Bioresource Technology 351 (2022) 127008

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Short Communication

Insights into high-solids anaerobic digestion of food waste enhanced by

activated carbon via promoting direct interspecies electron transfer
Lili Li a, 1, Qingwei Gao a, 1, Xiping Liu a, Qingliang Zhao a, *, Weiye Wang a, Kun Wang a,
Huimin Zhou a, Junqiu Jiang a
a
State Key Laboratory of Urban Water Resources and Environment (SKLUWRE), School of Environment, Harbin Institute of Technology, Harbin 150090, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• HS-AD of FW under high OLRs with the

addition of PAC, GAC and CAC was
examined.
• PAC performed better than GAC and
CAC in promoting methane yield at
higher OLRs.
• PAC enhanced the process stability via
accelerating the propionate
consumption.
• Potential DIET microorganisms were
selectively enriched with AC addition.
• DIET contribution on methane yield was
quantitively predicted with PAC
addition.

A R T I C L E I N F O A B S T R A C T

Keywords: High-solids anaerobic digestion (HS-AD) of food waste frequently confronted the acidification and failure under
Activated carbon high organic loading rates (OLRs). Results indicated powdered activated carbon (PAC) addition significantly
High-solids anaerobic digestion enhanced methane production and process stability than granular activated carbon, and columnar activated
Food waste
carbon at higher OLRs via accelerating the propionate consumption. Potential direct interspecies electron
Direct interspecies electron transfer
transfer (DIET) partners, including various syntrophic oxidation bacteria and methanogens, were enriched with
Anaerobic Digestion Model No.1
the activated carbon (AC) addition. Furthermore, DIET contribution to methane production was 35% by PAC,
predicated by the modified Anaerobic Digestion Model No.1 (ADM1). This study deeply elucidated the DIET
mechanism and offered the potential foundations for the selection and applications of AC-based materials in HS-
AD of food waste.

1. Introduction to reach 2.2 billion tonnes by 2025 (Mehariya et al., 2018). Anaerobic
digestion (AD) could recover energy in the form of methane (CH4), and it
Food waste (FW), as energy-rich organic waste, is globally estimated had been widely used for efficient disposal of FW (Capson-Tojo et al.,

* Corresponding author.
E-mail address: qlzhao@hit.edu.cn (Q. Zhao).
1
These authors contributed same to this paper.

https://doi.org/10.1016/j.biortech.2022.127008
Received 27 January 2022; Received in revised form 11 March 2022; Accepted 12 March 2022
Available online 16 March 2022
0960-8524/© 2022 Elsevier Ltd. All rights reserved.
L. Li et al.
2021). High-solids anaerobic digestion (HS-AD) (i.e., total solids >15%)
is recognized as a significantly promising technology due to small
reactor size, high reasonable compatibility at high organic loading rates
(OLRs) (Li et al., 2022). However, high OLRs in HS-AD may lead to se­
vere volatile fatty acids (VFAs) accumulation, trigger systematic acidi­
fication, and system failure (Guo et al., 2021). Multiple syntrophic
metabolism of bacteria and archaea could better tolerate environmental
stress caused by high OLRs (Zhang et al., 2018a).
Syntrophic metabolism between VFAs oxidation bacteria and
methanogens convert VFAs into CH4 via generally interspecies hydrogen
transfer (IHT) (i.e., using H2 as the electron acceptor), and direct
interspecies electron transfer (DIET) (i.e., using electrically conductive
pili and c-type cytochromes) (Cavalcante et al., 2021). DIET could
maintain the syntrophic metabolism by resisting to high hydrogen par­
tial pressure (pH2) and providing exogenically favorable Gibbs free en­
ergy, performing faster than IHT (Guo et al., 2021). Therefore, enhanced
DIET is one of the ways to promote system stability and methane pro­
duction in HS-AD under high OLRs. To date, most of studies on DIET
enhancement are mainly focused on the low solids AD of simple organic
waste and wastewater, DIET have rarely been studied during HS-AD of
FW.
Activated carbon (AC), as a common and cheap conductive material,
could significantly increase methane production via strengthening DIET
(Zhang et al., 2018a), accelerating VFAs consumption (Ma et al., 2020),
and reducing the activation loss during electron transfer (Guo et al.,
2021). Moreover, the enrichment of syntrophic microorganisms with the
addition of AC was advanced to promote methane production (Ryue
et al., 2019). Many types of AC materials, such as powder activated
carbon (PAC), granular activated carbon (GAC), and columnar activated
carbon (CAC), are available and retained by filling biomass-support
media composed of AC in the HS-AD reactors. However, few studies
have been conducted to compare the effects of multiple types of AC on
HS-AD performance in FW treatment. DIET mechanisms at high OLRs
have not been fully understood with the introduction of different types
of AC.
In addition, most of studies revealed the DIET mechanism of carbon-
based materials by microbial composition, proteomics (Jing et al., 2017)
and metagenomics (Ma et al., 2020), but they still could not compre­
hensively demonstrate the contributions of DIET. The widespread
application of Anaerobic Digestion Model No.1 (ADM1) offers new in­
sights to gain an understanding of the response of the electron transfer to
the introduction of AC (Batstone et al., 2002). Thus, ADM1 simulations
are critical to reveal DIET-related mechanisms with carbon-based
materials.
This study investigated the performance and DIET mechanism of
different types of AC (i.e., PAC, GAC and CAC) under high OLRs in HS-
AD of FW. The objectives were (1) to evaluate the methane production
and process stability; (2) to explore the dynamics of microbial commu­
nity; (3) to perform quantificationally prediction of the DIET pathway
contribution using the modified ADM1.
2. Materials and methods
2.1. Materials, experimental operation, and analytical methods
The FW and inoculum (i.e., seed sludge) used here were prepared
and stored according to previous study (Wei et al., 2021). More details of
the characteristics of the FW, inoculum, and AC were shown in Sup­
plementary Materials.
Four semi-continuous digesters were built from 500 mL three-necked
flasks with a working volume of 400 mL at 37 ± 1 ◦ C. The semi-
continuous AD lasted for 50 days to shorten start-up period (OLRs
increased from 0.75 to 12 gVS L− 1 d− 1), and all digesters were fed once a
day. PAC, GAC, CAC at 20 g L− 1 were added to digester as follows: ADS,
PAC, ADS,GAC, and ADS,CAC, respectively. One set of digesters was oper­
ated without AC (ADS,CT).
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Bioresource Technology 351 (2022) 127008
Propionate as the sole substrate were added to 200 mL glass serum
bottles with the working volume of 150 mL at 37 ± 1 ◦ C. Three batch
tests were conducted for 10 days, as follows: (i) seed sludge without PAC
(ADB,CT), (ii) seed sludge with PAC (3 g L− 1) addition (ADB,SPAC), and
(iii) digestate from ADS,PAC with PAC (3 g L− 1) addition (ADB,DPAC). The
ratio of propionate substrate and inoculum (based on VS) was 1:3.
The specific surface areas were analyzed by Multi-point BET nitrogen
absorption/desorption method (Quantachrome, USA). Other analysis
involved in this study were determined based on pervious study (Zhou
et al., 2022).
2.2. ADM1 modifications
Several assumptions and simplifications were identified for the
modified model. The decay rates (kd,j ) and ammonia inhibition were
ignored (Razaviarani and Buchanan, 2015). Extracellular electron me­
diators were incorporated in ADM1 according to previous studies (Liu
et al., 2017; Pan et al., 2013). The specific degradation rates of substrate
(km,j ), and half-saturation coefficients (Ks,j ) were taken as variables in
ADM1 in this study. The modified model assumed that 50% VS was the
initial concentration of microorganisms in HS-AD, and the microbial
equivalent mole conversion coefficient was 8.85 mmol g biomass− 1
(Batstone et al., 2002). Equal concentrations of all five types of micro­
organisms, including propionate oxidation bacteria (Xpro ), acetate
oxidation bacteria (Xaa ), acetoclastic methanogens (Xac ), hydro­
genotrophic methanogens (Xh2 ), and methanogenic with DIET (XDIET ),
were assumed in the batch tests. The modified ADM1 was simulated by
AQUASIM 2.0 in this study. The initial state and kinetic equations were
shown in Supplementary Materials. The hydrogen inhibition coefficient,
relative sensitivity index (SI), and evaluation parameters (including the
root mean squared errors (RMSE), mean relative error (MRE), chi-square
test (χ2 ), and fit (R2)) were calculated (Batstone et al., 2002).
3. Results and discussion
3.1. Effect of different types of AC addition on the performance of HS-AD
With an increase in OLR from 0.75 to 12 g VS L− 1 d− 1, cumulative
methane productions of ADS,PAC, ADS,GAC, and ADS,CAC were 143.5%,
100.3%, and 45.2% higher than that of ADS,CT, respectively (Fig. 1a).
During 32 days of operation at the OLRs from 0.75 to 8 g VS L− 1 d− 1, no
significant differences in SCOD, pH, and methane production were
observed for all reactors (Fig. 1b). Subsequently, specific methane pro­
duction (SMP) in ADS,PAC improved by 18.3% as the values of OLRs from
8 to 10 g VS L− 1 d− 1, whereas the SMP of ADS,CT and ADS,CAC decreased
by 23.5% and 16.3%, respectively. ADS,CT performed a dramatically
decrease trend before OLRs raised as high as 12 g VS L− 1 d− 1, whereas
the methanogenic activity of ADS,PAC was not inhibited.
In addition, from 8 to 12 g VS L− 1 d− 1, the average total volatile fatty
acids (TVFAs) concentrations were 13355, 5467, 11055, and 18083 mg
COD⋅L− 1 in ADS,CT, ADS,PAC, ADS,GAC and ADS,CAC, respectively (Fig. 1c).
As one of the VFAs types, propionate was the main factor causing the
VFAs accumulation, which accounted for higher than 70% of the TVFAs.
Noteworthily, TVFAs in ADS,PAC maintained at a low level, even at 12 g
VS L− 1 d− 1.
These findings also indicated higher methane production and more
stable acid-environment with the assistance of larger specific surface
areas of AC, especially >8 g VS L− 1 d− 1. High OLRs easily led to an in­
crease of pH2, DIET might be a primary function to maintain the syn­
trophic metabolism between propionate oxidation bacteria and
methanogens instead of IHT (Guo et al., 2021). Thus, PAC addition
under higher OLRs enhanced system stability via accelerating the con­
sumption of VFAs (especially propionate) related to the syntrophic
metabolism.
L. Li et al. Bioresource Technology 351 (2022) 127008

Fig. 1. Evolution of cumulative CH4 production and SMP (a); pH, and SCOD (b); TVFAs, and VFAs (i.e., acetate, propionate, isobutyrate, butyrate, valerate and
isovalerate) (c); in all digesters during the experiments.

3.2. Dynamics of microbial community with AC addition
3.2.1. Bacterial community
At the class level, the microbiota was dominated by Clostridia. Most
of the syntrophic acetate oxidation (SAO) bacteria known so far belong
to the Clostridia class (Luo and Angelidaki, 2014). This class represented
the majority of the Firmicutes with relative abundances of 4.1%, 22.4%,
39.0%, 41.8% and 26.9% in the inoculum, ADS,CT, ADS,PAC, ADS,GAC and
ADS,CAC, respectively (Fig. 2a). Most importantly, electroactive micro­
organisms within Clostridia could stimulate DIET by utilizing conductive

3
L. Li et al.
Fig. 2. Relative abundance of (a) dominant bacteria class; (b) dominant bacteria genera (relative abundance >2%); (c) dominant archaea phylum in inoculum, ADS,
CT, ADS,PAC, ADS,GAC, and ADS,CAC samples (digested samples from semi-continuous reactors on day 45).
materials as electron conduits (Lim et al., 2020).
Regarding the composition of the genus, Candidatus Cloacamonas,
was the most predominant genus increased from 0.5% (ADS,CT) to 15.9%
(ADS,PAC), 9.4% (ADS,GAC), and 6.5% (ADS,CAC), respectively (Fig. 2b).
This genus was previously reported as hydrogen-producing syntrophic
propionate oxidation (SPO) bacteria (Seo et al., 2019). Ca. Cloacamonas
may lead to the establishment of DIET and IHT pathways in the AD
process (Muratcobanoglu et al., 2021). Syntrophomonas underwent
syntrophic VFAs oxidation in the presence of hydrogen-utilizing mi­
croorganisms. Conductive materials were reported to induce DIET in
syntrophic metabolism of Syntrophomonas with Methanosarcina and
Methanospirillum (Zhang et al., 2018b).
3.2.2. Archaeal community
Methanosaeta, as restricted aceticlastic methanogen, was the most
abundant methanogen in all reactors, which might be related to the
reduction of CO2 to methane by DIET (Rotaru et al., 2014). Compared to
ADS,CT, the relative abundance of Methanosaeta decreased in both ADS,
PAC and ADS,GAC, whereas the abundance of hydrogenotrophic metha­
nogen Methanospirillum significantly increased from 1.1% (ADS,CT) to
19.1% (ADS,PAC), and 26.3% (ADS,GAC), respectively (Fig. 2c). Meth­
anospirillum played a critical role in the biomethanation process by
participating in DIET (Jing et al., 2017).
Overall, the relative abundances of potential DIET partners in ADS,
PAC, including syntrophic oxidation bacteria (Clostridia, Candidatus Clo­
acamonas, Syntrophomonas) and methanogens (Methanosaeta, Meth­
anospirillum) were higher than that of ADS,CT, possibly indicating that
PAC addition improved CH4 production generally via DIET pathway.
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Bioresource Technology 351 (2022) 127008
3.3. DIET contributions on methane production based on modified ADM1
3.3.1. Basic experiment data and global sensitivity analysis
The degradation efficiency and rate of propionate in ADB,DPAC were
higher than that of in ADB,CT and ADB,SPAC during 10 days (Supple­
mentary Materials). Acetate rapidly increased in ADB,DPAC reaching the
peak at the first 2 days due to the faster degradation of propionate.
Compared to ADB,CT and ADB,SPAC, ADB,DPAC significantly shortened the
lag phase of methane production, and exhibited better performance of
methanogenesis. Furthermore, SMP in ADB,SPAC (453.34 mLCH4
gCOD− 1) and ADB,DPAC (475.29 mLCH4 gCOD− 1) enhanced by 15.5%
and 21.1% than that of ADB,CT, respectively. Syntrophic microbial
community in ADB,DPAC promoted the conversion of propionate to ace­
tate and enhanced methane production.
The nine identified sensitivity parameters, including half-saturation
value for hydrogen (KS,XH2 ), propionate (KS,Xpro ), acetate methanogenesis
(KS,Xac ), acetate oxidation (KS,Xaa ), and corresponding Monod maximum
specific uptake rate (km,XH2 ,km,Xpro ,km,Xac , and km,Xaa ) and Monod maximum
specific uptake rate of DIET methanogenesis (km,DIET ), were adopted for
global sensitivity analysis and parameter estimation based on the
experimental data of batch tests. Based on the sensitivity parameters
trends for propionate and methane yield (Supplementary Materials), the
seven high-sensitivity kinetic parameters, includingkm,Xpro ,km,XH2 , km,Xac
and the corresponding half-saturation value, andkm,DIET , were used for
calibrating model. The RMSE (16–36), MRE (0.26–0.48), χ 2 (98–285),
and R2 (>0.97) values of the calibration model had good agreement
between the experimental and simulated results. ADB,DPAC showed the
highest degradation efficiency of propionate (Fig. 3). However, the
fitting results of methane production by modified ADM1 deviated to
L. Li et al. Bioresource Technology 351 (2022) 127008

Fig. 3. Comparison of the simulated and experimental propionate and acetate concentration, and H2 partial pressure in ADB,CT (a), ADB,SPAC (b), and ADB,DPAC (c),
and methane production in ADB,CT (d), ADB,SPAC (e), and ADB,DPAC (f).

some extent from experimental results (Fig. 3d, e, and f). The modified
Table 1
ADM1 only simulated purely numerical calculations while ignoring
Calibration of the high-sensitivity kinetic parameters of the modified ADM1.
changes of the Monod maximum specific absorption rate and half-
saturation constant, inhibition factors, and unevenly microorganisms. Parameter ADB,CT ADB,SPAC ADB,DPAC

Further calibration of the models was needed for fitting the results. km,Xpro 8.55 9.50 10.00
km,Xaa 2.25 2.53 2.75
3.3.2. Prediction of DIET contributions on methane production with PAC km,Xac 2.50 2.50 2.50
km,XH2 5.49 5.56 7.50
Compare to ADB,CT, the values ofkm,Xpro ,km,Xaa , and km,DIET were
km,DIET 0.09 0.45 2.59
increased by 11.1%, 1.3%, and 400% in ADB,SPAC, respectively, and KS,Xpro 299.31 245.68 250.55
km,DIET in ADB,DPAC was substantially improved by almost 5 times than KS,Xaa 535.36 498.56 500
ADB,SPAC (Table. 1). The contribution of acetoclastic methanogens KS,Xac 588.18 620.53 500
6 6 5
(about 53%) was also similar in each reactor (Fig. 3d, e, and f). In ADB, KS,XH2 5.76 × 10− 5.78 × 10− 1.51 × 10−

CT, hydrogenotrophic methanogens also played a more important role.

The partial pressure of H2 was predicted below 10− 4 atm in three batch
CRediT authorship contribution statement
tests and thermodynamically favorable for the propionate oxidation
(Guo et al., 2021). The contribution of DIET increased to 17% in ADB,
Lili Li: Conceptualization, Methodology, Visualization, Data cura­
SPAC. In addition, the contribution of DIET in ADB,DPAC (35%) was higher tion, Writing – original draft, Writing – review & editing. Qingwei Gao:
than other reactors and exceeded the contribution of hydrogenotrophic
Methodology, Visualization, Data curation, Writing – original draft,
methanogens. The prediction also demonstrated that DIET pathway was
Writing – review & editing. Xiping Liu: Conceptualization, Methodol­
constructed and enhanced between propionate oxidization bacteria and
ogy. Qingliang Zhao: Conceptualization, Supervision, Data curation,
methanogens for methane production with the addition of PAC.
Writing – review & editing, Funding acquisition. Weiye Wang:
Conceptualization, Methodology, Writing – review & editing. Kun
4. Conclusions
Wang: Conceptualization. Huimin Zhou: Writing – original draft.
Junqiu Jiang: Funding acquisition.
This study revealed the effects and mechanisms with the addition of
PAC, GAC and CAC in HS-AD of FW under high OLRs. PAC had superi­
ority on the methane yield and VFAs consumption than GAC and CAC. Declaration of Competing Interest
AC with micropore–mesopore structure enriched potential DIET mi­
croorganisms (various SAO and SPO bacteria and methanogens). DIET The authors declare that they have no known competing financial
contribution was quantitively predicted with PAC addition (35%). The interests or personal relationships that could have appeared to influence
modified ADM1 requires further optimization. In addition, future works the work reported in this paper.
should focus on PAC retention, mixing strategy, inhibition factors, and
the assessment of PAC addition for biogas production in real application. Acknowledgements

This research was funded under the auspices of the National Key
Research and Development Program of China (No.2018YFC1900902),

5
L. Li et al.
and the State Key Laboratory of Urban Water Resources and Environ­
ment (No. 2022DX07).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.biortech.2022.127008.
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