Renewable and Sustainable Energy Reviews 115 (2019) 109373

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Renewable and Sustainable Energy Reviews

journal homepage: www.elsevier.com/locate/rser

A review on biochar-mediated anaerobic digestion with enhanced methane T

recovery
L. Qiua,b,1, Y.F. Denga,b,c,1, F. Wanga,b, M. Davaritouchaeed, Y.Q. Yaoa,b,∗
a
College of Mechanical and Electronic Engineering, Northwest A&F University, Yangling, Shaanxi, 712100, China
b
Northwest Research Center of Rural Renewable Energy Exploitation and Utilization of M.O.A, Northwest A&F University, Yangling, Shaanxi, 712100, China
c
School of Chemistry and Chemical Engineering, Jiangsu Key Laboratory for Biomass-based Energy and Enzyme Technology, Huaiyin Normal University, Huaiyin, 223300,
Jiangsu, China
d
The Gene & Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, WA, 99164, USA

A R T I C LE I N FO A B S T R A C T

Keywords: This work comprehensively reviewed the research progress of biochar application in enhancing anaerobic di-
Biochar mediated anaerobic digestion gestion (AD) proficiency. The biogas production and methane content improvement, AD buffering capacity
Methane production enhancement, and ammonia and VFAs inhibition alleviation were thoroughly discussed. AD is a technology for
Ammonia inhibition treating biowastes with energy recovery via microbial communities. However, this process has some limitations,
Acid inhibition
which are particularly noticeable in the AD of biomass which is prone to ammonia or acid accumulation. At the
Microbial metabolism
high ammonia nitrogen concentrations, biochar addition can improve the tolerance of AD system within a
Interspecies electron transfer
specific range. Likewise, at the high organic loading rate (OLR), biochar could effectively delay the time up to
VFAs accumulation threshold. At the microbial level, biochar has been used to support cell immobilization and
microbial growth in AD system. The substantial specific surface area (SSA) and porous structure of biochar favor
the colonization of syntrophic acetogenic bacteria and methanogenic archaea, which facilitate the total organic
carbon removal as well as the reaction rate in AD. As an electron conductor, biochar addition can stimulate
direct interspecies electron transfer (DIET) between syntrophic acetogen and methanogen communities in AD
process. On the surface of biochar, the released electrons from exoelectrogenic microorganisms are directly
transferred to electron-capturing microorganisms, instead of exoelectrogenic microorganisms. Microorganisms
like Geobacter sp. and Shewanella sp, are known to be capable of transporting electrons through a chain of
cytochrome c toward extracellular electron acceptors.
Furthermore, the role of biochar as a carrier material on microbial growth, breeding, and metabolism were
discussed. Also, the interspecies electron transfer (IET) mechanism involved in the AD process with biochar as an
electron carrier was reviewed. Eventually, the policy-oriented recommendations and the research methods of life
cycle assessment (LCA) on biochar-mediated AD are proposed, which can be considered as the reference for AD
development.

1. Introduction
Energy, an vital component of daily life, often taken for granted by
populations who enjoy the comforts of modern society. At the same
time, the degree of deterioration in the environment is much more se-
vere than imagined. The destructive impact of high fossil-oriented en-
ergy carriers consumption has exceeded the capacity of the environ-
ment. Climate changes have substantially endangered public health,
and these impacts are going to be more dangerous in the next decades
[1]. Accordingly, the need to accelerate the growth of alternative en-
ergy sources has attracted more public attention than ever. Wind, solar,
and biomass are the three primary sources of renewable energy and are
expected to become an important source of global energy supply in the
future [2]. Interest in biomass conversion processes has increased in
recent decades due to the need for non-renewable energy sources re-
placement while adding value to the wastes, and improving economic
returns and viability of processes. Different from wind and solar tech-
nologies, biomass is abundant, versatile, and has continuous power

∗
Corresponding author. College of Mechanical and Electronic Engineering, Northwest A&F University, Yangling, 712100, China.
E-mail addresses: xbgzzh@163.com (L. Qiu), dengyf@hytc.edu.cn (Y.F. Deng), alwaysinholiday@outlook.com (F. Wang),
m.davaritouchaee@wsu.edu (M. Davaritouchaee), dzhtyao@nwafu.edu.cn (Y.Q. Yao).
1
Author contributions: Ling Qiu and Yuanfang Deng contributed to this work equally.

https://doi.org/10.1016/j.rser.2019.109373
Received 18 April 2019; Received in revised form 29 August 2019; Accepted 1 September 2019
Available online 08 September 2019
1364-0321/ © 2019 Elsevier Ltd. All rights reserved.
L. Qiu, et al.
Abbreviations
ARISA Automated ribosomal intergenic spacer analyses
FA Free ammonia/NH3 (mg/L)
PBC Pine wood biochar
TAN Total ammonia nitrogen (mg/g)
VCBC Vermicompost biochar
WOBC White oak biochar
SDBC Sawdust-derived biochar
SSBC Sewage sludge-derived biochar
GCA granular activated carbon
SRB Sulfate-reducing bacteria
AD Anaerobic digestion
AFM Atomic force microscopy
CEC Cation exchange capacity (mmol/kg)
generation capacity [3]. According to World Bioenergy Association
(WBA), from 2017 bioenergy will remain the world's largest renewable
energy source, which accounts for 10.3% of the global primary energy
supply [4,5]. The biomass can be converted to energy in different ways,
such as combustion, gasification, and AD. Combustion is one of the
traditional and most straightforward technical processes: it involves the
use of an incinerator in which the biomass is combust. The flue gas is
then used to heat an exhaust-heat boiler in order to drive a turbine in a
steam cycle. The gasification process can produce a stream of syngas
rich in hydrogen and carbon monoxide, which have a relatively high
lower heating value (LHV). AD technology is another possible alter-
native to produce energy from biomass. AD, different from combustion
and gasification processes, not only recycles substances from various
biological wastes but also recovers energy [6].
AD converts organic matter into energy-rich biogas in the absence of
oxygen. Biogas, primarily consisting of CH4, can be used as a renewable
energy source for heating, combined heat and power generation, and
transportation fuel (after being upgraded to biomethane), or can be
upgraded to the quality of natural gas for diverse applications [7]. Since
the biological process for treating organic waste is more complex than
aerobic technologies, AD can be used to recover significant amounts of
energy and thereby benefiting local communities [8]. AD process in-
volves three main steps: substrate hydrolysis, acidification, and me-
thanogenesis [9,10]. In the hydrolysis and acidogenesis process, there
are about 50 bacterial genera, such as Clostridium Spp., Bacillus Spp.,
Bacteroides Spp., Bifido Spp. Bacterium Spp., Butyrivibrio Spp., Proteo-
bacteria Spp., Pseudomonas Spp., Streptococcus Spp., Eubacterium Spp.
and others [11,12]. Methanogens are archaea, so far it has been found
that 65 kinds of species belong to 3 orders, 7 families, and 19 genus.
Methanobacterium Spp., essential Methanosarcina spp., Methanococcus
Spp., Methanobrevibacter Spp., and Methanomicrobium Spp. are the main
microorganisms responsible for methane production [13,14]. Metha-
nogenesis, the most sensitive stage during the AD process, can be in-
hibited by small variations in operational conditions [15]. The sub-
strates for AD mainly consist of both nitrogen-rich materials (e.g.,
animal feces, food waste, and slaughterhouse effluent) and carbon-rich
materials (e.g., lignocellulosic residues, lipid/carbohydrate, kitchen
wastes, and vegetable wastes). These two types of organic materials are
prone to lead to the excess accumulation of organic ammonia and
acids/VFAs, which inhibit the methanogenesis, resulting in poor sta-
bility and low efficiency of the AD system [16]. In order to overcome
the problem of ammonia and acids inhibition, approaches such as
adding dominant strains [17–19], reducing loading rate [20], adjusting
pH [21], utilizing multiphase AD [22,23], and controlling reaction
temperature [24–26] are usually adopted.
In AD system, ammonia is an essential nutrient for microorganisms
growth, as well as acting as an inhibitor beyond a particular con-
centration [27,28]. Ammonia is derived from nitrogen-rich biomass
2
Renewable and Sustainable Energy Reviews 115 (2019) 109373
DIET Direct interspecies electron transfer
EC Electrical conductivity (ms/cm)
IET Interspecies electron transfer
IFT Interspecies formate transfer
IHT Interspecies hydrogen transfer
IIET Indirect interspecies electron transfers
LHV Lower heating value (J/m3)
OFMSW Organic fractions of municipal solid waste
OLR Organic loading rate (g/L·d−1)
SSA Specific surface area (m2/g)
LCA Life cycle assessment
EC Electrical conductivity (ms/cm)
M.barkeri Methanosarcina barkeri
M. thermophila Methanosarcina thermophila
degradation. The inorganic total ammonia nitrogen (TAN) in aqueous
solution mainly exists in the form of NH4+ and NH3/free ammonia (FA)
[29–31]. The fermentation of proteins and urea releases ammonia-ni-
trogen material which exists largely as the ionized form (NH4+), but
this depends strongly on pH as its pKa is 9.3. Hence the unionized
ammonia form (FA) increases with increasing pH [32]. It has been
proved that the inhibition/toxicity in AD process is due to FA formation
in the solution rather than the NH4+ generation [33]. So far, several
possible mechanisms of ammonia inhibition have been proposed, such
as changing intracellular pH, increasing energy requirement, and in-
hibiting specific enzyme reactions [30,34–36].
VFAs are the main precursor for methane formation, which play an
important role in the AD process [37,38]. In addition, VFAs can be used
as a parameter to signal the process imbalance in anaerobic digesters
[39]. For easily biodegradable feedstocks which are rich in carbon, AD
always suffers from instability and low biogas output. This is mainly
attributed to the rapid accumulation of VFAs, resulting in pH drop with
a high degree and the methanogens inhibition [40,41].
Biochar is characterized by its large specific surface area (SSA), high
porosity, small bulk density, high stability, feeble electrical con-
ductivity (EC), and strong adsorption capacity which has been widely
used in soil improvement, pollutant adsorption, carbon capture, carbon
storage, etc. [42,43]. The physicochemical properties of biochar pre-
pared from different biomasses vary in elemental composition, mineral
element, SSA, porosity, ash content, carboxylic ester, aromatic, and
aliphatic chain structure [44–46]. In general, pyrolysis temperature
influences the properties of biochar to a different extent [47], and the
increases of the carbonization temperature can affect the positive bio-
char properties such as the degree of carbonization and aromatization,
the pH value [48,49], the proportion of ash, the percentage content of
P, K, Ca, and Mg [50], the SSA, and total pore volume [51,52]. The
negative correlation indicators of biochar include: the polarity [53,54],
pore width [55], production rate, the content of oxygen-containing
functional groups, and the cation exchange capacity (CEC) [50]. The
pores of biochar are responsible for absorbing compounds such as
phosphate, nitrate, nitrite, ammonium, pesticides, metals, and carbon
dioxide [56]. The sorption mechanisms of a biochar material are similar
to other adsorbents (e.g., activated carbon, zeolite, and bentonite)
[57–59]. Biochar offers surfaces that can be used as carriers for mi-
crobial enrichment and colonization [60], which promote the inter-
species electron transfer (IET) in AD process.
In recent years, biochar has been studied as an additive in AD, and
has been widely verified to be able to improve the biogas production
and methane content, enhance buffering capacity, alleviate ammonia-
acid inhibition, and improve microbial enrichment and IET among
syntrophic consortia [61–64]. Biochar can enhance microbial enrich-
ment and colonization as a microbial-carrier by accepting electrons
from a donor and transferring them to the acceptor. Currently, the
L. Qiu, et al. Renewable and Sustainable Energy Reviews 115 (2019) 109373

influence of biochar as a microbial-carrier on microbial enrichment and
colonization as well as the mechanism of an electron carrier in IET in
AD has become a research hotspot. This study reviewed the role of
biochar in AD in terms of methane production, ammonia, and VFAs
regulation, and microbial metabolism, especially the IET mechanism
related to methanogenesis.
2. Influence of biochar addition on biogas production and
methane content of AD
Present studies mainly focus on the behavior of biochar in the AD
system. It is known that biochar possesses the ability to improve the
biogas production and methane content. Improving biogas production
rate and methane content and enhancing process stability and slurry
quality are important factors for the practicability of AD. In addition,
some intermediate inhibitors which are produced during AD process,
such as sulfide and inorganic nitrogen, VFAs, long-chain fatty acids, and
limonene have a serious negative effect on efficiency and process sta-
bility of AD. Table 1 combines the studies of biochar additive in the AD
process and indicates that the addition of biochar helps improve
biogas/methane production. Kumar et al. (1987) and Ithapanya et al.
(2012) carried out mesophilic (35°C) AD of cattle manure, where the
produced biochar from charcoal powder and rice husks at 900–1000°C
were added to AD system and led to 17.4% and 28.9% increase of
biogas production, respectively [65,66]. Luo et al. (2015) implemented
mesophilic (35°C) AD of glucose in which biostable biochar obtained
from fruitwoods at approximately 800°C of pyrolysis temperature was
added to the process. The result showed that biochar shortened the
methanogenic lag phase, and the maximum methane production rate
increased by 86.6% [67]. For mesophilic (40°C) solid-state AD of or-
ganic fractions of municipal solid waste (OFMSW), both biogas and
methane productions increased around 5% with 5% of biochar addi-
tion. The used biochar was produced from a clean forestry wood residue
(holm oak) at 650°C of pyrolysis temperature [68]. It is speculated that
biochar can absorb CO2, ammonia, and H2S. Biochar also acts as a
buffering agent for alleviating ammonia and acids inhibition simulta-
neously. In addition, the porous structure of biochar creates habitat for
microbials and provides a suitable environment for microorganisms
colonization, thus benefits the quality improvement of biogas [69].
Various results have shown that biochar also can promote the conver-
sion of dissolved organic substrate into methane. In AD of chicken
manure, biochar improved cumulative methane production [70]. Viggi
et al. (2017) selected three charcoal-like products obtained from
pyrolysis of different lignocellulosic matadge. The produced biochar
from pine wood (PBC) and white oak biochar (WOBC) at 500–700°C of
pyrolysis temperature was added to AD system [71]. It was found that
biochar addition enhanced the activities of methanogenic microbial and
reduced the CO2 content in biogas. For both mesophilic and thermo-
philic operations, all biochar-amended digesters led to higher methane
content (75.3–96.7%) than no biochar addition group (65%) on day 1.
SEM images showed that both PBC and WOBC consist of irregularly
shaped particles with a rough surface, highly honeycomb-like porous
structure with desirable chemical properties. These biochar types were
used as AD amendment material to separate CO2 from biogas in the
digester. For both mesophilic and thermophilic AD, the digesters with
biochar addition maintained pH in a slightly alkaline range (7.24–7.43
and 7.43–7.61 for mesophilic and thermophilic, respectively). How-
ever, during thermophilic AD, the methane content (75.3–84.3%) from
the biochar-amended digesters on day 1 were significantly lower
(p < 0.001) than that observed at mesophilic temperature
(89.7–96.7%). These results showed biochar improved methane content
of mesophilic digesters more pronouncedly than that of thermophilic
digesters [71]. This is due to the weak adaptability of initial microflora
to the temperature changes [72]. Under the mesophilic condition, the
dominate microbials are Methanosarcina spp. and Methanosaeta spp.,
and in thermophilic condition, Methanomicrobiales and Methanobacter-
iales are the major microbials [73]. The dominant microflora of in-
oculum in ambient temperature is more similar to that in mesophilic AD
[74]. Liang et al. (2016) studied AD of chicken manure and muskmelon
leaf residue under different AD temperatures [75]. The effect of 5%-
biochar addition from fruitwood on the anaerobic reactor was dis-
cussed, and the results showed mesophilic AD (35°C, 45°C) started
faster with inoculum domesticated at ambient temperature, compared
to that of thermophilic AD (55°C) [75]. Therefore, biochar addition
enhanced process stability of mesophilic AD with a lower dosage
(2.20–2.49 g/g dry matter of sludge), but microbial activity and kinetics
could be inhibited by high dosage (4.40–4.97 g/g dry matter of sludge)
[71]. Yin et al. (2019) applied biochar into microbial electrolysis cells
for methane production, compared with the control group, biochar
addition increased methane production by 27%, meanwhile increase
the volatile solids (VS) removal efficiency by 179% [76]. Linville et al.
(2017) applied in-situ biogas upgrading for CO2 removal during AD of
food waste with walnut shell biochar. Research founded that the fine
walnut shell biochar has better CO2 absorption capacity compared with
the coarse walnut shell biochar. The former could improve the methane
content to 85.7%, and remove the carbon dioxide up to 61%

Table 1
Biogas/Methane yield changes in biochar mediated process.
Biochar/amount Pyrolysis Substrate in AD Temperature in AD Methane production efficiency Ref.
temperature

Charcoal powder/5% – Cow slurry 35°C Batch operation: Biogas yield increased 17.4% [65]
Continuous operation: Biogas yield increased 34.7%
Rice husks/– 900–1000°C Cattle manure 35°C Biogas yield increased 28.9% [66]
Waste wood chips of apple trees/5% 550°C Chicken manure 35°C Biogas yield increased 45.24% [78]
Fruitwood/5% 550°C Muskmelon leaf residue & 35°C Methane production increased 18% [79]
chicken manure
Fruitwood/10g/L 800°C Pulp sewage/Glucose 35°C Methane production rate increased 70.6% [67]
Orchard/1.25g 500°C Food waste 20 °C Methane production rate enhancement 5.0 fold [80]
Wheat bran/1.25g 800°C Food waste 20 °C Methane production rate enhancement 3.9 fold [80]
Wheat straw/5% 550°C Chicken manure 35°C Methane production increased 33.33% [70]
Wood chips/5% 550°C Chicken manure 35°C Methane production increased 68.97% [70]
Wood/1.25g 500°C Food wast 20 °C Methane production rate enhancement 4.6 fold [80]
PBC/2.49g/g – Wastewater sludge 37°C Methane volume percentage increased 14.42% [71]
PBC/2.49g/g – Wastewater sludge 55°C Methane volume percentage increased 47.80% [71]
WOBC/2.20g/g – Wastewater sludge 37°C Methane volume percentage increased 14.87% [71]
WOBC/2.20g/g – Wastewater sludge 55°C Methane volume percentage increased 46.38% [71]
Walnut shell biochar/.83 g biochar 900°C Food waste/sewage sludge 55°C Methane volume percentage was 85.7%, carbon [77]
(g VS added)−1 dioxide removal was 6%
Chicken manure/5% 550°C Chicken manure 35°C Methane production increased 32.76% [70]

3
L. Qiu, et al.
simultaneously. Response surface analysis models presumed that high-
quality methane content (> 90%) can be achieved byutilizing 1.94 g
biochar (g VSadded)−1 at mesophilic temperature. This technology
provided a new upgrading process to efficient and economical methane
production from food waste AD, including enhanced carbon dioxide
removal, improved process stability, as well as elimination of energy-
intensive biogas cleanup process [77].
3. Influence of biochar addition on the metabolic mechanism of
intermediate products in AD
Although biogas production through AD has been established for
some decades, there is still a need for optimizing this process in terms of
process stability and methane production efficiency [81]. Biochar has
been found to promote methane production due to the absorption of
produced inhibitive intermediate metabolites in AD [82–84]. In the AD
process, the mismatch between physicochemical properties of fermen-
tation materials and physiologically metabolic demands of micro-
organisms is a common phenomenon [31,85,86]. Ammonia or acid
inhibition is mainly manifested as the localized overconcentration in
AD of a single substrate, which can break the nutritional balance be-
tween microorganisms and feedstock. This phenomenon can result in
the disability of functional bacteria to grow, breed, and metabolize
[16,67]. For the AD of nitrogen-rich materials, an increase in both pH
and temperature engages a shift to FA (Eq. (1)). FA is membrane-
permeable, which is considered as the main reason for inhibition
[35,87]; accordingly it has a stronger inhibitory effect on methanogenic
microorganisms than NH4+ [88,89]. The hydrophobic ammonia mo-
lecule can passively diffuse into the cell, causing proton imbalance, and
potassium deficiency [89,90]. The resulted inactivation of methanogens
prevents its consumption of VFAs. Process instability caused by am-
monia often leads to accumulation of VFAs, which causes a decline in
pH and a decrease in FA concentration. The mutual effect between FA,
VFAs, and pH may give rise to an “inhibited steady-state” condition.
Under this type of condition, the process has a stable operation but
suffers from low methane production [91,92]. The observation above is
related with often observed shifts from acetotrophic to hydro-
genotrophic methanogenesis with increased total/FA concentrations
[93–95]. Hence, the efficiency and process stability of the AD system
are low which restrict the quality of biogas output [96]. In AD system, it
is challenging to enable the transformation of TAN through microbial
metabolism; also, ammonia inhibition is often hard to avoid when the
load of the organic substrate is high [97].
NH+4 + OH· ↔ NH3 + H2 O (1)
For the AD of carbon-rich materials, during the hydrolysis phase,
macromolecules (such as carbohydrates) are decomposed into amino
acids, sugars, and fatty acids by bacteria [13] and fungi [98]. After-
ward, the acidification bacteria convert hydrolysate into micro-
molecules (such as organic acids, acetate, alcohols, CO2, and H2).
Table 2
Evaluation of ammonium adsorption in biochar for treatment of AD.
Biochar sources Pyrolysis condition AD substrate
Paper sludge & wheat husks 500°C/20 min CH6N2O2CH5NO3
Wood cuttings 600°C/10 h Piggery manure + NH4Cl
Rice husks 600°C/10 h Piggery manure + NH4Cl
Corn cobs, hardwood and mixed 600°C/8 h Swine manure
sawdust
Holm oak 650°C Pig and cattle slurry& food wastes
Straw from biogas residue Impregnated in KOH/12 h, NH4+-containing of pig manure
550°C/2 h slurry
Pig manure from biogas residue Impregnated in KOH/12 h, NH4+-containing of pig manure
550°C/2 h slurry
Pig manure from biogas residue Hydrothermal carbonization Pig manure
190°C/4 h
4
Renewable and Sustainable Energy Reviews 115 (2019) 109373
Acidification bacteria then consume fatty acids and alcohols to produce
acetate. The accumulation of VFAs is a point where the buffering ca-
pacity of the digester is broken, and the pH falls to < 6, which corre-
sponds to a loss of methane production [99–101]. Siegert and Banks
(2005) found that VFAs concentrations of 2 g/L resulted in 75% in-
hibition in cellulose hydrolysis. Similarly, another study reported in-
hibition of cellulose hydrolysis when VFAs exceeded 1.8 g/L [102,103].
Another study investigated the effect of VFAs accumulation with the
high organic load in a batch reactor treating kitchen waste. It is found
that VFAs at 5.8–6.9 g/L was completely inhibitory to methanogens
[104]. Consequently, the accumulation of intermediate metabolites
leads to the inhibition of microbial activities, which is the main reason
for acidity in AD system [96].
Using biochar to achieve local slow-release of inhibitor in the AD
system with high concentration is one of the most promising techno-
logical strategies to improve the quality and efficiency of biogas pro-
duction [105–108].
3.1. Biochar addition for overcoming ammonia inhibition in AD
A well-known problem concerning AD of nitrogen-rich materials is
the inhibition resulted from excess ammonia accumulation [109].
Nevertheless, nitrogen-rich materials, such as animal wastes and
slaughterhouse by-products are desirable substrates for biogas pro-
duction [31,84,110]. Biochar addition can improve the tolerance of AD
system to the high concentration of ammonia. Giwa et al. (2019) found
that biochar has a significant effect on the reduction of Ammonium-N
concentration above 2450 mg/L, while is beneficial to the biode-
gradation of VFAs in long run operations [111]. It has been observed
that biochar can improve the efficiency of AD by reducing the inhibi-
tion of ammonium (NH4+-N), meanwhile, promoting the breeding of
archaea. Table 2 shows the adsorption effect of biochar on ammonium
in AD. Mumme et al. (2014) pyrolyzed paper sludge and wheat husks
(500°C) to make biochar as additives for mesophilic (42°C) AD, where
no significant effect on biogas production was observed, however, ki-
netic and microbiota analysis revealed that biochar could prevent am-
monia inhibition with a 2.1 g/kg of TAN concentration in AD system
[112]. Lü et al. (2016) also reported that the application of biochar
alleviated ammonia inhibition during AD of a glucose solution at 7 g-N
L−1 of NH4+ [16]. The ability of biochar to sorb ammonia has been
indicated before [113]. Previous work has shown 8.61–114 mg TAN
g−1 as a range of ammonia sorption for biochar mediated AD system
(Table 2) [112,114–117]. A possible explanation is that microbial can
grow on the surface of biochar particles and form biofilms, which is
known to be more effective in overcoming ammonia inhibition than
suspended microorganisms [118]. According to Su et al. (2019), bio-
char has been supplied to control internal circulation (CIC) reactor with
the ammonia nitrogen stress of 1500 mg/L. High-throughput sequen-
cing revealed that the abundance of Clostridiales, Lactobacillales, and
Methanoculleus spp. increased, while the abundance of Syntrophomonas
Ammonium load Absorption efficiency Ref.
−1
500 mg N kg Prevented mild ammonia inhibition [112]
1390–1450 mg/L NH4+-N adsorption was 44.64 mg g−1 [114]
1390–1450 mg/L NH4+-N adsorption was 39.8 mg g−1 [114]
500–580 mg/L NH4+-N adsorption between 27.2 and [115]
114 mg g−1
3195–4207 mg/L NH4+-N removal was 8.61 mg g−1 [116]
855 mg/L NH4+-N adsorption was 19.16 mg g−1 [117]
855 mg/L NH4+-N adsorption was 26.82 mg g−1 [117]
– N2 adsorption was 8.5 cm3g−1STP [136]
L. Qiu, et al.
spp. decreased. Meanwhile, the abundance of Methanoregulaceae, Bac-
teroidales, Anaerolineales, and Syntrophobacterales. increased [119]. Ac-
cording to Giwa et al. (2019), in long run operations (350 days) AD
system, with ammonia-N concentrations above 2450 mg/L and Metha-
nothrix spp. would be the most abundance methanogens in the biochar
addition reactors [111]. The mentioned obtaining prove that the ad-
dition of biochar could alleviate the inhibition from high ammonia
nitrogen concentration in AD system. The functional groups on the
surface of biochar can influence its ammonia adsorption rate [120]. It is
known that black carbon materials have particular properties (e.g.,
oxygen groups, pyrroles, pyridines, quaternary ammonium, OH−, and
benzene ring) that can influence the soil nitrogen cycle and hence, ni-
trogen availability [121–124]. Studies have found that black carbon can
react with various nitrogen compounds [125,126]. Briefly, it is known
that oxygen groups on the surface of oxidized black carbon react with
the adsorbed ammonia, resulting in the formation of amines and amides
under ambient conditions [127]. Additionally, development of che-
mical ring structure (e.g., pyrroles, pyridines, quaternary ammonium)
have been seen in previous system at high temperatures [123,124].
Aqueous water and steam can compete with ammonia for sorption sites
[127,128], while the water films cover black carbon and increase am-
monia solubility which leads to ammonium ions production [123,127].
At ambient conditions, ammonia, with the similar function as Brønsted
or Lewis acid, can react with a surface carboxyl group [124,129], which
leads to the formation of an ammonium salt or an amide. Since am-
monium salts could be dissociated in water, the nitrogen can exist in the
form of ammonium [113]. Moreover, the presence of sulfur groups
[130,131], alkali earth metals [132], and other metals [133] on black
carbon structure enhance the adsorption of ammonia and other com-
pounds by chemical catalytic reactions. Otherwise, ammonia is an al-
kaline substance; therefore the adsorption of ammonia by black carbon
was related to the number of acidic groups on its surface [134,135].
So far, most literature illustrated the relationship between the in-
hibition of the AD process and ammonia concentration [137–139].
There are numerous remediation techniques that have been reported
for controlling ammonia inhibition in AD processes such as struvite
precipitation [140], use of zeolite, and carbon fiber textiles [141,142].
However, these techniques are expensive to implement on a large scale.
Biochar, as an additive, has been successfully applied in AD for over-
coming ammonia inhibition. Further research is essential to study the
role of biochar–microbial polymer in AD system. In the future, biochar
addition will become more and more popular as an alternative method
to solve the problem of ammonia inhibition.
3.2. Biochar addition for overcoming acid accumulation in AD
AD of easy-acidification substrates always suffers instability and low
biogas yield, and even in some cases, the operation can be failed
[143,144]. The acid inhibition in AD process mainly caused by the
rapid accumulation of VFAs, resulting in low pH that can inhibit the
activity of methanogens, particularly at a high organic loading rate
(OLR) [145]. A drop in pH value causes serious inhibition of VFAs and a
decrease in the activity of methanogens, which may result in activity
declines of the acid-sensitive glycolytic enzymes [104,146–148]. Also, a
high concentration of undissociated acids can permeate into the cell
membranes and damage macromolecules [149]. From the perspective
of microbial metabolism, it is mainly due to many reactions (e.g., long-
chain fatty acids/alcohols which are degraded to short-chain acetic
acid, CO2, and hydrogen). Generated acids have high Gibbs free energy
under standard conditionsthat can not carry out spontaneously from the
view of thermodynamics. On the other hand, methanogens are sensitive
to external environment changes, and their growth rate is slower than
acid-producing bacteria [150,151]. In the AD process, hydrolysis,
acidogenesis, and acetogenesis are performed by bacteria, while the
methanogenesis is completed by a specific branch of archaea [152]. In
the acetotrophic methanogenesis phase, acetic acid is converted to
5
Renewable and Sustainable Energy Reviews 115 (2019) 109373
acetyl-CoA, and then methyl is transferred from acetyl-CoA to ectoine
methylpurine. In the hydrogenotrophic methanogenesis phase, methyl
is carried by CO2 and protons is formed by ectoine methylpurine, in
which reduced coenzyme F420 is the leading proton donor; in the me-
thyl compound utilization pathway, the methyl group can sometimes be
directly transferred from the methyl compound [104,153,154]. It is
reported that there are different sensitivities to inhibitors for different
methanogenic pathways. Methanogenesis can take place via the hy-
drogenotrophic or acetotrophic pathway [155,156]. A shift in metha-
nogenic pathways and methanogenic community composition has been
observed when the microbial culture is exposed to the increasing con-
centrations of acetate and ammonia [157]. This means that VFAs as an
inhibitor may have different effects on these pathways. However, it is
unclear what the main pathways and related vital factors are, which are
affected by the excessive accumulation of VFAs during AD [158]. The
exact composition and primary inhibitory type still need to be in-
vestigated when the VFAs inhibition occurs under different OLR of AD
with different materials as substrates. Currently, the main methods for
reducing the VFAs inhibition on methanogenesis activities were focused
on adjusting C/N ratio [159], adding trace elements to accelerate the
growth of methanogens [160], and employing a two-stage digestion
system in order to distinct methanogenesis stage from hydrolysis and
acidification stages [161,162]. All in all, almost all the methods men-
tioned above attempted to reduce the VFAs accumulation, but not much
attention has been paid to the promotion of methanogens viability at
high VFAs concentration. The latest research from Wang et al. (2019)
indicated that biochar addition in high OLR reacter could delay the
time of VFAs accumulation occurrence [163].
Alkaline biochar is widely used to regulate the pH value in the AD
system [143]. The alkalinity of biochar is determined by the properties
of raw material [164–166]. Research in this field also showed that the
alkalinity of biochar raises with an increase in the pyrolysis operating
temperature [167]. The alkaline property of biochar is considered to be
able to raise CH4 content by reacting H2S and CO2 with alkaline sub-
stances in ash. Biogas in-situ and biogas cleanup levels can also be
improved by alkaline property of biochar [69]. Table 3 shows the acid-
buffering capacity of biochar in AD. Biochar can act as a key to link bio-
waste disposal and its valorization, based on its nature of acid-buffering
in the AD process [143]. Luo et al. (2015) compared biochar and non-
biochar incubation of AD system and found that biochar enhanced
biogas production and degradation of intermediate acids simulta-
neously [67]. Likewise, Sunyoto et al. (2016) reported that the appli-
cation of biochar not only enhanced microbial metabolism, but also
maintained a stable pH level during the process of bio-hydrogen pro-
duction [168]. Zhao et al. (2016) found that biochar addition promoted
propionate degradation and alleviated acidification outstandingly.
Thus, it is conducive to optimize the design and stabilize operational
parameters of AD digester [169]. Capson-Tojo et al. (2018) and Wang
et al. (2018) indicated that the biochar promoted propionic and butyric
acids conversion to acetate in the absence of metabolism by H2-con-
suming methanogen [170,171]. The vermicompost biochar (VCBC) has
the alkaline properties, as shown in literature, the contents of alkali
metals (Na, K) and alkaline-earth metals (Ca, Mg) were 8.47 g/kg,
2.53 g/kg, 15.82 g/kg, and 0.44 g/kg in VCBC, respectively [172,173].
Hence, it can be inferred that the source of alkaline biochar buffering
capacity is from the following chemical reaction (Eq. (2)) which forms a
buffer system. Moreover, the acidic and alkaline functional groups on
the biochar can also provide a certain buffering capacity in solution.
However, further investigation is needed. According to Wang et al.
(2019), sawdust-derived biochar (SDBC) more effectively delayed the
time of VFAs accumulation threshold (30 gCOD/L) than sewage sludge-
derived biochar (SSBC). Meanwhile, the author infers that SDBC would
promote the synthesis oxidation of VFAs [163]. Ye et al. (2018) re-
ported that in two-phase AD for food waste, biochar addition decreased
the lag time for methane production by 41–45%, simultaneously both
VFAs consumption and CH4 output were improved [174]. Cai et al.
L. Qiu, et al. Renewable and Sustainable Energy Reviews 115 (2019) 109373

(2016) also confirmed that in biochar mediated AD, the lag phase is

[168]
[168]
[143]

[143]
[143]
[170]
[67]
Ref.
shortened faster as the inoculum/substrate rate decreased [175].
However, for AD reactors in which acid accumulation have already

The buffering capacity of AD to acetic, propionic, butyric and valeric acid can be greatly improved to 1426.0 mg/L, 712.6 mg/L,
The accumulation and degradation of VFAs under the biochar treatments were significantly faster compared without biochar.
occurred, biochar addition cannot adjust pH value into the normal
range. Luo et al. (2015) showed that pH buffering capacity of AD re-
actor was not significantly increased by biochar addition when acid
accumulation took place due to the increased loading [67].

Ca(Mg)CO3 + Cx Hy COOH ↔ [C x Hy COO]2 Ca(Mg) + H2 O+ CO2

(2)
Ye et al. (2018) also pointed out that the critical role of biochar was
not the lower lag time for biogas production, but sludge inoculum do-
mesticating is much more efficient than adding additives. Biochar has
an important role in microbial metabolism and promoting DIET me-
Propionic acid decreased from 1429.6 mg/L to 585.2 mg/L as biochar supplemented.

chanism, which will be discussed in the following section.

There have been many types of research on the mechanism of al-
leviating ammonia inhibition by the addition of biochar in AD.
However, the number of reports which investigate the mechanism of
VFAs inhibition are few. Biochar mediated AD with a high level of VFAs
should be used to solve the problem of intermediate inhibition. In the
future, further studies on the effects of biochar addition on metabolic
The acetic acid increase at the biochar supplemented group.

pathways, microorganism metabolism, and methane production po-

tential in AD should be conducted.

4. Biochar addition for improving microorganism metabolism and

3064.7 mg/L, and 3783.9 mg/L, respectively.

IET in AD

The porous characteristic of biochar can influence mass transfor-

Propionic type of fermentation.

mation and microorganism metabolism in AD system [16,61,176]. It

Promoting butyrate oxidation
Butyric type of fermentation.

provides an effective way to improve the metabolism of the microbial

community and enhances the potential of microbial breeding in the AD
process. Recent studies have shown that biochar has the potential of
promoting co-metabolism of anaerobic microorganisms via IET.
Efficiency

4.1. Influence of biochar addition on bio-enrichment and breeding of the

microbial community in AD
16.6, 25.1, 33.3 g/L

Strengthening the metabolism balance of microbial community is an

effective way to stabilize AD process. Biochar, as a suitable carrier for
Biochar dosage

biofilm formation in AD system with different waste streams as sub-

strate [67,177] has been used to support cell immobilization and mi-
8.3 g/L
10 g/L

15g/L

crobial growth [178]. The large SSA and porous structure of biochar
Evaluation of the acid-buffering capacity of biochar for the treatment of AD.

5%

5%
5%

favor the colonization of syntrophic acetogenic bacteria and methano-

genic archaea, then facilitate the total organic carbon removal as well
Acetic, propionic, butyric and valeric

as the reaction rate in AD [67,179–181]. For the use of biochar as an

Food waste dewatered activated

additive, Kumar et al. (1987) found an increased number of anaerobic

microorganisms in AD [65]. Liang (2016) found that, under different
ambient temperature, biochar-mediated AD can optimize microbial
community structure and enrich Methanosarcina spp. up to 74.9%,
Food waste-bread
Food waste-bread

Chicken manure

which is 17% higher than that of the non-biochar added group.

Kitchen waste
AD substrate

Meanwhile, the abundance of sulfate-reducing bacteria (SRB) was ex-

Glucose

pressively decreased, and thereby the H2S concentration was sig-

sludge
acid

nificantly diminished [75]. Luo et al. (2015) observed that Methano-

saeta spp. is usually abundant archaea in AD of organic matters;
Pyrolysis condition

nevertheless, biochar addition appeared to improve its resistance to

highly acidic conditions. The percentage of Syntrophomonas spp. in-
650°C/20min
650°C/20min
500°C/2.0 h

500°C/2.0 h
500°C/2.0 h
500°C/1.5 h

creased from 8.0% to 29.2%, when the glucose concentration of AD

system increased from 6 to 8 g/L. The control treatments with no bio-
800°C

char, increased the percentage of syntrophic bacterium Syntrophobacter

spp. from 0% to 13.6% [67]. Schwede et al. (2017) successfully im-
Biochar sources

mobilized methanogenic archaea from AD residues on biochar derived

Vermicompost

Vermicompost
Vermicompost
Pine sawdust
Pine sawdust
Fruitwoods

from municipal solid green waste (pyrolysis at 575°C). In this study, the
Sawdust

immobilized methanogens biochar and artificial syngas mixture (H2,

Table 3

CO, CO2, and CH4) were incubated in mesophilic AD. Conversion of H2,
CO2, and CO was shown within the first 24 h by the formation of CH4.

6
L. Qiu, et al. Renewable and Sustainable Energy Reviews 115 (2019) 109373

However, no CH4 generation was observed throughout the whole AD
with autoclaved biochar. This observations confirm that biochar is a
suitable carrier for methanogenic archaea [182].
From the aspect of spatial and temporal, with the existing of the
biochar, the evolution of the archaea is listed in Table 4. It is found that
fatty-acid-oxidizing and biofilm-producing Syntrophomonas spp. tightly
contacted on the surface of biochar [183]. Meanwhile, its percentage in
the tightly-bound biochar was much higher compared with loosely-
bound and supernatant of biochar. Bacterias belonging to the families
of Ruminococcaceae, Porphyromonadaceae, and Enterobacteriaceae were
observed to be dominant in the suspension fraction, followed by the
loosely-bound biochar and finally, the tightly-bound biochar [67]. Luo
et al. (2015) observed the colonization of Methanosarcina spp. on
fruitwood-derived biochar (pyrolysis at 800°C) in mesophilic AD system
(35°C) of glucose solution, using automated ribosomal intergenic spacer
analyses (ARISA). For the biochar added group, the archaea were found
tightly bound on biochar, and its proportion was higher than the con-
trol where no biochar added. The same conclusion was obtained in the
study by Lü et al. (2016) [16], where Methanosarcina spp. resided deep
within the pore channel of the coarse biochar. This phenomenon was
beneficial for the establishment of methanogenic zones in AD system
[184]. Additionally, Methanosaeta spp. tended to attach on the outer
surface of fine biochar [67]. In AD of molasses waste streams, Vrieze
(2016) found that biochar derived from pinewood (Pyrolysis at 650°C)
possesses the potential of stabilizing AD via high-activity methanogenic
zones [176]. Compared to the AD without biochar addition, the relative
abundance of both Methanosaeta spp. and Methanobacteriales increased
in both mixed liquor and biochar. The relative abundance of Metha-
nosaetaceae on biochar at the end of AD was much higher (13.7% of
total methanogenic communities). While only 0.5% for the mixed li-
quor has been seen, indicating selective enrichment of Methanosaeta-
ceae on biochar as a carrier material. In AD without biochar addition,
the relative abundance of Methanosarcinaceae decreased to values
below the detection limit in the mixed liquor. The Methanomicrobiales
abundance increased on average with a factor of 10 in the mixed liquor
and on the carrier materials. The abundance of Methanosaetaceae, Me-
thanosarcinaceae, and Methanobacteriales were significantly correlated
positively to the methane production, while the Methanomicrobiales
abundance was significantly correlated negatively to the methane
production. This study showed that biochar is an appropriate carrier
material for the selectivity enrichment of methanogens [176].
From the aspect of biochar particle size, as shown in Table 4, The
content of bacteria belonging to the family of Clostridiaceae included
Clostridium spp., Oxobacter spp., and Clostridiaceae spp. type II, in the
larger biochar particle (2–5 mm) treatments, were higher than that in
the smaller biochar particle (75–150 μm) treatments [67]. Methano-
sarcina spp. was located on the surface of tightly-bound part of the
biochar and was most abundant in the type with 2–5 mm particles size.
Methanosaeta spp. was enriched in the loosely-bound parts by all-size
types and enriched in small particles (75–150 μm) in tightly-bound
parts of the biochar [67].
From the aspect of modified biochar, most of the microbial com-
munities in carbon nano-tubes, belong to Clostridia spp. which mainly
involves in the families of Ruminococcaceae and Clostridiaceae. With
respect to microbial metabolism, the metabolites of Ruminococcaceae
mostly include acetate and ethanol, while it is butyrate for
Clostridiaceae [185]. However, other fermentative bacterial genera such
as Caloramator spp., Anaerobaculum spp., Thermogutta spp., and Hy-
drogenispora spp. showed a relatively lower abundance when biochar
was present [186–189].
4.2. Influence of biochar addition on IET involved in AD
4.2.1. IET mechanism
In AD system, IET between syntrophic partners plays a vital role in
oxidizing high organic matters and reducing CO2 to CH4, which is also a
crucial procedure to break through the thermodynamic barrier to
maintain breeding between syntrophic bacteria and methanogens
[190]. It is well known that the syntrophic partners for methane pro-
duction involve indirect interspecies electron transfers (IIET) me-
chanism: interspecies hydrogen transfer (IHT) and interspecies formate
transfer (IFT) [190]. Lately, direct interspecies electron transfer (DIET)
has been recommended as a new mechanism in AD system
[63,191–193]. DIET mechanism replaces hydrogen as the primary route
for IET, which can improve the resistance of the anaerobic system to
some severe conditions, and maintain the syntrophism between aceto-
genic and methanogenic bacteria [194].
In DIET communities, released electrons from exoelectrogenic mi-
croorganisms are directly transferred to electron-capturing micro-
organisms [195,196]. Most well-known exoelectrogenic microorgan-
isms, such as Geobacter sp. and Shewanella sp, are known to be capable
of transporting electrons through a chain of cytochrome c toward ex-
tracellular electron acceptors [197]. Biological DIET includes two kinds
of mechanisms in the form of cell-to-cell electron transfer via biological
components like c-type cytochromes and conductive pili. In first me-
chanism, electrons passed directly to the acceptors via cytochrome c on
the cell membrane [198–200]. Summers et al. (2010) reported that
Geobacter metallireducens and Geobacter sulfurreducens were able to form
conductive aggregates resort to conductive cytochrome c from G. Sul-
furreducens in the ethanol oxidation syntrophic system to achieve IET
[201]; In second mechanism, extracellular electrons transferred
through Pili and other cell appendages [197,202,203]. Conductive pili
are protein filaments produced by microorganisms for long-range
electron transfer under suitable conditions, and have been observed in
many studies by atomic force microscopy (AFM). Through pili, longer-
range electron transfer can occur without direct contact to insoluble

Table 4
Temporal and spatial evolution of archaea in biochar addition AD system.
Type of microbial community Ref.

Spatial evolution of microbial
community
Temporal evolution of microbial
community
All-size biochar fraction
Larger-sized biochar particle
(2–5 mm)
Medium-sized biochar
(0.5–1 mm)
Small-sized biochar
(75–150 μm)
Carbon nano-tubes
Early stages of AD
Later stages of AD
AD day of 42
End of AD
Syntrophomonas spp. (tightly-bound fraction), Methanosaeta spp. (loosely-bound fraction) [183]
Clostridium, Oxobacter and Clostridiaceae type II, Methanosarcina spp. (tightly-bound fraction), [16,67]
Methanosaeta spp. (loosely-bound fraction), Methanoculleus (tightly-bound fraction)
Methanosaeta spp. (loosely-bound fraction), Methanosarcina spp. (inner sphere of biochar), [16]
Methanoculleus (tightly-bound fraction)
The innermost layer of biochar: Methanosaeta spp. (tightly-bound fraction), Methanosarcina [16,67,184]
spp., Methanoculleus;
The outer surface of biochar: Methanosaeta spp. (tightly-bound fraction)
Ruminococcaceae and Clostridiaceae [185]
Methanosaeta spp. [16]
Methanosaeta spp. (loosely-bound fraction), Methanoculleus (tightly-bound fraction), [16]
Methanosarcina spp. (inner sphere of biochar)
Methanomicrobiales (Increased tenfold) [176]
Methanosaetaceae (13.7%) [176]

7
L. Qiu, et al.
minerals, solid electrodes, other microorganisms, and even electrically
conductive biofilm. Reguera et al. (2005) proved that the conductive
pili of G. sulfurreducens could play an important role as nanowires in the
electron transfer process from the surface of the cell to extracellular Fe
(Ⅲ) oxides [204]. However, Malvankar et al. (2011) found evidence of
the irrelevance of cytochromes and electron transfer in conductive
biofilms of G. sulfurreducens [205]. AFM images showed that cyto-
chromes were not located close enough on pili to enable the hopping or
tunneling of electrons. Furthermore, the inactivation of the cyto-
chromes did not have any negative effect on biofilm conductivity. Thus,
the authors reported that long-range electron transfer via nanowires of
G. sulfurreducens was based on nonlocality electron transfer [205,206].
4.2.2. The IET mechanism related to methanogenesis
In terms of IET mechanism, studies are currently focusing on me-
thane production via organic acids (acetic acid, propionic acid, butyric
acid, and benzoic acid) conversion in syntrophic association system
[169,194,207–209]. Table 5 shows the representative strains of archaea
involved in IET. The archaea that have been proved to be able to pro-
duce methane mainly through IET mechanism are Methanosarcina spp.
and Methanosaeta spp [210]. Currently, the reported microorganisms
that take part in the syntrophic metabolism with methanogenic archaea
mainly include: Geobacter spp., Pseudomonas spp. [195,211], Syn-
trophomonadaceae [208], Syntrophomonas spp., Sulfurospirillum spp.
[212], Tepidoanaerobacter spp., Coprothermobacter spp. [213], Thauera
spp. [214], Clostridium spp. [215], Peptococcaceae spp., Bacillaceae spp.
[209], Sporanaerobacter spp. [63,216], Bacteroides spp., and Strepto-
coccus spp [217]. New research in this area demonstrated that there is
an IET mechanism between Geobacter sp. and its syntrophic partners in
the anaerobic biotreatment system of wastewater (Table 5) [201]. The
electron transfer efficiency of Geobacter sp. was improved by the ad-
dition of activated carbon [218]. Rotaru et al. (2014) proved the ability
of methanogens (M. barkeri) to participate in IET with Geobacter me-
tallireducens in a co-culture system (Table 5) [192]. The presented re-
sults were comparable to that of the first experimental study in which
two species exchanged electrons for the metabolism of ethanol to me-
thane [201]. The experimental results strongly suggested that the direct
use of electrons by M. barkeri occurred as shown in Fig. 1, rather than
conventional hydrogenotrophic methanogenesis [219].
Furthermore, it is well known that adding conductive materials such
as carbons and iron nano-particles to AD digester can stimulate DIET
mechanism within numerous microorganisms, which do not create
conductive nanowires like Geobacter species [218]. Biochar could pro-
mote IET in defined co-cultures and may aid in the enrichment of
syntrophic partners capable of DIET [169]. On the surface of biochar,
the enrichment of syntrophic bacteria can utilize biochar as electrical
conduits for electron exchange [196]. The electron transfer velocity of
DIET is 106 times faster than IIET [194], which makes the substrate to
degrade much faster. Compared to IIET, the DIET mechanism consumes
substrates and intermediates faster and is more stable [220]. Besides,
DIET does not need a complex enzymatic reaction to produce, consume,
Table 5
Representative strains of archaea involved in IET.
Representative microbiota Cooperative metabolic bacteria
Methanothermobacter thermoautotrophicus Pelotomaculum thermopropionicum
Methanosaeta spp. harundinacea Geobacter metallireducens
M. barkeri Geobacter metallireducens
Metallireducens-M. barkeri Metallireducens–Geobacter sulfurreducens
Geobacter metallireducens Geobacter sulfurreducens
Methanobacterium IM1
Carbon dioxide-reducing methanogens Propionate-oxidizing acetogens
Methanospirillum,
Methanosphaerula, and Methanobrevibacter
M. thermophila Tepidanaerobacter syntrophicus
M. thermophila Coprothermobacter proteolyticus
8
Renewable and Sustainable Energy Reviews 115 (2019) 109373
Fig. 1. Mechanisms of conductive material-mediated DIET: Biochar as a con-
ductive material can promote DIET, which has been identified as an important
mechanism for IET between syntrophic microorganisms involved in the anae-
robic degradation of VFAs in AD [196].
and diffuse the redox mediators [196]. Chen et al. (2014) found that
ethanol can hardly be degraded without the addition of biochar in the
co-culture system, and only a small amount of methane was produced
[221]. The biochar mediated group can degrade ethanol rapidly and
thoroughly, and the amount of produced methane is equivalent to the
theoretical value of stoichiometry. Wang et al. (2019) found that Te-
pidimicrobium spp. and Methanothermobacter spp. were abundant on
SDBC; these two kinds of microorganisms have the potential ability of
extracellular electron transfer [163]. Yin et al. (2019) found that bio-
char addition could facilitate DIET through substituting Thermincola
spp. on the anode, meanwhile enrich Methanothermobacter spp. on
cathode [76]. Adding conductive materials such as biochar could not
only provide sites for the microflora, but also act as electrical conduits.
It was speculated that conductive biochar can promote DIET between
syntrophic acetogen and methanogen communities by serving as an
electron conductor in AD process, accelerating methanogenesis [221].
Biochar addition can also attain the richness of the electro-active
Anaerolineaceae and Methanosaeta spp., and thus stimulate DIET [170].
Besides, the addition of magnetite (Fe3O4) to acidogenesis could en-
hance the acidification efficiency, thus increased the syntrophic con-
version of alcohols and VFAs to CH4 in the activated carbon-added
methanogenic phase [222]. The latest research shows that the potential
mechanism of DIET includes two aspects: one is to resist acidic shock in
the presence of propionate and butyrate accumulation. The other is to
change the electron transfer pathway to promote methane production
[174].
The EC of the biochar-amended reactor can strengthen the electron
transfer and IET mechanism from electron donors to acceptors [71]. EC
is proportional to the ionic concentration in AD digester, and its mea-
surement can be used to estimate the concentration of VFAs, cations,
and total alkalinity [223]. The EC values of the biochar-amended AD
were 9.97–28.20 mS cm−1, as reported previously [224]. The EC of
Substance of electron transport Ref.
Pilus-like appendages [229]
Electrically conductive pili [192]
Pili, GAC, biochar [192,221,230]
Carbon cloth [231]
Cytochrome c [201]
Fe [207]
Magnetite particle (Fe3O4) [194]
Fe3O4 nano-particles [214]
Conductive iron oxides [213]
Conductive iron oxides [213]

Table 6
The summary of review articles on the application of biochar in AD published in recent years.
Review articles title
A review of biochar properties and their roles in
mitigating challenges with anaerobic
digestion
Insights into biochar and hydrochar production
and applications: A review
Application of nano-structured materials in
anaerobic digestion: Current status and
perspectives
Biochar characteristics and early applications in
anaerobic digestion-a review
Improving the stability and efficiency of anaerobic
9
digestion of food waste using additives: A
critical review
Biochar characteristics and early applications in
anaerobic digestion-a review
Recent achievements in enhancing anaerobic
digestion with carbon-based functional
materials
Direct interspecies electron transfer via conductive
materials: A perspective for anaerobic
digestion applications
The challenges of anaerobic digestion and the role
of biochar in optimizing anaerobic digestion
Advances towards understanding and engineering
direct interspecies electron transfer in
anaerobic digestion
Use of biochars in anaerobic digestion
Published The important point of views
years
2019 Conventional management methods
for AD have their limitations.
2019 Biochar has enormous potential for
energy and environmental demands
2019 Nanomaterial used in the biogas
process were classified and fully
discussed.
2018 Biochar characterization
2018 Poor system stability and low reactor
efficiency are in the AD of food waste
2018 Biochar characterization
2018 Carbon supplementation improves AD
performance.
2018 DIET via conductive materials is a
promising technology for AD.
2017 Acclimation of microbial cells to
substrate inhibition.
2017 Fundamental and engineering aspects
of DIET in AD were reviewed.
2014 Pyrolytic biochar can mitigate mild
ammonia inhibition.
Biochar can potentially improve the
performance of AD.
Formation, properties, and
applications of biochar/hydrochar.
Effect of nanomaterials on the biogas
process.
Biochar in AD: case studies
Additives for AD of food waste are
reviewed regarding system stability
and efficiency.
Biochar in AD: case studies
Carbons favor microbial activity and
electron transfer among anaerobes.
Critical reviews on the current
understanding of DIET were
conducted.
Mechanisms of biochar adsorption and
desorption.
Performances of various conductive
materials in engineering DIET were
summarized.
Hydrothermal biochar can serve as
feedstock for anaerobic digestion.
L. Qiu, et al.
Ref.
Biochar can promote digester stability Biochar can improve digestate [64]
and methane concentration in biogas. agronomic properties and reduce
GHG emissions.
The mechanisms of biochar/hydrochar Biochar applications in energy, [233]
generation. waste management, and agriculture.
Usage of multi-functional [234]
nanomaterials in the biogas process is a
promising area.
[235]
Perspectives for future study on the Co-digestion of food waste and [174]
application of economical additives are landfill leachate in high rate reactors
discussed. is proposed.
[235]
Carbons facilitate microbial Carbons may raise biogas quality. [236]
immobilization and metabolism.
Relevant studies published to date were Future perspectives for practical [237]
systematically analyzed. applications are proposed.
Impact of biochar on AD. [62]
[195]
Biochars support formation of a A simple syringe-based fermentation [112]
methanogenic microflora. technique for biochar analyses is
described.
Renewable and Sustainable Energy Reviews 115 (2019) 109373
L. Qiu, et al.
biochar was positively correlated with its fused-ring aromatic structures
and aromatic groups [225]. Because of the high degree of aromaticity of
gasification biochar [226], the biochar-amended AD showed a re-
markably higher EC than that of AD without biochar. Although the
conductivity of biochar was 1000 fold less than that of granular acti-
vated carbon (GAC) [195], biochar had the active redox property
[170]. Thus, DIET would occur, when the butyrate-oxidizing bacteria
oxidized butyrate to acetate, where biochar acted as the temporary
electron acceptor because of the metabolic inactivity of methanogenic
archaea [170]. The EC of biochar is extremely weak, but it is enough to
improve the metabolic rate of ethanol by promoting IET [221]. How-
ever, it was found that biochar can reduce the CH4 release from the soil
into the atmosphere [227], which does not contradict with the current
research. Biochar, as a complex material, can regulate the environment
by other properties besides EC [221].
At present, the specific strains involved in IET process in biochar
mediated anaerobic environment are unclear. There is a lack of micro-
mechanism cognition and the electrons absorption by methanogens
archaea, which are provided by extracellular organisms and non-living
organisms [228]. Furthermore, the direction of electron transfer be-
tween Geobacter sp. and Methanogenic archaea needs to be illustrated
in the syntrophic-methanogenic associations. Therefore, it is usually
indirectly verified whether the IET mechanism exists or not in a cor-
responding syntrophic system by adding biochar [221].
In conclusion, biochar can be used as a carrier material for micro-
bial growth, breeding, and metabolism. Research on the IET mechanism
in biochar mediated AD has an important technological significance,
which can realize the quality improvement and efficiency enhancement
of AD. It has a great practical significance for the utilization of agri-
cultural and forest waste and the efficient exploitation of ecology re-
sources.
Many literatures have shown that biochar-mediated AD can sig-
nificantly promote methanogenic efficiency. In recent years, there were
many review articles have been published about the application of
biochar in AD. Table 6 summarizes the influential review articles about
biochar application in AD that have been published recently.
However, the environmental benefits of using biochar are rarely
confirmed, and adoption has been slow, which raises the question of
how to align environmental benefits with business motivation to drive
more comprehensive implementation. Therefore, government policies
can play an important role in accelerating commercial-scale production
and application [232]. Here are three policies suggestions for pro-
moting the large scale industrial application of biochar: The first one is
scientific research and development support, which can provide the
necessary foundation for early innovation and it may become a com-
mercially feasible option in the future. The second suggestion is non-
financial policy support; it is crucial mechanism to nurture consumers
and expand market demand. The last suggestion is commercial financial
incentives, which can stimulate application adjustments timely to adapt
to instant changes in business practices.
5. Practical implications of this study
The DIET mechanism is an efficient electron transfer pathway
compared to interspecies hydrogen transfer, but rarely used in AD
systems to deal with complex organic matter. Its mechanism of influ-
ence on AD is not yet clear and requires in-depth research. At the same
time, biochar is a high-quality functional material as it has a wide range
of sources, and even can be obtained from biogas residue without ad-
ditional investment. Functional groups in biochar can be used as elec-
tric shuttles which are as important as conductivity (pili) and require
further research. The application of biochar for AD of carbon-rich
materials is still scarce compared to nitrogen-rich materials. In the fu-
ture, special attention should be directed toward the application of
biochar in AD with carbon-rich materials and the related mechanism of
overcoming VFAs inhibition.
10
Renewable and Sustainable Energy Reviews 115 (2019) 109373
For future research, biochar can be combined with microorganisms
in the form of biochar-microbial polymer in the AD system. The me-
chanism of inhibition and efficiency enhancement by the biochar-mi-
crobial polymer needs to be studied further. Studies on realizing the
local slow-release of inhibitors and improving resistance ability of mi-
croorganisms to environmental changes in AD reactor is thereby
needed. The implementation of this approach has a significant practical
effect on developing harmless organic waste disposal.
However, the relationship between the input cost of biochar pro-
duction and the output benefit of energy production is unclear [174].
The potential economic and environmental benefits associated with the
AD systems should be judged by the life cycle assessment (LCA). The
main product from AD is biogas which is preferential, because, the
energy offset by displacing conventional fossil fuels generally plays a
dominant role in the system's overall carbon abatement capacity fol-
lowed by the carbon sequestration by biochar [238]. Energy input-
output LCA method can be used to calculate the energy associated with
each cost components during the AD process, and estimate the total
energy input for biogas production and the actual energy return on
investment. In this way, a more efficient methane production me-
chanism can be established in future industrial application. Chris-
tiansen et al. (2018) introduced a platform to estimate the costs, input-
output energy analysis, and energy returns on investment of conven-
tional and emerging biofuels feedstocks [239]. This new research model
should be promoted and applied in AD field in the future.
6. Conclusions
Biochar applied in AD process plays different roles. Four important
aspects are: promoting rate-limiting hydrolysis, maintaining a stable
pH, providing the environment for microbial growth, and promoting
DIET mechanism. These factors can address the inevitable obstacles and
optimization pathways to ensure that the AD system remains stable and
efficient with excellent energy conversion rates. This work reviewed the
application of biochar in AD process and its effect on the biogas pro-
duction, the metabolic mechanism of intermediate products from the
aspects of ammonia and acid accumulation, DIET mechanism, and bio-
enrichment of the microbial community. The biochar approach pro-
vides an effective way to enhance AD efficiency by improving the
biogas production and methane content, adsorbing inhibitors, colo-
nizing microbes selectively, alleviating inhibition of ammonia and
VFAs, and maintaining process stability.
Acknowledgments
This work was supported by the Program of the National Natural
Science Foundation of China (51576167); and the Laboratory Research
Fund for Jiangsu Key Laboratory for Biomass-based Energy and Enzyme
Technology (BEETKC1805).
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