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Article history: The fundamental mechanism behind biosorption to recover carbon from wastewater through high-
Received 17 May 2017 rate activated sludge (HRAS) system is insufciently studied. The most accepted method of quantifying
Received in revised form 5 September 2017 biosorption capacity of activated sludge depends on higher settling velocity solids. As HRAS had different
Accepted 7 September 2017
settling characteristics and in addition, raw wastewater fed to the HRAS system contained approximately
Available online 8 September 2017
55% settleable organics, the conventional biosorption capacity test was not capable of accurately den-
ing biosorption. Thus, we studied ex-situ aerobic yield as an alternative approach for determination of
Keywords:
biosorption in batch systems. However this approach similarly to biosorption capacity was not sensitive
Adsorption
Carbon recovery enough to quantify differences between HRAS types, potentially due to enhanced storage mechanisms
Contact-stabilization under the feast-famine approach. A viable method to determine biosorption in the batch system was
Energy based on measurement of ex-situ oxygen uptake rate (OUR) of HRAS over 40 h and the biosorption yield
Municipal wastewater was considered as the area underneath the OUR curve normalized for solids concentration. In addition,
High-rate activated sludge in-situ based biosorption quantication was proposed in this study based on detailed measurement of
carbon mass balances including contribution of extracellular polymeric substances. A clear relationship
between biosorption yield and in-situ biosorption with carbon mass-balance, carbon redirection and
solids retention time of HRAS systems was observed suggesting two viable methods for quantication of
biosorption.
2017 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.bej.2017.09.006
1369-703X/ 2017 Elsevier B.V. All rights reserved.
34 A. Rahman et al. / Biochemical Engineering Journal 128 (2017) 3344
The biosorption mechanism is a combination of physical- Since the conventional biosorption capacity approach possibly
chemical and biological phenomena in activated sludge, which determines the maximum or saturation carbon capture capacity
includes outer cell surface adsorption of particulate and colloidal of activated sludge, knowing the in-situ biosorption contributions
organic matter and storage of soluble COD (chemical oxygen in HRAS systems is necessary to understand the carbon redirec-
demand) inside the cell [1014]. Biosorption capacity of the tion. Rahman et al. [9] rst proposed a simple approach to quantify
sludge has been mostly quantied in bench scale experiments to biosorption in a batch reactor using the oxygen uptake rate (OUR) of
understand the kinetics of organic matter transformation from the sludge which contained biodegradable organic matter as a form
wastewater to sludge matrix [10,1219]. Riffat and Dague [14] rst of biosorption occurred in a continuous system, and the approach
measured the biosorption capacity on anaerobic granular biomass was referred as biosorption yield. In this study, we evaluated this
mixed with non-fat dry milk (soluble COD) for short contact time approach to quantify biosorption for various HRAS systems at dif-
(230 min) in which COD removal was determined by subtract- ferent SRT conditions to nd the relationship between biosorption
ing the supernatant COD (after settling) from initial COD of carbon yield and inuent carbon balance and other operational parameters
source. The advantage of that test was that the granular sludge gen- (SRT).
erally has higher settling velocity than occulent sludge and thus Although, the conventional biosorption capacity and the
the supernatant was sufciently clear to determine the removal of biosorption yield was focused on ex-situ measurement based
COD. Tan and Chua [18] and Zhang et al. [19] adopted the simi- approach, the biosorption has rarely been investigated on in-situ
lar approach for measuring the biosorption capacity of high mean continuous reactor systems to consider the impact of operational
cell residence time activated sludge (5 days) mixed with settled parameters (SRT, HRT), inuent, efuent, and waste activated
domestic wastewater in a batch system open to the atmosphere. sludge (WAS) characteristics and most importantly the extracellu-
In their study, the oxidation of COD from wastewater in a short lar polymeric substances (EPS) in the reactor. In fact, EPS is the key
contact time was neglected. In addition, the non-settling fraction for the microbial community to grow at high-cell density by attach-
of biomass was also negligible due to the better settleability of ing their surfaces [2325]. Therefore, microorganisms are required
high SRT sludge. Later, Guellil et al. [10] and Lim et al. [12] applied to hold together via EPS production for better bioocculation which
a modied approach of Tan and Chua [18] by centrifuging the caused biosorption of organic matter from wastewater [26]. A novel
supernatant after settling to separate out non-settleable biomass approach was proposed in this study to quantify in-situ biosorption
from wastewater. In this case, the possible soluble COD (sCOD) using operational parameters, inuent carbon balance and EPS of
oxidation or biomass growths were also neglected. However, non- a pilot-scale reactor system treating chemically enhanced primary
settleable particulate matter from wastewater and the adsorption treatment (CEPT) efuent.
of particulate and colloidal matter to the non-settling biomass The main purpose of this study was to evaluate four differ-
cannot be separated out by the centrifugation, thus overestimat- ent approaches of biosorption quantication on HRAS systems and
ing the biosorption capacity. Modin et al. [17] further improved their potential applications, advantages, and limitations in HRAS
the method by separating sCOD oxidation by active and inactive systems. The specic objectives of this study were (a) to quantify
biomass (sodium azide addition) experiment for determining the biosorption capacity of HRAS and biological nutrient removal (BNR)
biosorption of municipal wastewater. Lim et al. [11] reported that sludge in batch systems using the conventional method (sludge
inactive biomass mixed with wastewater for a short contact time mixed with wastewater) established in literature and its limitations
determines extracellular adsorption while active biomass quanti- for applications, (b) to determine the biosorption using ex-situ aero-
es extracellular adsorption and intracellular storage. However, bic yield of starved and non-starved biomass of HRAS systems, (c) to
they did not measure polyhydroxyalkanoates (PHA) as a stored quantify ex-situ biosorption yield using OUR on various SRT sludge,
compound and neglected oxidation of soluble COD. Since this (d) to estimate in-situ biosorption on pilot-scale HRAS systems
conventional biosorption capacity approach is inuenced by the using operational parameters, inuent carbon balance and EPS con-
possible interference of oxidation, biomass growth, non-settleable centration, and (e) to evaluate these four biosorption quantication
particulate matter from wastewater and non-settling biomass, an approaches, their potential relationship with SRT and carbon redi-
alternative approach is required for HRAS systems to quantify rection, benets and limitations for applications in wastewater
actual biosorption of organic matter from wastewater. In addi- treatment processes
tion, the HRAS systems have comparatively different settleability
characteristics (lower efuent quality) compared to the low-rate
systems [20,21], thus a proper method is required for biosorption 2. Materials and methods
quantication in HRAS systems
In HRAS systems, the inuent carbon redirection is dened as 2.1. Origin of sludge and wastewater location
entrapment, adsorption and storage of COD from the wastewa-
ter to the sludge matrix, which depends on the SRT [22,9]. The The sludge used for this study was collected from the Blue Plains
lower the SRT in a HRAS system, higher the carbon redirection Advanced Wastewater Treatment plant (AWWTP) (Washington,
from wastewater was found in previous literatures [15,8,9]. More- DC) and the pilot-scale high-rate CS systems operated there by Rah-
over, it was found that observed yield increased with decreased SRT man et al. [9] and Rahman et al. [27]. The Blue Plains AWWTP treats
and increased carbon redirection via biosorption [9]. Thus, yield, a raw wastewater through enhanced primary treatment (CEPT), bio-
stoichiometric coefcient was considered as an indirect parame- logical step-feed HRAS reactors (23 d SRT) and is followed by
ter to predict biosorption in continuous systems [9]. In high-rate biological nutrient removal (BNR) (15 d SRT) systems based on
continuous systems, the observed yield is dened as sludge pro- conventional nitrication-denitrication with methanol dosing to
duction which includes the adsorption of particulate and colloidal meet low nitrogen levels. The total inuent ow rate for 20 CEPT
organic matter, intracellular storage of soluble carbon, microbial clarier (East side) is 1095607 m3 /d and each circular clarier has
growth, and possibly decay. All of these mechanisms contribute diameter of 36.57 m, side water depth of 4.37 m and center water
to the sludge production for removal of COD from wastewater depth of 5.89 m. Each clarier has HRT of 2 h. The range of coagu-
and thus inuence the yield coefcient. Therefore, we propose an lant dosage in CEPT is between 6 and 9 mg Fe3+ /L. The primary and
approach to quantify biosorption on HRAS systems by determining high-rate WAS are hydrolyzed through a pretreatment step called
the ex-situ aerobic yield through the establishment of famine and thermal hydrolysis (CAMBI) and then digested in conventional
feast conditions (similarly to CS) in the batch reactor. mesophilic anaerobic digestion. The plant inuent (raw wastew-
A. Rahman et al. / Biochemical Engineering Journal 128 (2017) 3344 35
Table 1
Characteristics of full-scale plant inuent raw wastewater and chemically enhanced primary treatment (CEPT) efuent measured based on 24-h composite sample analysis
(n: 6580).
Note: HRT-Hydraulic retention time, SRT-Solids retention time, DO-Dissolved oxygen, tCOD-Total COD, pCOD-Particulate COD, cCOD-Colloidal COD, ffCOD-Flocculated ltered COD, WAS-Waste activated sludge, CS-Contact-
in batch experiments. In famine conditions, biomass is gener-
5.43 1.03
508 194
ally aerated for a longer period (> 2 h) to oxidize biosorbed COD
(extracellular adsorbed and intracellular stored COD) to create a
227
86
starvation phase. This creates more extra and intra cellular space
S
for adsorption and storage of organic carbon from wastewater in
feast condition. For this approach, it was assumed that the starved
2.18 0.23
0.69 0.17
0.51 0.46
CS 0.69 d
253 86
biomass expected to have higher aerobic yield coefcient under
76 36
31 15
52 8
56 9
21 4
58 5
pulse feed condition (feast regime) in the batch reactor. In conven-
227
30
C
feed conditions in the batch reactor. This is because the sludge with-
227
86
239 39
41 13
38 28
51 32
35 12
49 14
24 9
rO2
227
Y =1 (2)
86
S
rCOD
1.09 0.11
0.66 0.33
2.30 0.26
479 39
75 16
56 34
73 12
35 10
denotes the oxygen consumption rate (mgO2 /L/h) due to COD oxi-
59 8
25 4
dation and rCOD denotes the soluble COD (ltered through 1.5 m
227
30
C
2.05 0.53
0.28 0.20
47 14
46 32
51 45
26 13
46 24
40 17
2.18 0.26
0.36 0.25
618 139
CS 1.73 d
is illustrated in Fig. 1.
61 11
62 25
77 29
67 14
48 8
20 7
mgVSS/L
mgO2 /L
(3)
Unit
rO2,NP
min
1 YNP =
%
%
%
%
%
d
L
rO2,P
For pretreated sludge : 1 YP =
Efuent solids concentration
Carbon harvesting efciency
rCODP
ffCOD removal efciency
pCOD removal efciency
cCOD removal efciency
tCOD removal efciency
Volumetric loading rate
+ Biosorption
1 YNP
Parameter
rO2, P rO2, NP
Biosorption = (5)
Table 2
1 YP 1 YNP
HRT
SRT
DO
A. Rahman et al. / Biochemical Engineering Journal 128 (2017) 3344 37
Fig. 1. Conceptual diagram of biosorption yield determination, ex-situ aerobic yield coefcient determination using aerobic pretreatment and no-pretreatment approach in
a batch experiment.
where, biosorption computed in mgCOD/L/h unit, YNP , YP = Yield yield is dened here as the amount of oxygen consumed from
coefcient (gCOD/gCOD) in no-pretreatment (NP) and pretreat- biodegradable organic matter contained in the sludge as a form
ment (P) batch test, respectively; rO2,NP and rO2,P = oxygen of adsorbed COD and stored COD for any SRT condition systems.
consumption rate (mgO2 /L/h) in NP and P batch test, respectively; This denition was based on the ASM3 model which assumed
rCODNP and rCODP = removal rate of COD (mgCOD/L/h) ltered that the readily biodegradable COD from wastewater can be stored
through 1.5 m glass ber lter in NP and P batch test, respectively, as a form of intracellular products under aerobic conditions [30].
rsCODNP and rsCODP = removal rate of soluble COD ltered through In biosorption yield experiments, the biodegradation happens
1.5 m glass ber lter in NP and P batch test, respectively. through biological oxidation and hydrolysis processes in the batch
In pretreatment sludge experiment, a 2 L of freshly collected reactor. The oxidation of biodegradable COD from the sludge matrix
HRAS from the full-scale step-feed reactor (SRT of 2 d) was col- for certain aeration period provides the measurement of total oxy-
lected and aerated (DO > 4 mgO2 /L) for 24 h to create starvation gen consumption after subtraction of oxygen consumption due to
phase. After that, a 30 mL of aerated sludge were mixed with 1.9 L endogenous respiration.
of CEPT efuent as a carbon source and continuously aerated (DO A volume of 2 L of HRAS (mixed liquor) was collected from high-
of 45 mgO2 /L) for 2 h to measure oxygen consumption rate (rO2 ) rate full-scale (2.5 d and 3.5 d) and pilot scale systems (CS 1.7 d, CS
using a respirometry setup of DO controller. The respirometry 1.5 d, CS 1 d, CS 0.8 d, CS 0.7 d) at different SRT conditions and then
setup is described in Section 2.5. The samples were taken for settled for approximately 30 min to remove supernatant. The set-
every 1030 min to measure COD ltered through 1.5 m. In no- tled sludge was then diluted with nal efuent (inert soluble COD
pretreatment sludge experiment, above procedures were followed of 1220 mgCOD/L) of the full-scale plant to make the total volume
except pre-aerating the sludge. The aerobic yield coefcient for of 2 L. The sludge was aerated without adding any external sub-
both types of sludges was measured using Eq. (3) and (4). The both strate for certain time in which the decreased OUR response with
pretreatment and no-pretreatment sludge experiments were also the time indicated the oxidation of biodegradable COD. After com-
conducted to determine yield coefcient for ltered (1.5 m) CEPT plete degradation of biodegradable COD, OUR followed a constant
efuent as a carbon source to avoid the impact of active biomass response showing the endogenous respiration phase. The whole
from CEPT efuent. Then, the biosorption was calculated using Eq. area under the OUR vs time curve (excluding endogenous respira-
(5). tion) was considered as total oxygen consumed by biodegradation
of biosorbed COD. A conceptual diagram of biosorption capacity
determination is illustrated in Fig. 1. The biosorption yield was
2.5. Quantication of biosorption yield calculated by the following formula:
Fig. 3. A conventional approach of ex-situ aerobic yield determination of high-rate activated sludge (full-scale step-feed system of SRT 2 days) in a (a) high F/M ratio batch
test in which R2 0.89 and (b) low F/M ratio batch test in which R2 0.07 for COD fractions (tCOD, pCOD, sCOD) response and cumulative oxygen consumption during the
test where chemically enhanced primary treatment efuent added as a carbon source.
Fig. 5. Ex-situ aerobic yield coefcient (in a batch test) and in-situ observed yield
(continuous system) determination on reactor sludge from high-rate pilot-scale sys-
tem of completely mixed reactor (CSTR) and high-rate contact-stabilization (CS)
systems under variable SRT conditions.
the method of ex-situ aerobic yield was independent of sludge Fig. 6. The measurement of ex-situ oxygen uptake rate (OUR) of high-rate sludge
characteristics and operational conditions (SRT) of reactor process (full-scale step feed system of 2.5 d SRT) in a batch experiment where area under
congurations. This is because the yield was always higher than 0.7 the OUR curve was divided into two areas to quantify biosorption yield.
gCOD/gCOD suggesting that other key factors might have played a
contribution for high yield coefcient.
Based on the batch experimental results of pretreatment and full-scale 2.5 d SRT sludge was found to be 1256 mgO2 /gVSS and
no-pretreatment conditions, the high yield coefcient in both con- was most probably dependent on the variable operational condi-
ditions may indicated that adsorption mechanism is difcult to tions. In CSTR systems, the biosorption yield was 85 mgO2 /gVSS at
distinguish from intracellular storage in batch systems. Shifting the 3.5 d SRT while the range was 318373 mgO2 /gVSS when SRT 1.2
microbial community from a continuous reactor process conditions d (Table S6). In CS congurations, the biosorption yield increased
to a batch reactor potentially induced feast condition for microor- from 57 to 435 mgO2 /gVSS when SRT decreased from high SRT (1.7
ganisms and exhibited high yield which can be explained by d) to low SRT (0.5 d) conditions. The biosorption yield of stabi-
possible soluble COD storage [34]. The same phenomena were also lizer sludge (28293 mgO2 /gVSS) was always lower than contactor
conrmed by Chudoba et al. [35] in CSTR and PF systems feeding sludge (57435 mgO2 /gVSS) because biosorption happened in the
glucose substrate and found the ex-situ yield of 0.71 gCOD/gCOD contact tank whereas starvation occurred in the stabilization tank.
and 0.88 gCOD/gCOD, respectively. High ex-situ yields have also In this study at SRT<1 d in HRAS systems (CSTR and CS), the range of
been reported before for acetate (0.7 gCOD/gCOD) and glucose (0.8 biosorption yield was 318435 mgO2 /gVSS which was higher than
0.9 gCOD/gCOD) [29,36]. The high ex-situ yield was potentially SRT>1 d. Thus the biosorption yield approach certainly can predict
caused by changing the environmental condition from continu- the biosorption of HRAS occurred in a continuous system.
ous feeding style to a sudden rise of pulse feed. The substrate A relationship between carbon redirection, carbon oxidation
uptake rate may increase signicantly with a higher rate under and total SRT observed from pilot-scale reactor is shown in Fig. 7a.
pulse feed compared to growth limiting conditions (continuous This indicated that SRT had a positive correlation with carbon
systems). During rapid uptake of the substrate, some of the carbon oxidation and negative correlation with carbon redirection. Sim-
can be converted to storage polymer as the microorganisms can- ilar to these observations, the relationship between biosorption
not use excess substrate for their growth because of having a risk of yield and SRT (Fig. 7b), in-situ observed yield (Fig. 7c) and carbon
metabolism imbalance [37]. Therefore, storage might have played redirection, carbon oxidation (Fig. 7d) of pilot-scale high-rate CS
a dominant role in ex-situ conditions which contributed to high congurations were observed. It was found that biosorption yield
yield. However, further research is needed to evaluate this method of contactor sludge negatively correlated (R2 0.85) with total SRT
by measuring and analyzing the intracellular stored compounds of the system (Fig. 7b). The biosorption yield was also linearly cor-
and sludge oc structure to conrm biosorption mechanism. related with the observed yield of the CS system because observed
yield of a high-rate system involved sludge production through
3.3. Ex-situ biosorption yield growth, adsorption, and storage (and possibly decay) by remov-
ing COD from wastewater (Fig. 7c). In addition, biosorption yield
A change of oxygen uptake rate (OUR) against time for a 2.5 d was positively correlated with carbon redirection indicating the
SRT sludge (full-scale step-feed system) is shown in Fig. 6. The trend importance of biosorption to enhance carbon recovery (Fig. 7d).
of OUR showed that it decreased rapidly with time and reached a Ge et al. [38], Jimenez et al. [15] and Rahman et al. [9] reported
steady OUR condition after 10 h. The sharp drop of the OUR was that carbon redirection negatively correlated with SRT. In addi-
due to oxidation of biosorbed biodegradable organic matter within tion, the carbon oxidation was positively correlated (R2 0.79) with
the sludge as no biodegradable soluble organics were present. The SRT exhibited in this study (Fig. 7d). Thus, the biosorption yield
total cumulative oxygen consumption due to organic matter oxi- had a negative correlation (R2 0.75) with carbon oxidation. At low
dation and endogenous respiration was 87 mgO2 /L of which 73 mg SRT and HRT, carbon oxidation is comparatively lower than high
O2 /L was due to endogenous respiration. The biosorption yield was SRT as biosorption taken place as the dominant mechanism of
then calculated using Eq. (6) and found to be 56 mg O2 /g VSS. Fig. removing particulate and colloidal organic matter from wastew-
S2 and Table S6 illustrate the typical OUR proles as a function ater and suggested the higher biosorption yield. The biosorption
of time for various sludge collected from pilot-scale CSTR (3.5 d, yield is so far the rst parameter that can be measured in ex-situ
1.2 d, 0.3 d SRT), CS (1.7 d, 1 d, 0.8 d, 0.7 d, 0.5 d SRT) and PF conditions and shows a direct correlation with SRT, carbon mass
(0.45 d SRT) congurations operated under different SRT with their balance and potential contribution of biosorption for carbon recov-
respective biosorption yields. The range of biosorption yield for the ery. However, further research is needed to evaluate this method by
42 A. Rahman et al. / Biochemical Engineering Journal 128 (2017) 3344
Fig. 7. (a) Relationship between carbon redirection, carbon oxidation, and total SRT of pilot-scale CS congurations (steady-state conditions), (b) impact of total SRT on
biosorption yield determined from pilot-scale CS congurations (steady-state conditions), (c) relationship between observed yield and biosorption yield of contactor sludge
from pilot-scale CS systems (steady-state conditions), and (d) relationship between carbon redirection, oxidation and biosorption yield of contactor sludge from pilot-scale
CS systems (steady-state conditions).
Table 3
Comparison of different approaches evaluated in this study to quantify biosorption capacity/yield on high-rate activated sludge systems.
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