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Biochemical Engineering Journal 109 (2016) 96–100

Contents lists available at ScienceDirect

Biochemical Engineering Journal


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

Regular article

Characterization of methanogenic activity during high-solids


anaerobic digestion of sewage sludge
Can Liu a , Huan Li a,∗ , Yuyao Zhang a , Qingwu Chen b
a
Key Laboratory of Microorganism Application and Risk Control of Shenzhen, Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China
b
Guangdong Haoyuan Environmental Technology Company, Shenzhen 518055, China

a r t i c l e i n f o a b s t r a c t

Article history: High-solids anaerobic digestion of sewage sludge has advantages of smaller digesters and a lower energy
Received 2 September 2015 requirement for heating than conventional digestion, but its efficiency is negatively influenced by high
Received in revised form 8 December 2015 solids concentration. To discover the mechanism causing this deteriorative performance, the specific
Accepted 13 January 2016
methanogenic activity (SMA) of high-solids digestate was measured using typical substrates including
Available online 15 January 2016
acetate, propionate, butyrate, glucose, microcrystalline cellulose and hydrogen and carbon dioxide. When
the total solids content increased from 4.2% to 14.4%, the SMA of the digestate decreased 40%–50% for most
Keywords:
substrates except hydrogen and carbon dioxide, mainly because of blocked mass transfer in the high-
Acetic acid
Anaerobic processes
solids digestate. On the other hand, some features remained stable: acetotrophic methanogens exhibited
Biogas more activity than hydrogenotrophic methanogens, butyrate fermentation rather than propionate fer-
Sewage sludge mentation was still the main metabolic pathway during the degradation of glucose and cellulose, and
Specific methanogenic activity hydrolysis was still the rate-limiting step during the anaerobic digestion of cellulose.
Waste treatment © 2016 Elsevier B.V. All rights reserved.

1. Introduction Thus, the digestibility of the sludge having a high viscosity can-
not be deduced exactly from that of other wastes. A few studies
Anaerobic digestion is a widely-used method of sludge treat- have reported that the HSAD of sewage sludge easily suffers from
ment because of its good performance in waste reduction and long digestion time or low biogas production. For example, the time
energy recovery in the form of methane [1,2]. During conventional required to complete digestion extended from 16 days to 46 days
anaerobic digestion, the total solids (TS) content in feed sludge when sludge TS increased from 1.79% to 15.67% [6].
is usually controlled in the range of 2%–5%. Correspondingly, this Three aspects may be involved in the poor performance of HSAD
process needs large digesters, which are not always feasible in of sewage sludge. The first of these reasons is the low water con-
small-scale wastewater treatment plants (WWTPs) or at WWTPs tent in high-solids digestate. Water is essential for biochemical
in highly urbanized areas [3]. In such situations, high-solids anaer- reactions. During anaerobic digestion, water promotes substrate
obic digestion (HSAD) of sewage sludge is often recommended as hydrolysis and enables the transfer of hydrolysis products and other
an alternative because smaller reactor volumes and lower energy intermediates to the sites of bacteria. The lack of free water results
requirements for heating are needed and less material handling is in deteriorated molecular diffusive behavior and corresponding
required [4]. poor transfer efficiencies in high-solids digestate. For example, dur-
High-solids anaerobic digestion has been successfully applied to ing dry fermentation of MSW, the effective diffusion coefficient
a variety of solid wastes such as the organic fraction of municipal decreased drastically when the TS content increased, with numeri-
solid waste (MSW), agricultural wastes and green wastes, whereas cal values 50 to 185 times smaller than the reference value in water
the knowledge on mono-HSAD of sewage sludge is rare. Unlike at 8% TS and 25% TS, respectively [7]. A static batch experiment on
uncompacted wastes, high-solids sludge is a sticky semisolid. In anaerobic digestion at different TS levels also demonstrated that
fact, sewage sludge with 2%–15% TS behaves as a pseudoplastic biogas yield was directly influenced by the decreased water content
fluid and its viscosity increases exponentially as TS increases [5]. [8]. The second reason for poor HSAD performance may be related
to the accumulation of some intermediate products, which result
from blocked mass transfer and high concentration of substrates
∗ Corresponding author at: L205B, Tsinghua Campus, University Town, Shenzhen, [6]. These intermediate products, such as free ammonia and volatile
China. Fax: +86 755 26036105. fatty acids (VFAs), have a negative impact on microorganisms. Sig-
E-mail address: li.huan@sz.tsinghua.edu.cn (H. Li).

http://dx.doi.org/10.1016/j.bej.2016.01.010
1369-703X/© 2016 Elsevier B.V. All rights reserved.
C. Liu et al. / Biochemical Engineering Journal 109 (2016) 96–100 97

Table 1
Main reactions presented in methanogenesis.

Substrate Microbial population Reaction

Acetate Acetoclastic methanogens CH3 COOH → CH4 + CO2


Propionate Propionate degradation bacteria CH3 CH2 COOH + 2H2 O → CH3 COOH + CO2 + 3H2
Butyrate Butyrate degradation bacteria CH3 CH2 CH2 COOH + 2H2 O → 2CH3 COOH + 2H2
Glucose Acidogenic bacteria C6 H12 O6 → CH3 CH2 CH2 COOH + 2CO2 + 2H2
C6 H12 O6 + 2H2 O → 2CH3 COOH + 2CO2 + 4H2
C6 H12 O6 + 2H2 → 2CH3 CH2 COOH + 2H2 O
Cellulose Hydrolytic bacteria (C6 H10 O5 )n + nH2 O → nC6 H12 O6
H2 /CO2 Hydrogenotrophic methanogens CO2 +4H2 → CH4 + 2H2 O
H2 /CO2 Homoacetogenic bacteria 2CO2 + 4H2 → CH3 COOH + 2H2 O

nificant microbial inhibition was found at free ammonia nitrogen biodegradable organic matter and limit endogenous activity [9,10].
(FAN) concentration range of 600–800 mg/L during the operation Thus, the residual VS was mainly comprised of live microorgan-
of a pilot-scale HSAD reactor [3]. A maximum FAN of 968 mg/L was isms. The final composition of the digestate was 14.4% TS with 54.5%
observed in a batch HSAD test of sewage sludge, resulting in a rel- VS/TS for the HSAD tests, and 4.2% TS with 56.9% VS/TS for the LSAD
atively low specific biogas yield [6]. Finally, due to the difficulty in tests.
microorganisms acquiring substrates, as well as the negative effect
of accumulated metabolites, microbial activity may decrease and
2.2. Experimental procedure
result in the deteriorative performance of HSAD. It was found that
the specific methanogenic activity (SMA) decreased linearly with
The frequently-used indicator of microbial activity during
increasing TS content from 18% to 35% during dry fermentation of
anaerobic digestion is specific methanogenic activity, which is cal-
MSW [9].
culated by dividing the maximum methane production rate by
Although some previous studies have verified the phenomena
the biomass (i.e., the inoculum, based on the VS content) during
of blocked mass transfer and accumulative intermediate products,
batch anaerobic digestion experiments using specific substrates
there is still a lack of direct observation of the microbial activity
[11]. SMA values based on different substrates can reveal the activ-
involved in different reaction steps during mono-HSAD of sewage
ities of not only methanogens but also other microflora involved
sludge. Several microbial pathways are related to methanogen-
[9,12,13], and thus, show the metabolic pathways to some extent.
esis, as shown in Table 1. Organic wastes are first hydrolyzed
In this study, the SMA tests were divided into an HSAD series
into glucose, organic acids and other oligomers, and these inter-
and an LSAD series, and each series included eight groups. Each
mediate products are then degraded to VFAs. Finally, methane is
of the first six groups in each series used one of the following
produced from the decomposition of acetic acids or the synthesis
specific substrates: sodium acetate, sodium propionate, sodium
of carbon dioxide and hydrogen. Previous research has reported
butyrate, glucose, microcrystalline cellulose, and hydrogen (H2 )
only the influence of high solids concentration on methanogene-
and carbon dioxide (CO2 ), respectively. Two “blank” groups with-
sis during dry fermentation of MSW [9]. However, during HSAD
out any substrate were also set in each series to eliminate the
of sewage sludge, the efficiency of each step in the complex reac-
probable influence of residual biodegradable organic substances
tion chain, including hydrolysis, fermentation, acetogenesis and
in the inoculum and endogenous activity. Each experiment was
methanogenesis, has been rarely studied so far. Thus, in the present
performed in triplicate in 140-mL glass vials under mesophilic
study, the microbial activities in sludge digestate from HSAD and
temperature condition (35 ± 2 ◦ C). The digestate (inoculum) and
low-solids anaerobic digestion (LSAD) were measured based on dif-
the substrate were mixed well at a 10:1 ratio of inoculum VS to
ferent typical substrates. Using these data, the influences of high
substrate chemical oxygen demand (COD) to ensure sufficient sub-
solids concentration on different reaction steps were analyzed, giv-
strate and prevent inhibition [10]. In the LSAD series, 90 g of mixture
ing insight into the differences and similarities between HSAD and
were added into each vial and the vials were shaken frequently
LSAD.
during the subsequent digestion to ensure homogeneity and facil-
itate the release of biogas. In the HSAD series, 30 g of mixture were
2. Materials and methods smeared on the inner wall of the vials, forming a thin layer to
facilitate the release of biogas. All the vials were flushed with nitro-
2.1. Characterization of digestate gen to remove oxygen, and then immediately sealed with rubber
plugs. The biogas produced was transported through a perfusion
The digestate discharged from two laboratory-scale semi- tube into a fermentation tube that was filled with displacement
continuous anaerobic digesters was used to assess the microbial liquid of a sodium hydroxide solution (3 mol/L) with thymolph-
activity. One digester (HSAD) was fed with dewatered sludge col- thalein pH-indicator, so as to determine the methane production.
lected from a full-scale WWTP in Kunming city, China, which had a For the groups using H2 and CO2 as the substrates, the volume ratio
high TS content of 15.7% and a volatile solids (VS) content of 64.2% of H2 to CO2 was 4:1, and the gas mixture was injected frequently
based on TS. The other digester (LSAD) was fed with the same dewa- into the vials. The discharged gas from the vials was measured by
tered sludge as used in the HSAD digester, except diluted to a TS displacing saturated NaHCO3 solution in fermentation tubes. In the
content of 5.7% and a VS/TS ratio of 63.5%. Both digesters had run blank groups, NaOH solution and NaHCO3 solution were used for
steadily for six months at a temperature of 35 ◦ C and a solids reten- the measurement of methane and biogas, respectively.
tion time of 30 days. The average removal rates of sludge organic There has been no consensus on whether other nutrients and
matter for the HSAD reactor and the LSAD reactor were 35.7% and trace elements have an impact on SMA tests of sludge digestate.
37.2%, respectively, and the specific biogas production per unit VS Thus, several additional groups of experimental vials were added
added for the two digesters averaged 233.0 mL/g and 316.1 mL/g, during preliminary experiments. In these groups, glucose was also
respectively. used as the substrate, but with supplementary growth factors
The digestate collected from the two digesters was first [10,14] in the form of concentrated solution (Table 2). The methane
stored anaerobically at 35 ◦ C for several days to remove residual production from glucose alone and from the mixture of glucose, the
98 C. Liu et al. / Biochemical Engineering Journal 109 (2016) 96–100

nutrients and the trace elements were almost the same, indicating
that the supplementary growth factors were an unnecessary addi-
tion for the SMA test of sludge digestate. Therefore, added nutrients
and trace elements were not used in the remainder of the study.
The modified Gompertz equation Eq. (1) was used to estimate
the main experimental parameters for each group [13].
 R ×e

max
Pnet (t) = Pmax × exp −exp × ( − t) + 1 (1)
Pmax
In Eq. (1), Pnet (t) is the net accumulative methane production
per gram inoculum VS (mL/g) at time t, Pmax is the methane produc-
tion potential per gram inoculum VS (mL/g), Rmax is the maximum
methane production per gram inoculum VS per hour [mL/(g·h)], 
is the lag phase time (h) and e is the natural exponential constant.
For the groups using the solid substrates, Pnet (t) was calculated
by subtracting the average methane production of the inoculum
at time t from the methane production of these groups. For the
groups using H2 and CO2 as the substrates, Pnet (t) was one quar-
ter of the decrement in the total gas volume, based on the reaction
equation (Table 1). The values of Pmax , Rmax and  were calculated
by fitting Eq. (1) to the experimental data (Pnet and t). The value
of SMA [mL/(g d)] was directly converted by multiplying Rmax by
a fixed coefficient of 24. To facilitate showing the total fermenta-
tion period, a parameter of T95 was defined as the time required for
methane production to reach 95% of Pmax .

2.3. Analytical methods

The physical and chemical parameters TS, VS, pH and COD were
determined according to standard methods [15].

3. Results and discussion

All accumulated methane production curves (after correction


using the methane production from the blank groups) are shown
in Fig. 1. The simulated curves produced using Eq. (1) fit the mea-
sured values well, and the calculated parameters are shown in
Table 3.In the LSAD series and the HSAD series, the actual accumu- Fig. 1. Accumulative methane production from different substrates in the low-
lative methane production from acetate, propionate and butyrate solids anaerobic digestion (LSAD) tests (a) and the high-solids anaerobic digestion
were all close (Fig. 1), though the calculated Pmax from propionate in (HSAD) tests (b).
the LSAD tests was a little higher than that for the other substrates.
These substrates were transformed into biogas in the same degree
when the digestion time was long enough. According to the ratio the theoretical values. The accumulative methane production from
of inoculum VS to substrate COD (10:1) and the reaction equations glucose and microcrystalline cellulose were relatively low because
(Table 2), the theoretical methane yield should have been 35 mL the chemical energy related to the lost methane may be stored in
per gram inoculum VS if all the substrates had been converted into some other products during the complex degradation processes
biogas. However, when using propionate or butyrate as the sub- of glucose and cellulose. When H2 and CO2 were used as the sub-
strate, a small quantity of the generated H2 may have been released strates, the acquired substrates by hydrogenotrophic methanogens
from the vials to the biogas collection device and not further con- in sludge digestate were restricted by the difficult gas-liquid mass
verted into biogas. Thus, the actual yields were a little lower than transfer. Thus, the methane production was also low.
Although HSAD tests exhibited similar Pmax with the LSAD tests,
the digestion time (T95 ) nearly doubled and the lag phase () also
Table 2
increased several times in the HSAD tests, except when H2 and CO2
Composition of growth factors (nutrients and trace elements).
were used as the substrates (Table 3). This verified that the reac-
Components Concentration tion rate in high-solids digestate indeed was slower than that for
Nutrients LSAD. Because acetate and hydrogen can be utilized directly for
NH4 Cl (g/L) 26.60 methanogenesis, the lag times in these groups were very short.
KH2 PO4 (g/L) 10.00 The lag time was also short for butyrate and glucose, because
MgCl2 ·6H2 O (g/L) 6.00
these substrates are readily degradable and the hydrogen pro-
CaCl2 (g/L) 2.27
duced at the beginning of their degradation could be captured and
Trace elements recorded by the measurement device. Propionate and cellulose had
FeCl2 ·4H2 O (mg/L) 2.00
CoCl2 ·6H2 O (mg/L) 0.49
the longest digestion time and lag phase owing to their relatively
MnCl2 ·4H2 O (mg/L) 0.10 poor biodegradability. The long lag phase of propionate and the
NiSO4 ·6H2 O (mg/L) 0.11 short lag phase of glucose reflected that butyric fermentation rather
ZnCl2 (mg/L) 0.05 than propionic fermentation should be the dominant metabolic
H3 BO3 (mg/L) 0.05
pathway during the degradation of glucose and cellulose, whether
C. Liu et al. / Biochemical Engineering Journal 109 (2016) 96–100 99

Table 3
Parameters estimated for the modified Gompertz model (mean ± standard deviation).

Substrates Acetate Propionate Butyrate Glucose Cellulose H2 + CO2

LSAD
R2 0.996 0.993 0.997 0.996 0.997 0.999
Pmax (mL/g) 35.24 ± 0.40 44.69 ± 1.07 33.98 ± 0.37 25.78 ± 0.29 27.50 ± 0.55 19.97 ± 4.79
Rmax [mL/(g·h)] 0.79 ± 0.01 0.32 ± 0.00 0.82 ± 0.02 0.72 ± 0.01 0.45 ± 0.01 0.31 ± 0.06
 (h) 6.53 ± 0.06 28.55 ± 0.66 10.43 ± 0.16 5.46 ± 0.02 42.41 ± 0.20 5.73 ± 0.60
T95 (h) 71.39 ± 0.86 230.53 ± 4.80 70.93 ± 1.48 57.85 ± 0.62 131.52 ± 1.29 100.87 ± 11.00

HSAD
R2 0.994 0.998 0.994 0.975 0.994 0.997
Pmax (mL/g) 34.65 ± 5.01 33.55 ± 9.49 33.41 ± 0.38 21.92 ± 3.82 21.56 ± 1.35 18.37 ± 0.43
Rmax [mL/(g·h)] 0.39 ± 0.02 0.11 ± 0.02 0.45 ± 0.01 0.43 ± 0.05 0.21 ± 0.02 0.26 ± 0.01
 (h) 13.99 ± 0.90 117.73 ± 15.84 35.93 ± 0.37 17.53 ± 0.43 157.32 ± 6.80 1.96 ± 1.57
T95 (h) 142.41 ± 13.77 570.80 ± 77.88 145.19 ± 3.62 91.34 ± 4.07 305.46 ± 2.57 105.05 ± 3.10

Furthermore, acetotrophic methanogens had much higher activ-


ity than hydrogenotrophic methanogens whether in the low-solids
digestate or in the high-solids digestate, but the preponderance of
acetotrophic methanogens was reduced in the high-solids diges-
tate according to their relative activities. The results suggested
that acetotrophic methanogens were still the dominant type dur-
ing HSAD, but hydrogenotrophic methanogens could contribute
more to methanogenesis. Previous research [19] verified that the
methane fraction derived from H2 and CO2 increased from 33% to
47% as the organic loading rate increased during a two-stage HSAD,
but the acetoclastic Methanosaeta was still dominant in the anaer-
obic filter. On the other hand, in the present study, the tests using
H2 and CO2 as the substrates showed the lowest reduction rate
(15%). This was because the solids concentration only influenced
the transfer of H2 and CO2 in the digestate, and the influence of
solids concentration on the gas-liquid mass transfer, which was
the rate-limiting step, was negligible.
When propionate was used as the substrate, the digestate exhib-
Fig. 2. Specific methanogenic activity (SMA) of the digestate using different sub- ited the lowest SMA, whereas the digestate with the addition
strates during the low-solids anaerobic digestion (LSAD) tests and the high-solids
of acetate, butyrate or glucose showed high SMA. These results
anaerobic digestion (HSAD) tests, and the reduction in SMA from LSAD to HSAD.
demonstrated that propionate fermentation should not be the
dominant metabolic pathway in either the LSAD tests or in the
in the low-solids or high-solids digestate. The long lag phase of cel- HSAD tests. The relatively low degradation rate of microcrystalline
lulose and the short lag phase of glucose indicated that hydrolysis cellulose suggested that hydrolysis was the rate-limiting step in the
was still the rate-limiting step during the degradation of complex HSAD tests, even though all the steps involved in anaerobic diges-
organic substances. Hydrogen was also consumed slowly, but the tion were retarded due to the increased solids concentration. The
solids concentration in digestate had almost no influence on its tests using acetate, butyrate, glucose and cellulose as the substrates
digestion time. These results demonstrated that gas-liquid mass exhibited similar SMA reductions of approximately 40%–50% when
transfer rather than methanogenesis should be the rate-limiting the solids concentration increased from 4.2% to 14.4%. This meant
step during the conversion from hydrogen to methane. that the chain of reactions was prolonged evenly in the high-solids
The SMA values of the digestate fed with different substrates are digestate. In other words, all the reactions involved in anaerobic
shown in Fig. 2, and ranged from 7.4 mL/(g d) to 19.7 mL/(g d) for digestion—such as the hydrolytic process that was revealed by
the LSAD series and from 2.6 mL/(g d) to 10.7 mL/(g d) for the HSAD the consumption of microcrystalline cellulose; the fermentation
series. These values were lower than those measured previously in by glucose; the acetogenic process by butyrate; and methanogene-
systems with higher water content, which could be 100 mL/(g d) or sis by acetate—were slowed in an equal proportion. Therefore, the
more [16,17]. According to previous reports on dry fermentation decline in microbial activity in the high-solids digestate should be
of MSW, the methanogenic activity based on cellulose and acetate caused mainly by some systemic changes, including blocked mass
decreased almost linearly with the increase of TS content [9,18], transfer and the inhibitors threatening all relevant microorganisms,
such that SMA values deduced in the present study from this linear rather than the change in a certain kind of microflora. Or strictly
relationship were 3.9–12.0 mL/(g d) and 3.1–5.0 mL/(g d) at TS 4% speaking, the influence of probable changes in certain microbes on
and 14%, respectively. These deduced values were comparable to the performance of HSAD was much less than the influence of sys-
(but slightly lower than) the measured data in the present study; temic changes. Considering the low doses of the substrates used in
the slightly higher SMA values found in the present study suggested this study, the inhibition derived from intermediate products could
a relatively higher microbial activity in sludge digestate than in be excluded and the blocked mass transfer should be fundamen-
MSW. tally responsible for the deteriorative performance of HSAD. The
Although microbial activities in the HSAD tests were all weak- transfer of raw substrates, intermediate metabolites and final prod-
ened by high solids concentration in comparison to those in the ucts in digestate is dependent on the availability of water; thus, the
LSAD tests, the extent of reductions in SMA varied according to decreased water content and the corresponding decreased rate of
the different substrates (Fig. 2). Both acetate and hydrogen led to mass transfer in high-solids digestate decides the efficiency of bio-
considerable SMAs, indicating the combined contribution of ace- chemical reactions. This deduction also can be verified from another
totrophic and hydrogenotrophic methanogens to methanogenesis.
100 C. Liu et al. / Biochemical Engineering Journal 109 (2016) 96–100

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