)3.36,37
Similarly, for the AD-HT-AD system, the first-stage AD Interestingly, despite the different species observed by XAS
converted a portion of the Cr(III)-humic complex in raw for Cu, Zn, and Cr, SCE reveals that the relative abundance of
sludge into FexCr1 − x(OH)3 and Cr(OH)3 for sample A15 Cu, Zn, and Cr in aqueous extracts and solid residues from
(Figure 4b). The fraction of the Cr(III)-humic complex sequential extraction of solid samples in HT-AD and AD-HT-
decreases and completely disappears in high-temperature HT AD systems is comparable. HT of raw sludge at pH 6.34 (HT-
hydrochars, whereas Cr-bearing silicates, Cr2O3, and Cr(OH)3 AD system) and A15 at pH 7.60 (AD-HT-AD system)
become the predominant species. For the second-stage AD, decreases acid-soluble and reducible fractions of Cu, Zn, and
Cr-bearing silicates and Cr2O3 in HT hydrochars transform to Cr in HT hydrochars but increases the oxidizable and residue
FexCr1 −x(OH)3 and Cr(OH)3 in the final AD solids. No fractions, in agreement with previous studies on the trans-
Cr(VI) compounds were used for fitting the hydrochar and AD formation of Cu, Zn, and Cr during HT of sewage sludge.15,26
solid samples, as no Cr(VI) was observed in raw sludge and The high acid-soluble fraction of Zn in HT hydrochars is likely
both HT and AD created reducing chemical and/or biological due to the presence of nano-ZnS, which has high surface area
environments.28 and many defect sites that are highly reactive and susceptible
to dissolution such as under acidic conditions.49,50
4. DISCUSSION 4.2. Transformation of Cu, Zn, and Cr during AD. Cu
is commonly present as Cu sulfides in sludge, including
4.1. Transformation of Cu, Zn, and Cr during HT. In CuFeS2, CuS, and Cu2S. Their solubility follows the order of
this study, both Zn and Cu exist predominantly as sulfides in CuFeS2 > Cu2S > CuS.51 Cu preferentially exists in its most
raw sludge, similar to previous findings on their speciation in reducible form (i.e., Cu 2 S) in anaerobically digested
mixed primary sludge and waste-activated sludge.15,32,35 sludge.52,53 A recent study reported the reduction of Cu(II)
Because HT also favors the sulfidation of Zn and Cu,15,41 it and formation of Cu2S during AD.18 Anaerobic sulfate-
is not surprising to find both elements remaining as sulfides in reducing bacteria (SRB) can be involved in the transformation
HT hydrochars similar to raw sludge. of chalcopyrite into ferrous sulfides and soluble Cu(II) under
For Zn speciation, nano-ZnS partially transforms to anaerobic conditions.54 The released Cu(II) can then be
sphalerite during HT in both HT-AD and AD-HT-AD systems reduced by 5-HMF derived from HT of sludge or hydro-
(Figure 3 and Table S4), likely due to the aging and quinone-like moieties in organic matter of sewage sludge.55 A
recrystallization of nano-ZnS into the bulk crystalline phase. recent study also showed that AD promotes the transformation
For Cu speciation, in the HT-AD system, HT partially of chalcopyrite into Cu2S.31
converts chalcopyrite (CuFeS2) into CuS and Cu2S (Figure During AD alone (control), CuFeS2 is transformed to CuS
2a). It is likely due to chalcopyrite dissolution in acidic ferric and Cu2S in samples A79 and A89, whereas it is absent in
solution (eq 1) and subsequent precipitation of CuS (eq 2),42 sample A15 (Figure 2). This suggests that 15-day AD is not
where soluble Fe3+ and S2− can be produced from the long enough to induce the transformation of CuFeS2,
dissolution of an Fe(III)-OM complex and hydrolysis of suggesting that transformation of CuFeS2 during AD is a
organic S during HT, respectively.28 slow process. AD of HT hydrochar slurries from higher HT
temperatures (155 and 185 °C) results in the formation of less
CuFeS2 + 4Fe3 + ↔ Cu 2 + + 5Fe 2 + + 3S (1) Cu2S but more CuS, likely due to the lower concentrations of
1621 https://dx.doi.org/10.1021/acs.est.0c05164
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organic matter as electron donors in these samples. Our recent oxidation state, coordination environment, and phase, but this
study showed that increasing HT temperature produces method has intrinsic limitations with a general error range of
hydrochars with more polyaromatic hydrocarbon networks,28 ∼10%. The uncertainty of LCF analysis is potentially caused by
which are not easily oxidized during AD. This is also consistent (1) the similarities in XAS spectra of some reference
with our recent observations that HT at higher temperatures compounds and (2) the difficulties in building a complete
induced less vivianite (Fe3(PO4)2) formation during the library of reference compounds for highly complex and
subsequent AD, where the concentration of Fe in sewage heterogeneous samples such as sludge. Moreover, XAS LCF
sludge is 45.5 times higher than that of Cu.28 analysis alone does not provide direct mobility information as
ZnS/nano-ZnS is previously shown to be the predominant SCE. On the other hand, SCE also has some limitations,15,68
Zn species in AD solids.18,56,57 Our results show the partial for instance (1) SCE cannot directly identify and quantify
transformation of nano-ZnS into adsorbed species (e.g., Zn metal species in mineral phases due to nonspecific dissolution
adsorbed on ferrihydrite) and an organic complex (e.g., Zn- and potential speciation alteration during extraction. For
humic complex) during AD. Compared with ZnS, nano-ZnS instance, as discussed above, SCE showed that the high acid-
has higher total surface free energy, making the surface Zn soluble fraction of Zn in HT hydrochars and AD solids was
atoms highly reactive and prone to dissolution.35,58 Previous due to the dissolution of nano-ZnS, desorption of Zn from
studies showed the transformation of ZnS into ligand ferrihydrite, and decomposition of the Zn-humic complex
complexes such as Zn(OH)m(HS)n or Zn-thiolate in alkaline during acetic acid extraction. (2) The chemical oxidation state
sulfidic solutions under anaerobic conditions.59,60 This is cannot be accurately reflected. For instance, SCE failed to
consistent with the high fraction of the Zn-humic complex observe the reduction of Cu(II) during the AD process. (3)
identified from LCF of Zn XANES in this study, as well as the The extraction efficiency is strongly affected by the sample
high sulfide concentration in AD process water reported in our matrix such as the aggregation state of the solid samples, pH,
parallel studies.28,29 For AD alone, the transformation of nano- and particle size.69 (4) It is difficult to quantify metals
ZnS in the 15-day AD is slower than that in the 79 and 89-day associated with specific minerals due to the nonselectivity of
AD, probably due to the shorter reaction time. extraction reagents and redistribution of analytes and the
Fuchsite and uvarovite formed in HT hydrochars are possible newly formed precipitates during the extraction.70
Cr(III)-bearing silicate minerals. Multiple microbial species With the intrinsic limitations of the two methods, it is thus
can lead to the dissolution of silicate minerals.61,62 Moreover, important to combine them in order to obtain a better
alkaline conditions favor the dissolution of Cr(III)-bearing understanding of such complex matrices. XAS as an in situ,
silicate minerals,63,64 and the pH values are higher than 7 nondestructive, and highly sensitive method can provide
during AD (Table 1). The produced Cr3+ then precipitates as information on the molecular-scale chemical state of an
Cr(OH)3 or the FexCr1 − x(OH)3 solid solution under alkaline element, which can be used to trace the chemical environment
conditions.65,66 during such complex and sequential treatment processes,
For SCE analyses, Cu and Cr predominantly exist as the whereas SCE as an empirical method provides more insights
reducible and oxidizable fractions in the AD solids, whereas Zn into the potential mobility and bioavailability of the solid
predominantly exists as acid-extractable and reducible phases upon contact with environmental media.
fractions. These observations are consistent with previous 4.4. Environmental Implications. This study showed
studies on Cu, Zn, and Cr speciation in anaerobically digested that HT affects the mobility of Cu, Zn, and Cr and promotes
sludge.15,67 The high fraction of acid-soluble Zn in AD solids is the formation of low-solubility Cu and Zn sulfides, Cr2O3, and
due to the dissolution of nano-ZnS, desorption of Zn from Cr-bearing silicates. High HT temperatures (155 and 185 °C)
ferrihydrite, and break down of the Zn-humic complex during favor the formation of lower mobility and bioavailability phases
acetic acid extraction. of Cu, Zn, and Cr.
Overall, the first-stage AD (15 days) in the AD-HT-AD Long-term AD (i.e., 74 or 79 days) favors the reductive
system does not significantly change the predominant species transformation of CuFeS2 into Cu2S and the partial conversion
of Cu and Zn. Thus, the transformation trends of Cu and Zn in of nano-ZnS into ferrihydrite-adsorbed Zn and the Zn-organic
the HT-AD and AD-HT-AD systems are similar. For Cr, the complex. Pre- and interstage HT at high temperatures (155
first stage transformed a portion of the Cr(III)-humic complex and 185 °C) inhibit the formation of Cu2S but enhance the
into FexCr1 − x(OH)3 and Cr(OH)3, but the dominant conversion of nano-ZnS during the subsequent AD. It is
reaction pathways during the AD-HT-AD system are similar important to note that a substantial amount of nano-ZnS is
to the HT-AD system. However, some differences (i.e., types present in HT hydrochars and AD solids. Nano-ZnS is
and contents of some metal species) in the AD-HT-AD system previously shown to be unstable and may pose environmental
are observed as compared to the HT-AD system because the risks through dissolution at low pH,49 with strong ligands,58 or
first-stage AD changed the sludge matrix. For instance, the under aerobic conditions.35 Ferrihydrite-sorbed Zn and the
speciation of Fe, S, and C and pH in the 15-day digested Zn-humic complex can release Zn into the environment
sludge are different from those in raw sludge,28,29 and such through desorption or organic matter mineralization, respec-
differences can affect the evolution pathways of other elements tively.18,35
during the subsequent treatments. For example, our results The predominant Cr species in AD solids are the Cr(III)-
shed light on the role of Fe in the transformation of Cu, Zn, humic complex, FexCr1 − x(OH)3, and Cr(OH)3. Although
and Cr during the combined HT/AD. FexCr1 − x(OH)3 and Cr(OH)3 are the low-solubility phases of
4.3. Comparison of XAS and SCE. This study employed Cr, previous studies have shown that organic ligands (i.e.,
both XAS and SCE to provide complement speciation and siderophores and oxalate) can promote the dissolution of
mobility information on the metals of interest. Synchrotron FexCr1 − x(OH)3 and Cr(OH)3.36 The released soluble Cr(III)
XAS analysis (including LCF analysis) is a well-established and the Cr(III)-OM complex are susceptible to oxidation by
method for determining elemental speciation such as the environmental Mn oxides to form toxic Cr(VI) species.36,71
1622 https://dx.doi.org/10.1021/acs.est.0c05164
Environ. Sci. Technol. 2021, 55, 1615−1625
Environmental Science & Technology pubs.acs.org/est Article

This study provides an improved understanding on the Notes

chemical and biological processes involved in sludge manage- The authors declare no competing financial interest.

■
ment techniques using combined AD/HT. The results provide
insights for the selection and optimization of treatment ACKNOWLEDGMENTS
conditions that can balance the needs for energy and nutrient
recovery as well as contaminant immobilization. Considering This work was supported by the U.S. National Science
the importance of heavy metals for final sludge application or Foundation under grant no. 1739884 (Y.T.). We acknowledge
disposal,4 the transformation and mobility of heavy metals beamline scientists at beamlines 4-1 and 2-3 at the Stanford
throughout their life cycle (i.e., in raw sludge, during Synchrotron Radiation Lightsource (SSRL), 12-BM at the
treatment, and upon disposal or land application in the soil Advanced Photon Source (APS), and 5-ID at the National
environment) warrant future investigation, such as the stability Synchrotron Light Source II (NSLS-II) for assistance in data
of metal sulfides during sludge land application under various collection. This research used resources of the SSRL, APS, and
soil conditions (e.g., varied pH, the presence of organics, and NSLS-II, U.S. Department of Energy (DOE) Office of Science
redox fluctuations). For instance, low-solubility Cu sulfides are User Facilities operated under contract nos. DE-AC02-
the predominant Cu species in AD solids, but the fate of metal 76SF00515, DE-AC02-06CH11357, and DE-SC0012704,
sulfides in soil conditions upon land application of AD solids respectively.

■
remains unclear.18

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*
ASSOCIATED CONTENT
sı Supporting Information
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