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Environmental Technology, 2013

Vol. 34, Nos. 13–14, 2105–2112, http://dx.doi.org/10.1080/09593330.2013.808675

The effect of solids retention time on dissolved methane concentration in anaerobic membrane
bioreactors
Hyeongu Yeo and Hyung-Sool Lee∗
Department of Civil and Environmental Engineering, University of Waterloo, Waterloo, Ontario, Canada
(Received 28 March 2013; final version received 21 May 2013 )

We assessed the effect of solids retention times (SRT) on dissolved methane concentration in a lab-scale anaerobic membrane
bioreactor (AnMBR) operated at SRT 20d and 40d at ambient temperature (23 ± 1◦ C). Daily methane production was
196 ± 17 mL/d and 285 ± 18 mL/d for SRT 20d and 40d, respectively. In comparison, the average concentration of dissolved
methane in AnMBR permeates was 9.9 ± 2.3 mg/L for SRT 20d (close to thermodynamic equilibrium), which was decreased
to 4.3 ± 0.3 mg/L for SRT 40d. We often found oversaturation of dissolved methane at SRT 20d, which means that mass
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transfer of dissolved methane from liquid to gas phase is dynamic at this short SRT. However, we never detected oversaturation
of dissolved methane at SRT 40d, due to slow endogenous decay kinetics. Higher daily methane production at SRT 40d than
that at SRT 20d indicates that methane was supplementarily produced from biomass electrons by endogenous decay. This
study shows that operation of AnMBRs under long SRT can keep low dissolved methane concentration in AnMBR permeate,
along with high methane yield.
Keywords: dissolved methane; endogenous decay; anaerobic membrane bioreactor; solids retention time; thermodynamic
equilibrium

1. Introduction up to a few hundred days,[5–8] and hence sludge dis-


Energy-recovering wastewater treatment technologies are posal costs can be reduced substantially. Finally, AnMBRs
the future direction that our society should pursue to produce methane gas from the wastewater, which can be
improve sustainability in wastewater management. Anaer- reused for heat energy. For these reasons, AnMBRs can
obic digestion (AD) is a mature biotechnology that allows transform energy-consuming WWTPs into energy-neutral
us to capture methane gas from organic wastes and wastew- or -positive bioprocesses. However, AnMBRs face two
aters, simultaneously with stabilization, which has been challenges to be addressed for successful application to
widely used for high strength industrial and agricultural domestic wastewater treatment. One is nutrient control, and
wastes and wastewaters.[1] To increase the impact of the other is dissolved methane. Conventional or advanced
AD on sustainable wastewater management we need to nitrification and denitrification (e.g. anammox, autotrophic
expand its application to municipal wastewater treatment denitrification using hydrogen gas/elemental sulphur as
where significant energy and materials have been spent. electron donor, etc.) can remove ammonium nitrogen,
For instance, annual operating and maintenance costs in the dominant nitrogen species in AnMBR permeates, to
municipal wastewater treatment plants (WWTPs) are $1.9 nitrogen gas.[9–12] Coagulant addition to AnMBRs can
billion approximately in Canada.[2] Unfortunately, domes- easily remove phosphorus.[13] In contrast, there is lim-
tic wastewater treatment using AD is quite challenging ited information on dissolved methane fate and control in
due to relatively poor effluent quality and large footprint AnMBRs.
requirement. To overcome these challenges a membrane Recent literatures commonly found dissolved methane
was integrated with AD, called anaerobic membrane biore- in AD effluents or AnMBR permeates,[6,14–20] which
actors (AnMBRs). Due to separation of colloidal and ranges from 8.5 to 28 mg CH4 /L (equivalent to 34–112 mg
suspended particles through the membrane in hydraulic COD/L). Different operating conditions in bioreactors can
retention time (HRT) close to existing aerobic systems vary dissolved methane concentration, such as tempera-
(e.g. activated sludge), the quality of permeates from ture; it is reasonable to observe high dissolved methane
AnMBRs is significantly improved up to 99% removal concentration at low temperature,[16,20] but some litera-
of chemical oxygen demand (COD) and undetectable tures still found high dissolved methane concentration of
suspended solids.[3,4] In addition, membrane separation 22–28 mg CH4 /L at 25–35◦ C.[17,18] Gimenez et al.[19]
allows AnMBRs to keep long solids retention time (SRT) even reported higher dissolved methane concentration at

∗ Corresponding author. Email: hyungsool@uwaterloo.ca

© 2013 Taylor & Francis


2106 H. Yeo and H.-S. Lee

33◦ C than that at 20◦ C. These results indicate mass trans- methane in the AnMBR. Finally, electron balances were
fer limitation of liquid to gas phase for dissolved methane established for the two SRTs, and assessed the implication
in anaerobic bioreactors. Pauss et al.[21] reported that of dissolved methane in AnMBRs.
dissolved methane could be concentrated by a factor of
10–12 over thermodynamic equilibrium in AD because
2. Materials and methods
of substantial limitation of liquid to gas mass transfer for
dissolved methane. In fact, methane molecules produced 2.1. AnMBR setup and operation
by methanogens are dissolved forms in liquid medium or Figure 1 describes a lab-scale AnMBR used for experi-
wastewater until the methane molecules are released to gas ments. The AnMBR is a cylinder type (ID 10.2 cm and
phase (headspace in bioreactors). Advection can limit mass H 70.0 cm) with a total volume of 5.72 L, and equipped
transport of dissolved methane to gas phase, like insuffi- with a submerged ultrafiltration membrane module (Zee-
cient mixing conditions in some AD systems (e.g. upflow Weed®, GE Water and Process Technologies, Canada); the
anaerobic sludge blanket) where liquid velocity is relatively surface area of the module is 0.047 m2 and the average pore
slow without significant mechanical mixing. However, size of membrane is 0.04 μm. We inoculated the AnMBR
oversaturated methane concentration was found in com- with AD sludge (2 L) sampled from an anaerobic digester
pletely mixing AnMBRs using intensive liquid or biogas that had been operated over a year with glucose medium.
circulation.[18,20] Oversaturation of dissolved methane in After sludge transfer, we fed glucose medium (3 L) into
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anaerobic bioreactors implies that the mass transfer rate the AnMBR, and sparged it for 20 min with nitrogen gas
of dissolved methane from liquid to gas phase would be (99%, PraxAir, Canada). We operated the AnMBR in batch
rate-limiting. mode until permeate COD and biogas production rate were
Recent studies attempted to mitigate dissolved methane constant.
concentration in AnMBR permeates or AD effluents, which To maintain relatively high concentrations of VFAs
includes aerobic methanotrophic oxidation, collection of and COD in the permeate of the AnMBR, we inten-
the methane using gas permeable membrane, or post- tionally operated the AnMBR at a long HRT of 10d
treatment of AnMBR permeate by aeration [16,22,23]; and COD feed of 5300 mg/L (glucose 5 g/L); we had
Hatamoto et al. [22] reported removal efficiency of dis- found high VFAs accumulated under this operation mode
solved methane up to 95%. However, it is questionable in a preliminary study. At the constant organic load-
to add post-treatment processes into AnMBRs because of ing rate we changed SRT into 20d and 40d in the
supplemental costs in construction, operation, and main- AnMBR. We controlled feed and permeate rates with peri-
tenance. Economic and energy benefits in AnMBRs will staltic pumps (Masterflex Economy Drive, Cole-Parmer,
be traded off or be negative because of energy and mate- USA) and a programmable timer (RCT100, Garrison,
rial inputs in post-treatment processes. To minimize dis- Canada). We monitored membrane flux with a balance
solved methane concentration with optimization of oper- (New Classic MS Top-Loading Precision Balance, Met-
ating parameters in AnMBRs will be simpler and more tler Toledo, Switzerland) connected to a desktop computer,
attractive. One of the most important, and easily con- and collected data with Microsoft Excel 2010. The pH
trolled operating factors is SRT in AnMBRs, as com- and temperature in the AnMBR were monitored with a
pared to temperature, mixing conditions, HRT, or organic pH probe (PHE-1411, Omega, Canada) and a compact
loading rate.[1,8] SRT significantly affects the substrate- industrial resistance temperature detector probe (Oakton
utilization rate (the utilization rate for acetate or dis- Instruments, Vernon Hills, IL) inserted in the AnMBR.
solved hydrogen gas for methanogens) in AnMBRs, since Glucose was used as primary electron and carbon source
endogenous decay term becomes significant with increas- (glucose concentrations 5 g/L equivalent to 5300 mg/L
ing SRT. High concentration of hydrolysing/fermenting COD). Chemical composition of medium (in mg/L) is
bacteria at long SRT can decrease the concentration of NH4 Cl 170; NaH2 PO4 37; MgCl2 ·4H2 O 9; KCl 25; and
substrates for methanogens, which reduces the substrate- 1 ml/L of a trace element solution containing (in mg/L)
utilization rate for methanogens (i.e. methane production H3 BO3 50; FeCl2 ·4H2 O 2000; ZnCl2 50; MnCl2 ·4H2 O
rate), and hence dissolved methane concentration can be 500; CuCl2 ·2H2 O 30; (NH4 )6MoO7 ·4H2 O 90; NiCl2 ·6H2 O
varied. Despite of SRT significance in dissolved methane 50; Na2 SeO3 ·5H2 O 100; EDTA 1000; and 1 ml/L of
concentration there are no studies on the relationship 36% HCl. In addition, sodium bicarbonate (4 g/L) and
between SRT and dissolved methane concentration in potassium bicarbonate (4 g/L) were added to maintain
AnMBRs. neutral pH.
This study was carried out to evaluate SRT effect on We operated the AnMBR at a temperature of 23 ± 1◦ C,
dissolved methane concentration in a completely mixing and kept intensive mixing conditions with circulation of
AnMBR operated under two SRT conditions of 20d and biogas and liquid in the reactor. Using a peristaltic pump
40d. First, we compared biomass concentration and perme- (Masterflex Economy Drive, Cole-Parmer, USA) we cir-
ate qualities (volatile fatty acids (VFAs) and COD). Second, culated biogas at a flow rate of 790 ± 70 mL/min from
we regularly quantified the concentration of dissolved the headspace to the bottom of the membrane module
Environmental Technology 2107
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Figure 1. Schematic diagram of the AnMBR used in experiments.

system in which a gas diffuser was installed. This biogas filtrated with syringe filter (Hydrophilic PTFE Syringe
circulation can also mitigate biomass deposition on the Filters; 0.2 μm, Cole-Parmer, Canada) before analysis. We
membrane surface (biofouling). Mixed liquor was recircu- measured VFAs in quadruplicate.
lated at a constant flow rate of 1.60 ± 0.05 L/min with a We quantified biogas compositions with a GC equipped
peristaltic pump (Masterflex Economy Drive, Cole-Parmer, with a thermal conductivity detector (TCD) (SRI 310C
USA). GC-TCD, SRI Instruments, USA). A packed column
(PorapakQ, 6 ft × 1/8 inches, 80/100 mesh, Agilent Tech.,
USA) was used for gas separation in the GC. Helium
2.2. Analysis (99.999%, PraxAir, Canada) was used as a carrier gas with
The concentrations of COD in feed and permeate, mixed a flow rate of 10 mL/min under a pressure of 21 psi. The
liquor suspended solids (MLSS) and mixed liquor volatile temperatures of the column oven and the detector were kept
suspended solids (MLVSS) were measured with the Stan- at 31◦ C and 200◦ C, respectively.
dard Methods.[24] The concentration of dissolved methane in effluent
We quantified VFAs in feed and permeate using a gas was quantified according to the modified methodology
chromatography (GC) (Hewlett Packard HP 5890 Series II) suggested by Kampbell and Vandegrift (1998).[25] We
equipped with flame ionization detector and Nukol fused- transferred 10 mL of permeate to vials (20 mL) which
silica capillary column (15 m × 0.53 mm, Sigma-Aldrich were already sparged with helium gas (99.999%, PraxAir,
Co. LLC). The initial temperature of the GC column was Canada) for 20 min to keep anaerobic conditions. During
set at 110◦ C and increased to 195◦ C at a temperature gra- sample transfer to the vials we maintained atmosphere pres-
dient of 8◦ C/min. The temperatures of an injector and the sure in the vials by releasing vial pressure to a small water
detector were 220◦ C and 280 ◦ C, respectively. Injection vol- bottle (160 mL) connected with a needle. We then placed
ume of samples was 1 μL and helium (99.999%, PraxAir, the vials in an incubation shaker (VWR Incubating Orbital
Canada) was used as a carrier gas at a constant pressure of Shaker, VWR International Inc., Canada) for a day to allow
40psi. We built calibration curves with a standard solution equilibrium between headspace and liquid phase at 37◦ C
(Sigma-Aldrich, PN 46975-U, Canada) at every measure- and 170 rpm. After equilibrium we injected headspace gas
ment. Samples were acidified with concentrated phosphoric from the vials to the GC-TCD using a gastight syringe
acid (PX0996-6, HPLC grade, EM Science, USA) and (Hamilton Gastight High-Performance Syringe, Hamilton,
2108 H. Yeo and H.-S. Lee

USA). The concentrations of dissolved methane in permeate 3. Results and discussion


were calculated by Equation (1). 3.1. Biomass concentration, VFAs, and COD
concentration
CH4 (aq) Average MLSS concentration was 1250 ± 10 mg/L at SRT
  20d, which was decreased to 867 ± 82 mg/L at 40d, respec-
1000 mg
= CCH4 × P × KCH4 × MWCH4 × tively. MLVSS concentrations showed the same pattern
1g
  (935 ± 85 mg/L at 20d SRT and 708 ± 26 mg/L at 40d
1000 mg SRT). In theory, biomass concentration decreases with
+ CCH4 × Vhead × MWCH4 × × T0
1g increasing SRT in chemostat when growth rates are slower
1 than endogenous decay rates.[26] However, opposite phe-
× , nomena are often observed in literatures showing the
(Vhead × (22.4 L/1 mol) × (1000 mL/1 L) × T1 )
(1) increase of biomass concentration with SRT increase.[8,27]
These results can occur when growth rates are faster than
endogenous decay rates (typically at high organic loading
where CH4 (aq) is the concentration of dissolved methane rate and short HRT). Non-biodegradable or inert particulate
in AnMBR permeate (mg/L), CCH4 is the CH4 percent- matters in wastewaters can be accumulated in AnMBRs,
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age in headspace of vial, P is the pressure (1 atm), KCH4 which can show the increase of biomass concentration
is the Henry’s law constant at 37◦ C (0.0014 mol/L-atm), (expressed as MLSS or MLVSS) with increasing SRT.[27]
MWCH4 is the molecular weight of CH4 (16 g/mol), Vhead We, however, observed the reduction of biomass concen-
is the headspace volume of vial (10 mL), T0 = 273.15 K, tration with SRT increase from 20 to 40d in organic loading
and T1 = 310.15 K. rate 0.52 kg/m3 -d (measured feed COD 5216 ± 124 mg/L
and HRT 10d). This decreasing trend of biomass concentra-
tion to SRT increase indicates that endogenous decay term
2.3. COD (electrons) balance in the AnMBR becomes significant at SRT 40d, as compared to SRT 20d.
We established COD balances in the AnMBR run at SRT Figure 3 shows that propionate was dominant at VFAs
20d and 40d. Figure 2 illustrates COD input and output accumulated in AnMBR permeates for both SRT 20d and
parameters in the AnMBR. Output COD terms consist of 40d. Propionate concentration was 2530 ± 110 mg/L and
(1) permeate COD, (2) COD of liquid in wasting sludge, 1310 ± 270 mg/L, respectively, for SRT 20d and 40d.
(3) biomass growth, (4) methane gas, and (5) dissolved Acetate, the second largest VFAs, was 360 ± 80 mg/L
methane. We computed COD of biomass growth using and 530 ± 140 mg/L for the two SRTs; other soluble
the mass of sludge withdrawn daily from the AnMBR, products (e.g. butyrate, pentanoate, etc.) were trivial. The
given that MLVSS concentration represents biomass con- average COD concentration in AnMBR permeates was
centration and the chemical formula of microorganisms 2920 ± 200 mg/L at SRT 20d, which was 2940 ± 40 mg/L
is C5 H7 O2 N (113 g VSS = 160 g COD).[26] COD of at SRT 40d. Similar COD concentration, but smaller VFAs
methane gas is computed with a half reaction for methane (propionate) at SRT 40d indicates accumulation of sol-
to carbon dioxide and measured volumes of methane gas uble microbial products (SMPs), which is consistent to
(1 mol CH4 = 64 g COD). We computed COD of dissolved low biomass concentration at SRT 40d. SMPs (especially
methane in permeate, liquid in wasting sludge, and liquid biomass-associated products) accumulation becomes sig-
in the AnMBR. nificant at long SRT, as a consequence of endogenous
decay,[26] resulting in low biomass concentration and high
SMP.[28,29] Dissolved methane can contribute to COD
concentration, but the concentration of dissolved methane
at SRT 40d was lower than that at SRT 20d (discussed later).
During experiments pH in AnMBR permeates was kept at
7.3–7.5.

3.2. Dissolved methane concentrations


Methane gas production was 196 ± 17 mL/d and 285 ±
18 mL/d (0.042 ± 0.004 L/g VSS-d and 0.081 ± 0.005 L/g
VSS-d), respectively, for SRT 20d and 40d. Methane
percentages of biogas were relatively low at 35 ± 2%
to 41 ± 3% in the AnMBR. Figure 4 shows dissolved
Figure 2. Schematic diagram of electron distributions in the methane concentration in the AnMBR. Average dissolved
AnMBR. methane concentration was 9.9 ± 2.3 mg/L in SRT 20d,
Environmental Technology 2109

of dissolved methane clearly shows that the formation rate


of dissolved methane by methanogens would be faster than
the transfer rate of dissolved methane from liquid to gas
phase even in intensive mixing conditions in one hand. In
the other hand, the fluctuation of dissolved methane at SRT
20d indicates dynamic behaviours of dissolved methane
(non-equilibrium of methane between liquid and gas phase)
kept in the AnMBR even under intensive mixing (biogas cir-
culation rate 790 ± 70 mL/min and liquid circulation rate
1.60 ± 0.05 L/min).
Equilibrium concentration of dissolved methane in SRT
40d was computed at 10.8 ± 0.8 mg/L, which is slightly
higher than that at SRT 20d, due to high methane percent-
age in biogas (41% in SRT 40d vs. 35% in SRT 20d).
Interestingly, the measured average of dissolved methane
Figure 3. Concentrations of VFAs in AnMBR permeates. concentration was as low as 4.3 ± 0.3 mg/L at SRT 40d,
and we never detected dissolved methane concentration
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over the equilibrium concentration (Figure 4(b)). This


which was substantially decreased at 4.3 ± 0.3 mg/L in low concentration of dissolved methane at SRT 40d indi-
SRT 40d. The pressure inside of the AnMBR was stable cates that the production rate of dissolved methane by
at 1.03 atm (absolute pressure) for the two SRTs. Using methanogens is much slower than the mass transfer rate
the measured pressure inside the AnMBR, the equilib- of dissolved methane from liquid to gas phase. The con-
rium concentrations of dissolved methane were computed at centration of dissolved methane less than thermodynamic
9.3 ± 0.5 mg/L and 10.8 ± 0.8 mg/L, respectively, for the equilibrium at SRT 40d also implies methane gas trans-
two SRTs (Henry’s law constant of methane 0.0016 mol/L- fer from gas to liquid phase is dominant over reciprocal
atm at 25◦ C). Intensive mixing conditions with biogas and methane transfer from liquid to gas. However, our result
liquid circulation allowed dissolved methane concentration indirectly supports that methane transfer rate from gas to
close to thermodynamic equilibrium under SRT 20d, but liquid would be slow enough for methane gas to release to
we also found oversaturation of dissolved methane (8 over- atmosphere in the AnMBR.
saturated concentrations of 20 measurements); dissolved In comparison, we found daily methane production
methane concentration was increased up to 16.9 mg/L. The rate at SRT 40d (285 ± 18 mL/d) higher than that at SRT
oversaturated dissolved methane in anaerobic bioreactors 20d (196 ± 17 mL/d). These results firstly indicate that
was found in literatures.[17,20,30] Pauss et al.[21] reported the production rate of dissolved methane at SRT 40d
that dissolved methane concentration could be 10–12 times was steadily slower than that at SRT 20d (low dissolved
higher than thermodynamic equilibrium concentration even methane kept at SRT 40d). Secondly, more methane gener-
in a completely mixing anaerobic digester. Oversaturation ation via endogenous decay (electron flow from biomass to

Figure 4. Dissolved methane concentrations in the AnMBR operated under (a) SRT 20d and (b) 40d. The blue line indicates
thermodynamic equilibrium concentration of dissolved methane in the AnMBR for SRT 20d and 40d. (colour online only)
2110 H. Yeo and H.-S. Lee
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Figure 5. COD balances in the AnMBR for (a) SRT 20d and (b) 40d.

methane molecules) at SRT 40d can improve daily methane 3.3. COD balance
production (pseudo methane yield). However, the produc- We established COD (electron) balances in the AnMBR,
tion rate of dissolved methane by substrate utilization and as shown in Figure 5. COD balances were well closed, pre-
endogenous decay would be slower than the mass trans- senting unknown fractions from 3% to 7% for both SRTs. In
fer rate of liquid to gas for dissolved methane at SRT 40d, SRT 20d the COD in AnMBR permeate and liquid in wast-
which allowed dissolved methane concentration less than ing sludge was 1461 mg COD/d (56% of the input COD).
equilibrium concentration under intensive mixing condi- The second largest electron sink was methane gas (517 mg
tions. Two parameters would mainly affect the production COD/d, 20% of the input COD), followed by biomass
rate of dissolved methane based on the Monod equation, growth (331 mg COD/d, 13% of the input COD) and dis-
given that kinetic parameters (half-saturation concentra- solved methane (218 mg COD/d, 8% of the input COD).
tion (Ks ) and maximum specific rate of substrate utilization The COD in AnMBR permeate and liquid in wasting sludge
(qmax )) for fermenters and methanogens would not be var- was still the largest electron sink (1468 mg COD/d, 56%
ied significantly between the two SRT conditions. One key of the input COD) for SRT 40d. Methane gas production
parameter is substrate concentration, and the other is the accounted for 751 mg COD/d (29% of the input COD).
concentration of active methanogens. We found that acetate COD values for biomass growth and dissolved methane
concentration at SRT 40d was slightly higher than that were 125 mg COD/d (5% of the input COD) and 95 mg
at SRT 20d, and thus substrate would not slow down the COD/d (4% of the input COD), respectively. Relatively
production rate of dissolved methane by methanogens at large fraction of biomass growth at SRT 20d would be due
SRT 40d; dissolved hydrogen is another important electron to high portion of carbohydrates and proteins accumulated
donor for methanogens, but methane production by aceto- in extracellular polymeric substances, which was accounted
clastic methanogens is as large as 80% of the total methane for VSS quantification in glucose-fed bioreactors.[31] This
yield. Hence, we analysed substrate effect on the production interpretation well agrees to the decrease of biomass growth
rate of dissolved methane only with acetate substrate. The at SRT 40d (5% of the input COD), as a result of endoge-
other parameter is the concentration of active methanogens, nous decay. Dissolved methane was as high as 8% of the
but quantification of active methanogens as ‘concentration total input COD at SRT 20d, which reduced to 4% of the
unit’ is quite challenging. MLVSS concentration at SRT total COD at SRT 40d.
40d consistently lower than that at SRT 20d would support Given that an industrial wastewater treatment plant
less concentration of active methanogens at SRT 40d, which is operated with AnMBR system (treatment capacity:
can explain slow production rate of dissolved methane at 103 m3 /d and influent COD 5000 mg/L), the AnMBR
SRT 40d. However, more study should be conducted to con- system can release dissolved methane of 153 m3 /d at
firm this interpretation, along with molecular biology data SRT 20d (30, 000 kg COD/d × 0.08 × (1 kmol e− )/8 kg
(e.g. quantitative real-time PCR targeting rRNA or mRNA). COD × 1 kmol CH4 /8 kmol e− × 22.4 m3 /1 kmol CH4 ×
These results clearly support that AnMBRs should be oper- 298 K/273 K = 917 m3 CH4 /d). This dissolved methane
ated at long SRTs to improve methane production yield, but will finally emit to the atmosphere, and annual methane
mitigate dissolved methane concentration in permeates. emission by dissolved methane in AnMBR permeates is as
Environmental Technology 2111

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