Water Research xxx (2016) 1e9

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Water Research
journal homepage: www.elsevier.com/locate/watres

Chemically induced alterations in the characteristics of fouling-

causing bio-macromolecules e Implications for the chemical cleaning
of fouled membranes
Zhongbo Zhou a, b, Xiang He a, b, Minghao Zhou a, b, Fangang Meng a, b, *
a
School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, China
b
Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology (Sun Yat-sen University), Guangzhou 510275,
China

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

Article history: Chemical cleaning is an essential process for the permeability recovery of fouled membranes, which is
Received 21 July 2016 highly related to the interactions between chemicals and bio-macromolecules in fouling layers. In this
Received in revised form study, three bio-macromolecules (i.e., efuent biopolymers (i.e., 0.45 mme100 kDa) from a full-scale
15 October 2016
municipal wastewater treatment plant, bovine serum albumin (BSA) and dextran) were exposed to
Accepted 24 October 2016
Available online xxx
different chemicals (i.e., NaClO, H2O2, NaOH, and HCl) with varied concentrations to understand the
changes in their properties and functional groups. The results showed that exposure to oxidants and
alkali decreased the consistency index of all bio-macromolecules. With an increased oxidant dose, the
Keywords:
Membrane fouling
molecular sizes of efuent biopolymers and dextran continuously reduced because of the oxidative
Membrane cleaning cleavage of the long molecule chains. However, the molecular size of BSA sharply increased after being
Chemical backwashing treated with oxidants and alkali, likely due to the cross-linkage of protein molecules. Three-dimensional
Biopolymers uorescence excitation-emission matrix (3D-EEM) spectra showed that the aromatic protein-like and
Functional groups humic substances in the efuent biopolymers were destructed readily during the treatments of oxidants
and alkali. Fourier transform infrared (FTIR) and X-ray photoelectron spectroscopy (XPS) analyse further
conrmed that exposures to NaClO, H2O2 and NaOH led to the destruction of protein structures (i.e.,
amide I, II and III), the increase of carbonyl and carboxyl groups, and the decrease of fatty acids/lipids, all
of which could make the bio-macromolecules more hydrophilic. Most importantly, the bio-
macromolecules exposed to chemicals had better lterability, and their permeability through mem-
branes also signicantly increased, which could be explained well by the above analysis. The chemical
cleaning mechanisms of fouled membranes are understood in depth in this study, and all of the results
shed light on the implementation of on-line chemical enhanced backwashing in membrane processes.
2016 Elsevier Ltd. All rights reserved.

1. Introduction
Membrane technologies, including microltration (MF), ultra-
ltration (UF), nanoltration (NF), reverse-osmosis (RO) and
forward-osmosis (FO), have been increasingly applied for drinking
water (Halle et al., 2009; Huang et al., 2009) and wastewater
treatment (Huang and Lee, 2015). The use of membranes can
signicantly improve the quality of the treated water (Zheng et al.,
2010; Tadkaew et al., 2011) and recover nutrients (Qiu et al., 2015)/
* Corresponding author. School of Environmental Science and Engineering, Sun
Yat-sen University, Guangzhou 510275, China.
E-mail address: mengfg@mail.sysu.edu.cn (F. Meng).
energy (Scherson and Criddle, 2014; Li et al., 2015) from the
wastewater; however, membrane fouling is still a vital limitation to
membrane technologies (Meng et al., 2009). Even though vast ef-
forts have been made to control membrane fouling, such as pre-
treatment of feed water (Gamage and Chellam, 2014), development
of anti-fouling strategies (Adout et al., 2010; Kim et al., 2013) and
optimization of operating parameters (Huang et al., 2011b), this
issue has not yet been well resolved until now.
Among the strategies used for fouling control, chemical cleaning
is an essential process for the permeability recovery of severely
fouled membranes (Porcelli and Judd, 2010; Wang et al., 2014a).
Five types of chemical cleaning reagents are normally employed
(Liu et al., 2001): bases (e.g., NaOH), acids (e.g., HCl), disinfectants

http://dx.doi.org/10.1016/j.watres.2016.10.065
0043-1354/ 2016 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
2 Z. Zhou et al. / Water Research xxx (2016) 1e9
or oxidants (e.g., NaClO, H2O2), chelates and surfactants. Perme-
ability recovery is achieved by means of chemical reactions be-
tween the cleaning reagents and the deposited foulants, e.g., the
bases and acids can alter membrane foulant characteristics through
solubilization and/or hydrolysis, while the oxidants can destruct
the foulants via the oxidation of chemical functional groups (Liu
et al., 2001; Porcelli and Judd, 2010). Nevertheless, the imple-
mentation of chemical cleaning in membrane-based facilities is
usually based on rules of thumb; the factors affecting cleaning ef-
ciency, such as chemical species, reagent concentrations and the
reaction time of chemicals with foulants, have not been well
dened. One of the key challenges to the resolution of this issue is
the poor mechanistic understanding of the chemical cleaning
processes. For instance, how do chemical cleaning reagents change
the deposition or adsorption propensities of foulants on mem-
branes? What types of structural and functional groups of the
foulants are more susceptible to chemical reagents?
Bio-macromolecules are believed to be one primary compound
leading to membrane fouling in membrane facilities used for
wastewater treatment and efuent reuse (Meng et al., 2011). They
are composed of proteins, polysaccharides and humic substances
and mainly produced by microorganisms. Previously, considerable
efforts have suggested that the fraction of bio-macromolecules
with a molecular size above approximately 100 kDa, referred to
as biopolymers, is the predominant foulant in membrane bio-
reactors (MBRs) (Rosenberger et al., 2006; Meng et al., 2011), UF
ltration systems (Laabs et al., 2006; Zheng et al., 2010), and
drinking water treatment processes (Halle  et al., 2009). Moreover,
the cross-linked structure of biopolymers, particularly the poly-
saccharide fractions, grants the biopolymers with strong gelling
properties (Seviour et al., 2010; Bar-Zeev et al., 2015), which is
signicantly attributed to the formation of gel layers on membrane
surfaces (Rosenberger et al., 2006; Wang and Waite, 2009a; Xiao
et al., 2013; Hong et al., 2014). Lei et al. (2016). and Xiao et al.
(2013). further revealed the formation mechanism and evolution
process of gel layers with mathematical models. In addition to the
large-size nature and sticky character, the hydrophilic\hydrophobic
interactions between gelling biopolymers and membranes could be
another important contributor to membrane fouling (Liang et al.,
2007; Xiao et al., 2014). Yamamura et al. (2014). and Shen et al.
(2010), for example, showed that the hydrophilic fractions were
likely responsible for the high fouling potential of biopolymers,
which could be mainly related to their larger size. In contrast, the
hydrophobic fractions were thought to cause higher pore blocking
and gel layer resistance due to their smaller size and higher
abundance of carboxylic complexing groups (Xiao et al., 2014;
Zheng et al., 2014). Overall, these previous studies suggest that
the chemical cleaning of fouled membranes should be aimed at two
aspects: i) the changes in the physicochemical properties (i.e.,
gelling properties and size natures) of the biopolymers and ii) more
crucially, the chemically induced alterations in the functional or
structural makeup of biopolymers (i.e., carboxylic groups (Wang
and Waite, 2009a; Xiao et al., 2014)), which could be one major
mechanism for the detachment of biopolymers from the mem-
branes (Mo et al., 2010; Zeng et al., 2014).
Given the signicance of chemical cleaning mechanisms and the
lack of related information, the intention of this study is to reveal
the chemically induced changes in efuent biopolymers (0.45 mm-
100 kDa) from a full-scale municipal wastewater treatment plant
(WWTP) and two model foulants (bovine serum albumin (BSA,
66 kDa) and dextran (500 kDa)) upon exposure to different
chemicals (i.e., NaClO, H2O2, NaOH, and HCl) with varied concen-
trations. During chemical exposure assays, physiochemical prop-
erties (i.e., the consistency index, zeta potential and molecular size)
and functional groups of the treated bio-macromolecules were
Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
characterized by multiple techniques such as Zetasizer, rheometer,
uorescence spectrometer, Fourier transform infrared (FTIR) and X-
ray photoelectron spectroscopy (XPS). Finally, the lterability of
bio-macromolecules upon exposure to chemicals was studied by a
series of stirred dead-end ltration tests.
2. Materials and methods
2.1. Bio-macromolecules and chemical cleaning reagent solutions
In this work, the wastewater efuent was taken from a full-scale
municipal WWTP (A2/O process, Li-Jiao plant, Guangzhou, China)
and then the fraction of 0.45 mm-100 kDa in the efuent was
extracted and concentrated as the efuent biopolymer stock solu-
tions by a tangential ow ltration (TFF) system (Cogent M,
Millipore Corporation, USA). The TFF technique has been widely
used in the sampling of water and wastewater because of consid-
erable advantages, such as the ability to concentrate larger sample
volumes and lower membrane clogging through parallel uid ows
tangent to the lter surfaces (Cai et al., 2015; Ellis et al., 2015). In
this pretreatment, Pellico 2 microltration (HVMP, 0.45 mm, hy-
drophilic polyvinylidenuoride (PVDF)) and ultraltration (Bio-
max-100, 100 kDa, modied polyethersulfone (PES)) mini lters
were employed. The total organic carbon (TOC) concentration of
the concentrated efuent biopolymer solution was determined to
be 98.5 mg/L by a TOC analyzer (TOC-VCPH, Shimadzu, Japan). The
efuent biopolymer is a complex mixture, consisting mainly of
large-molecular size proteins and polysaccharides. To provide more
clear insights into the physicochemical property changes in these
bio-macromolecules compounds exposed to chemicals, pure
dextran (T-500 kDa, Sigma-Aldrich) and BSA (66 kDa, Sigma-
Aldrich) were investigated as two typical model bio-
macromolecules. They were received in the powder form and
separately dissolved in deionized (DI) water to prepare stock so-
lutions (10 g/L) without further purication. Four types of chemical
cleaning reagents, including NaClO, H2O2, NaOH, and HCl, were
used. More detailed information on these chemicals is provided in
Table S1. The NaClO solution with 10.0% effective chlorine was
diluted in DI water to obtain a set of NaClO solutions (2e140 ppm
(mL/L)). A 30.0% H2O2 solution was used to prepare a series of H2O2
solutions between 0.2 and 20.0%. A series of pH solutions ranging
from 0.7 to 13.3 was prepared using 1 M HCl and 1 M NaOH solu-
tions. All of the solutions mentioned above were freshly prepared
to avoid concerns of deterioration prior to the chemical exposure
assays.
2.2. Chemicals exposure assays
The bio-macromolecule solutions (i.e., dextran, BSA, and
efuent biopolymers) were added into different chemical cleaning
reagent solutions at a volume ratio of 1:1 in a 60 mL glass bottle and
then gently stirred at 25
C for approximately 2 h. The concentra-
tions of dextran, BSA, and efuent biopolymers in the mixed so-
lutions were 5 g-dextran/L, 5 g-BSA/L, and 49.25 mg-TOC/L,
respectively. Such high bio-macromolecule concentrations used in
the chemical exposure assay allow these mixed solutions to reach
lower limits of the rheometer measurement, while having a similar
condition as the zone near the membrane surfaces (e.g., concen-
tration polarization area). Afterwards, 20 mL of the mixtures were
taken out for rheological analyses, and the rest was used for the
measurements of the zeta potential and molecular size. Before
these analyses, the pH of all mixtures was determined. As a blank,
the same volume ratio (1:1) of bio-macromolecule solutions to DI
water was mixed for the same analyses as described above. To avoid
the effects of additives on the compositions and properties of the
 Z. Zhou et al. / Water Research xxx (2016) 1e9
bio-macromolecule-chemical mixture, the oxidation reactions in
the exposure assays of NaClO and H2O2 were not terminated by
adding reductants (i.e., sodium thiosulfate/sodium sulte). In fact,
the chemical reactions proceeded very rapidly, and the physico-
chemical properties of the bio-macromolecule-chemical solutions
became almost stable after the exposure assays. Additionally, no
buffers were employed in this study since base or acid buffers have
a limited pH range and normally have excessive ionic strengths.
2.3. Physiochemical property analysis
A Zetasizer Nano-ZS90 instrument (Malvern Instruments Co.,
UK) was used to measure the zeta potential and hydrodynamic
diameter (i.e., z-average diameter) of the bio-macromolecule-
chemical mixtures and the blank bio-macromolecule at 25
C. In
this study, the z-average hydrodynamic diameter was used to es-
timate the size variations of the bio-macromolecule compounds
induced by the chemicals. The viscosity and shear stress/rate of
these mixtures were determined at various rotating speeds
(50e200 rpm) with an ultra-low adapter (DV-III Ultra Rheometer,
Brookeld, USA) at approximately 25
C. Based on the data of the
shear stress and rate, the rheological behaviors of all samples could
be assessed by the Herschel-Bulkley model because of their non-
Newtonian properties.
t t0 K gn (1)
where t is the shear stress, t0 is the yield stress, K is the consistency
index, g is the shear rate and n is the ow index. All of the mea-
surements mentioned above were conducted in at least three
replicates for each sample, and the average values are presented.
2.4. Spectroscopic analysis
Since spectroscopic analysis can well identify the functional
groups or chemical compositions belonging to proteins or poly-
saccharides in the efuent biopolymers, the treated BSA and
dextran were not further used for the following analysis. In this
work, the efuent biopolymers exposed to four chemical reagents
at given conditions (i.e., 10 ppm NaClO, 5% H2O2, pH 12, and pH 2),
as well as the raw biopolymers diluted in DI water, were charac-
terized by three-dimensional uorescence excitation-emission
matrix (3D-EEM) spectra (F-4500, Hitachi, Tokyo, Japan). The pa-
rameters of the EEM technique were similar to those reported by
Huang et al. (2011a). The EEM spectra of 10 ppm NaClO, 5% H2O2, pH
12, pH 2 and DI water without the efuent biopolymers were
analyzed as blanks to be deducted from the corresponding EEM
spectra of the efuent biopolymers-chemical solutions and the
diluted raw biopolymers, respectively. The intensities and locations
of the EEM peaks were identied according to the method of Chen
et al. (2003).
Meanwhile, the efuent biopolymers-chemical solutions and
the raw biopolymers were dried in a vacuum freeze-dryer (ALPHA,
Marin Christ, Germany) for the FTIR spectra and XPS analyses.
Before the FTIR spectroscopy measurements, the dry powdered
sample and spectrometry grade KBr were mixed and pressed at a
ratio of 1: 100 under vacuum to avoid moisture uptake. Then, the
prepared samples were characterized by an FTIR spectrometer
(Nicolet 6700-Contiumm, Thermo Scientic Corporation, USA). An
XPS instrument with Al Ka (1486.6 eV) radiation (ESCALAB 250,
Thermo-VG Scientic) was used. The major element composition of
the treated efuent biopolymers was analyzed in a broad survey
scan with 20-eV pass energy. Moreover, a high-resolution scan with
80-eV pass energy was applied for the component speciation.
Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
3
2.5. Membrane ltration tests
To understand the lterability of bio-macromolecules upon
exposure to chemicals, the membrane ltration of treated bio-
macromolecule was performed in a dead-end stirred system
(MSC300, Mosu Corp., Shanghai, China) at approximately 25
C. The
BSA and dextran mixture with a concentration ratio of 3:2 was
prepared and the TOC was controlled to be approximately 100 mg/
L, which were all based on the composition of the efuent bio-
polymers in this work. Similar to the chemical exposure assay, the
bio-macromolecule solution was separately mixed with four
chemicals (i.e., 20 ppm NaClO, 10% H2O2, 0.02 M NaOH and 0.02 M
HCl) at volumes ratio of 1:1 in a 300 mL volume for approximately
2 h under gentle stirring. Afterwards, the mixtures were transferred
into the dead-end ltration system with a stirring rate of 300 rpm.
In this test, at-sheet PVDF membranes with a molecular weight
cut-off of 150 kDa (UV150, Microdyn-Nadir, Germany) and a
diameter of 80 mm were used. More detailed characteristics of this
membrane can be found in the work of Debien (Debien et al., 2013).
The ltration pressure was kept constant at 80 kPa by a pressure
regulator (Type 10, Bellofram Corp., USA) connected to a nitrogen
bottle. Moreover, the permeate amount was continuously and
automatically monitored by an electronic scale connected to a
computer. Prior to the ltration tests, new membranes were rst
soaked in DI water for 12 h and each membrane was then ltered
with at least 300 mL of DI water to remove impurities. The
permeability of bio-macromolecules was calculated by the differ-
ences between the feeding and permeate TOC concentrations.
3. Results
3.1. Changes in physicochemical properties of bio-macromolecules
upon exposure to chemical cleaning reagents
All of the chemically treated bio-macromolecule solutions
showed shear thickening behaviors (see Fig. S1e3 in the Supple-
mentary material le), which belongs to the dilatant uid. The
Herschel-Bulkley model can t the measured data well, and the
correlation efciencies (i.e., R2) were all over 0.99. In Fig. 1(c), the
consistency index and molecular size of efuent biopolymers
initially increased at low oxidant doses, but then signicantly
decreased at high oxidant doses. In contrast, the zeta potential of
efuent biopolymers exhibited a sharp decrease at the low oxidant
doses, whereas it became less negative at the high oxidant doses.
Interestingly, the consistency index and zeta potential of dextran
presented similar change trends as that of efuent biopolymers
when exposed to the NaClO solution (Fig. 1(a) and (c)). Note that the
consistency index of efuent biopolymers and dextran, as well as
their molecular sizes, both declined at the high oxidant doses.
However, the oxidant treatments resulted in an increased molec-
ular size of BSA, especially when exposed to a high NaClO dose (in
Fig. 1 (b)). Under the alkaline conditions (pH 10e13), the consis-
tency index of bio-macromolecule solutions all decreased. In
addition, the alkaline (pH 10e13) treatments also decreased the
molecular size of dextran and efuent biopolymers. Nevertheless,
the molecular sizes of BSA and efuent biopolymers signicantly
increased under the alkaline condition, probably because of the
denaturation of proteins (Wang et al., 2016).
3.2. Changes in uorescent components of efuent biopolymers
upon exposure to chemical cleaning reagents
Even though the EEM technique is unable to detect poly-
saccharides (Her et al., 2003), it can give a semi-quantitative
analysis about the changes in components of biopolymers. As
4 Z. Zhou et al. / Water Research xxx (2016) 1e9

shown in Fig. 2a, three typical uorescence peaks were detected in
the raw efuent biopolymers solution. Peak A at excitation/emis-
sion wavelengths (Ex/Em) of 230e240 nm/335e360 nm is related
to the aromatic protein-like substances (Chen et al., 2003), Peak B at
Ex/Em of 275e285 nm/325e340 nm is associated with tryptophan
protein-like substances, and Peak C at 345e355 nm/425e440 nm is
attributed to humic acids (Wang et al., 2009). The uorescence
intensities of Peaks A and B were much higher than that of Peak C
(See in Table S2), indicating that the aromatic and tryptophan
proteins were the major uorescent compounds in the raw efuent
biopolymer solutions. After being exposed to 10 ppm NaClO
(Fig. 2b) for 2 h, the uorescence intensities of Peak A and Peak B
declined remarkably and Peak C almost disappeared. Notably, the
locations of Peak A and Peak B showed a blue shift in their emission
wavelengths, which can be attributed to the decomposition of the
aromatic ring-structures and fragmentation of large-molecular
weight compounds into smaller molecules (Korshin et al., 1999;
Swietlik and Sikorska, 2004). In Fig. 2c, the EEM spectra of
efuent biopolymers also changed substantially upon exposure to
5% H2O2, and even Peaks A and B were undetectable. Similarly, Liu
et al. (2011). reported that the uorescence intensities of protein-
like and humic-like substances in wastewater decreased by 65%
and 35% after ozone oxidation, respectively. Wenk et al. (2013).
further found cleavage of aromatic rings during the chemical
oxidation of DOM. As is well known, the uorescence intensity of
organic compounds can be inuenced by solution chemistries (i.e.,
pH and ionic strength) (Patel-Sorrentino et al., 2002; Sheng and and
Yu, 2006). In this current work, decreases of the EEM peak in-
tensities to a certain extent were also observed upon exposure to
pH 2 (Fig. 2e), while in the alkaline solution (pH 12), the uo-
rescence intensities of proteins (i.e., Peak A and Peak B) showed
only a slight decrease (Fig. 2d). Compared with the EEM result of
efuent biopolymers upon exposure to NaClO and H2O2, this sug-
gests that the oxidation of NaClO and H2O2 plays a dominant role in
the decrease of the uorescence intensity of efuent biopolymers
although their solutions are alkaline and acidic, respectively
(Fig. S4). In addition, the uorescence intensity of Peak C increased
by 26.4% in the alkaline solution (pH 12), which could be due to
the release of more uorophores of humic substances with a linear-
like and unfolding structure (Patel-Sorrentino et al., 2002). Overall,
our ndings coupled with previous work reveal that the proteins
and humic substances are easily subjected to oxidant damage (i.e.,
NaClO and H2O2), especially to the aromatic structures.
3.3. Changes in functional groups of efuent biopolymers upon
exposure to chemical cleaning reagents
FTIR and XPS analyses were further used to provide deep in-
sights into the functional group changes of efuent biopolymers
upon exposure to chemicals. As shown in Fig. 3, the FTIR prole of
the raw efuent biopolymers presented several typical functional
groups (see Table S3 for details): lipids (2930e2860 cm1), amide I
(1660e1600 cm1), amide II (1500e1300 cm1), carbohydrates/
nucleic acids (1200e900 cm1) and the ngerprint region

Fig. 1. Variations of consistency index, molecular size, and zeta potential of dextran (a), BSA (b), and efuent biopolymers (c) upon exposure to different NaClO, H2O2, alkali and acid
concentrations. Solid black square is consistency index; solid red circle is zeta potential; solid blue triangle is molecule size. Each data was measured at least three times, and the
average values with error bars were reported. Note: The chemical reagent concentrations are the theoretical or pristine values and the practical pH after exposure assays could be
found in the supporting information le. (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of this article.)

Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
 Z. Zhou et al. / Water Research xxx (2016) 1e9 5

Fig. 2. Composition and intensity of uorescent compounds in efuent biopolymers mixed with DI water, 10 ppm NaClO, 5% H2O2, NaOH (pH 12), and HCl (pH 2) solutions. X
axis is emission wavelength; Y axis is excitation wavelength; and the uorescence intensity is denoted by the color bar in the left side of the Figure. (For interpretation of the
references to colour in this gure legend, the reader is referred to the web version of this article.)

(900e600 cm1). Signicant differences were observed in the FTIR
spectra of efuent biopolymers upon exposure to different chem-
icals. In Fig. 3(c) and (d), the oxidant exposures induced the
disappearance of the amide I band at 1559 cm1 as well as a
decrease in the intensities of the amide II (1620 cm1) and III
(1389 cm1) bands, implying that the protein structure of the
efuent biopolymers was destructed, which agreed with the results
of Section 3.2. Given that the 10 ppm NaClO solution has a higher
pH value (ca. 11), the alkaline conditions are also expected to
change the functional groups of efuent biopolymers. Decreased
FTIR intensities in the 3518e2918 cm1 and 1125e1047 cm1 re-
gions of the efuent biopolymers upon exposure to NaClO and
NaOH (pH 12) were observed, indicating that the groups asso-
ciated with lipids and polysaccharides were damaged. The FTIR
intensity of the peak belonging to the amide groups in proteins (ca.
at 1620 cm1) also decreased in the NaOH (pH 12) solution,
which is in agreement with the investigation of Wang et al. (2012).
In addition, the exposure to HCl (pH 2) resulted in lower in-
tensities of the protein bands at 1620 and 1389 cm1, which could
well explain the decreasing intensities of Peaks A and B in the EEM
spectra (Fig. 2e) after being treated with the strong acid (pH 2).
The XPS spectra were recorded in the energy range of 0e1100 eV
for efuent biopolymers in DI water, 10 ppm NaClO, 5% H2O2, pH 2
and pH 12 solutions (Fig. S6). The high-resolution scans (Fig. S7)
were analyzed to obtain more detailed information about the
changes of the chemical functionalities of C (284.8 eV), N (400.0 eV)
and O (532.8 eV) induced by chemicals. As shown in Table 1, in the
raw efuent biopolymers, the organic element abundance was in
the order of C>O>N>S>P, with percentages of 45.99, 40.38, 1.80,
1.74 and 0.90%, respectively. In addition, some residual inorganic
elements such as Na (3.35%) and Ca (2.96%) were detected in the
efuent biopolymers. The functional group of Ce(C, H) was pre-
dominant in the raw efuent biopolymers, with a percentage of
49.6% of the total carbon, followed by Ce(O,N) (34.8%) and CeOeH/
CeOeC/CeOeP (1.9%). This indicates that the raw efuent bio-
polymers were rich in lipids, proteins and polysaccharides. In
addition, the N element was mainly contributed by Nnonpr
(approximately 96%) rather than Npr, which is consistent with the
results of EPS extracted from bacteria (Badireddy et al., 2008) and
NOM in a river (Meng et al., 2012). Interestingly, exposures to
NaOH, NaClO, and H2O2 resulted in considerable reductions in the
abundance of Ce(O, N). Notably, the abundance of CeOeH/CeOeC/
CeOeP (i.e., the O1s peak at 532.7 eV) decreased in the NaClO and
NaOH treatments, while the ratios of P]O/O]C (the O1s peak at
531.3 eV) and O]CeOH/O]CeOR (the C1s peak at 288.2 eV)
increased. In addition, the loss of organic oxygen in the efuent
biopolymers was found in the treatment of oxidants as a result of
the generation of CO2 and H2O (Wang et al., 2014a). The NaClO
treatment also reduced the amount of Nnonpr in the efuent bio-
polymers because of the transformation of amides, amines, and
pyridine (Meng et al., 2012). Briey, the chemical compositions and
functional groups of efuent biopolymers (i.e., aromatics, proteins
and lipid-like structures) were susceptible to NaClO, H2O2 and
NaOH.
3.4. Membrane lterability of the chemically treated bio-
macromolecules
As shown in Fig. 4a, under the same initial TOC content in the
samples, the untreated raw bio-macromolecules led to the most

Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
6 Z. Zhou et al. / Water Research xxx (2016) 1e9

information on the fundamental interactions between fouling-

causing bio-macromolecules and chemical cleaning reagents ex-
ists, leading to a lack of understanding and premature optimization
of the chemical cleaning process. In the present work, we have
given a deeper insight into this issue by focusing on the changes in
the physicochemical property and functional group of chemically
treated bio-macromolecules. Furthermore, a close relationship
between the two factors is built as a novel way for promoting
chemical cleaning of membranes.

4.1. Relationship between physicochemical property and functional

groups of chemically treated bio-macromolecules

All of these changes in the functional groups of bio-

Fig. 3. Changes of FTIR of efuent biopolymers in DI water, 10 ppm NaClO, 5% H2O2,
HCl (pH 2), and NaOH (pH 12) solutions. Each spectrum is the average of 16 scans.
The bands at 3398 cm1 and at 3518 cm1 indicate the presence of the OeH groups in
polymeric compounds (i.e., polysaccharides) and amino groups (i.e., proteins). The
peaks at 2918 cm1 and 2848 cm1 are attributed to the asymmetric and symmetric
stretching vibrations of CH2 from lipids. The peak at 1734 cm1, corresponding to the
stretching of carboxyl and ketonic carbonyl groups, is likely indicative of the presence
of fatty acids. The bands in the region of 1620e1660 cm1 are assigned to the amide I
(i.e., C]O stretching vibrations). The peak at 1550 cm1 is due to the stretching vi-
brations of CeN and the bending of NeH (Amide II), which also indicate the presence
of proteins. The peak at ca.1389 cm1 is involved in the CeO stretching of COOe
groups. The spectra bands between 1150 and 1030 cm1 are assigned to ring vibrations
of P]O, CeOeC and CeOeP in phosphodiesters and lipopolysaccharides (Badireddy
et al., 2008).
signicant ux decline; however, all the chemically treated bio-
macromolecules had a better lterability compared with the raw
one, especially in the treatments of NaClO and NaOH. Moreover, the
permeability of bio-macromolecules exposed to the oxidants and
alkaline was much higher (approximately 35%) than that of the raw
one (near 15%) (Fig. 4b). These results further corroborate that the
characteristics of bio-macromolecules are signicantly changed
after being treated by these chemical cleaning reagents and thus
interactions between the treated bio-macromolecules and mem-
branes are weakened.
4. Discussion
Chemical cleaning technologies have been widely used in
various membranes for fouling control. However, limited
macromolecules upon exposure to the chemicals are responsible
for the variations of their molecular size, consistency index and zeta
potential. In our work, the amine and amide groups associated with
proteins (i.e., Ce(O, N)) and the groups involved with lipids and
polysaccharides (i.e, Ce(C, H) and CeOeH) were strongly destroyed
by the oxidants and alkali. In fact, the proteins and polysaccharides
are readily hydrolysable in the oxidants and alkali because of the
disruptions of peptide and 1,4-b-glycoside bonds (Brodeur et al.,
2011). The fatty acids and lipids could also react with caustic
chemicals through saponication (Liu et al., 2001). As a result of
molecular oxidation, hydrolysis and saponication, the double
bond structures (i.e., carbonyl and carboxyl groups) in the com-
pounds could increase, which would denitely increase the hy-
drophilicity and thus decrease the consistency index of bio-
macromolecules (Sangseethong et al., 2010; de Moura et al.,
2011). Additionally, the breakage of long-chain molecules or
cross-linked structures could be another reason for the decreasing
molecular size and consistency index of polysaccharides treated by
the oxidants and alkali (Li and Hou, 2011). Meanwhile, previous
research has denoted that polysaccharides undergo a sol-gel tran-
sition with decreasing pH (Seviour et al., 2010), which could also be
responsible for the molecular size and rheological property. They
have relaxed helical structures under the alkaline condition as a
result of the neutralization of amino groups (Mitsumata et al.,
2003) and the ionization of hydroxyl groups (Williams et al.,
2000), whereas they can form condensed aggregates, i.e., gels, in
the neutral/acidic solutions. Draget et al. (1994). reported that
intermolecular electrostatic attractions, such as hydrogen bonding
in the carboxyl groups, were one primary reason for such sol-gel
transitions.
However, the covalent modication of the side chain of the
amino acids occurs upon exposure to the oxidants, which leads to
the cross-linkage between protein molecules and thus the

Table 1
Atomic fractions for elemental composition obtained from XPS high-resolution C s1, N s1 and O s1 spectra of efuent biopolymers in DI water, 10 ppm NaClO, 5% H2O2, pH 2 and
pH 12 solutions.

Element Peak Assignments Chemical functions (molar ratio with respect to total carbon)
(eV)
Raw pH12 10 ppm NaClO 5% H2O2 pH2

C1S 284.6 Ce(C,H) 0.496 0.585 0.631 0.644 0.527

285.7 Ce(O,N) 0.348 0.185 0.236 0.249 0.353
286.2 C]O,OeCeO 0.128 0.094 0.103 0.083 0.101
288.2 O]CeOH, O CeOR 0.028 0.136 0.03 0.024 0.02
Total C 284.6 At. % 45.99 40.01 46.62 63.37 56.45

O1S 531.3 C]O, P]O, PeO 0.239 1.294 0.559 0.115 0.178
532.7 CeOeH,CeOeC, CeOeP 1.877 0.978 0.615 0.913 1.265
Total O 531.5 At. % 40.38 41.55 27.73 26.8 32.53

N1S 399.9 Nnonpr 0.09 0.081 0.044 0.117 0.12

402.2 Npr 0.004 0.006 0.01 0.004 0.006
Total N 399.7 At. % 1.8 2.2 1.83 4.38 4.14

Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
 Z. Zhou et al. / Water Research xxx (2016) 1e9
Fig. 4. Fouling behaviors (a) and permeability (b) of bio-macromolecules (mixtures of
BSA and dextran with a concentration ratio of 3:2) upon exposure to chemicals (i.e., DI
water, 10 ppm NaClO, 5% H2O2, HCl (pH 2), and NaOH (pH 12)). The ltration test
was conducted twice and the averaged permeability of bio-macromolecules was
shown.
generation of large-size aggregates (Hazell et al., 1994; Hazen et al.,
1998). Meanwhile, the carbonyl groups of oxidized lipids and pro-
tein side chains (i.e., amines) could also form covalent cross-
linkages leading to aggregates (Hohn et al., 2013). Zeng et al.
(2014). and Chapman et al. (2003). also found noncovalent in-
teractions between the hydrophobic cores of protein molecules to
be another factor for such aggregate formation. In addition, the loss
of protein secondary structures was reported to promote the
increasing molecular size of proteins (Gulseren et al., 2007; Zeng
et al., 2014). In our work, the protein secondary structures of the
treated efuent biopolymers were also analyzed (Fig. S5) according
to the derivative spectra and the peak assignments via curve-tting
procedures for the amide I band of the original spectra (Stuart,
2004). Note that the abundance of aggregated strands in the
efuent biopolymers decreased sharply after the NaClO treatment
(Table S4). Exposure to strong alkaline (pH 12) solutions led to a
decreasing abundance of the aggregated strands and a-helixes,
which is consistent with previous studies (Omoike and Chorover,
2004; Wang et al., 2009; 2016). It has been reported that
increasing a-helixes was important for the occulation of protein
molecules (Kwaambwa and Maikokera, 2008). Moreover, the
Please cite this article in press as: Zhou, Z., et al., Chemically induced alterations in the characteristics of fouling-causing bio-macromolecules e
Implications for the chemical cleaning of fouled membranes, Water Research (2016), http://dx.doi.org/10.1016/j.watres.2016.10.065
7
abundances of b-sheets and a-helixes in the proteins of efuent
biopolymers increased after being exposed to the oxidants. All of
these results suggest that the protein secondary structures are
indeed responsible for the increasing molecular size of BSA in the
treatments of oxidants and alkali.
4.2. Implications for chemical cleaning
This current work provides some fundamental information on
the characteristic alterations of bio-macromolecules upon exposure
to chemical cleaning reagents, which can aid us in shedding light on
the chemical cleaning mechanisms of fouled membranes. Treat-
ments with higher doses of oxidants and alkali decreased the
consistency index of bio-macromolecules; that is, the ow index of
the bio-macromolecules increased, which could be used to explain
the mechanism of the treated bio-macromolecules detaching
readily from the membranes. Our previous work has demonstrated
that NaClO and NaOH online backwashing enhanced the detach-
ment of biopolymers in the gel-layers compared with DI water
backwashing (Wang et al., 2014b; Zhou et al., 2014). In addition, the
decreasing molecular sizes of bio-macromolecules in the treat-
ments of oxidants could also facilitate the transport of bio-
macromolecules through the membrane. Notably, upon exposure
to the oxidants and alkali, the destruction of the aromatic and
protein-like structures, the increase of carbonyl and carboxyl
groups, and the decrease of fatty acids and lipids could induce the
changes in the composition and gel structures of the biolm/bio-
cake on fouled membranes. This is an important clue that oxidant
and alkaline cleaning/backwashing can recover membrane
permeability well.
It should be noted that even though NaClO, H2O2 or NaOH
cleaning or online backwashing could be good solutions to alleviate
membrane fouling, it is crucial for us to understand that a higher
chemical dose does not always mean a better cleaning strategy for
membrane performance. In this work, a higher H2O2 dose induced
an abrupt increase of BSA molecular size, which probably caused
severe membrane fouling although it did not produce toxic
byproducts compared with NaClO (Wang et al., 2014a). Meanwhile,
a higher NaClO and NaOH dose exposure has also been reported to
result in physical damage to the membranes (Wang et al., 2014b;
Zhou et al., 2014) and the death of bacteria (Cai and Liu, 2016;
Han et al., 2016). Although the treatment with acids resulted in
uctuations in the molecular size/zeta potential of BSA/efuent
biopolymers, the role of acids in the removal of inorganic fouling
(i.e., calcium, magnesium and struvite) (Wang et al., 2014a) should
be further considered, especially the effect of acids on the com-
plexing structures with some inorganic salts. Therefore, the types
and concentrations of chemical cleaning reagents should be care-
fully considered based on the compositions of foulants prior to
conducting membrane cleaning.
4.3. Research needs and challenges
Given that the focus of our current work was to understand the
changes in the chemical nature of bio-macromolecules upon
exposure to cleaning reagents, membrane fouling behaviors of
chemically treated bio-maromolecules were only preliminarily
evaluated at a macro level here. In our future work, the detailed
interactions between the treated bio-macromolecules and mem-
brane surfaces will be further studied at the micro or molecular
level by some advanced techniques. For instance, development or
use of atomic force microscopy (AFM) (Wang et al., 2013) and
quartz crystal microbalance with dissipation monitoring (QCM-D)
(Contreras et al., 2011; Armanious et al., 2014) are promising to
provide deeper information based on the determination of
8 Z. Zhou et al. / Water Research xxx (2016) 1e9
interfacial adhesion forces. However, we have to admit that
membrane cleaning is a very complex process. Apart from the
foulant-chemical and foulant-membrane interactions, it involves
the interaction between chemicals and membranes. Indeed, the
characteristics of membranes, such as hydrophobicity and surface
functionalities, would change after long-term exposure to chemical
cleaning reagents (Levitsky et al., 2011; Regula et al., 2014), which
could alter the deposition behavior of foulants on membranes (Tian
et al., 2010). Therefore, future work need also focus on the changing
interactions between foulants and chemically treated membranes
to advance the understanding of membrane fouling and cleaning
processes (Robinson et al., 2016).
5. Conclusions
In this study, the alterations of physicochemical properties and
functional groups of three bio-macromolecules (i.e., efuent bio-
polymers, dextran and BSA) upon exposure to different chemical
cleaning reagents (i.e., NaClO, H2O2, NaOH, and HCl) were under-
stood in depth. The principle conclusions can be drawn as follows:
C Oxidants and alkali decreased the consistency index of all
bio-macromolecules. The molecular size of efuent bio-
polymers and dextran were signicantly decreased after
being exposed to the oxidants. In contrast, considerable in-
creases in the molecular size of BSA were found in the
treatments of oxidants and alkali.
C Treatments with NaClO, H2O2 and NaOH also induced sub-
stantial changes in the functional groups of bio-
macromolecules such as the destruction of protein struc-
tures (i.e., amide I, II and III), the increase of carbonyl and
carboxyl groups, and the decrease of fatty acids and lipids,
which could make the bio-macromolecules more
hydrophilic.
C The lterability of bio-macromolecules improved after being
exposed to chemicals. In particular, a higher percentage of
bio-macromolecules through the membranes was observed
in the treatments of oxidant and alkali, which could be highly
related to the changes in the characteristics of bio-
macromolecules (i.e., molecular sizes, surface charges and
functional groups).
Acknowledgements
This study was supported by the Natural Science Foundation of
Guangdong Province (No. 2014A030306002), the Pearl River S&T
Nova Program of Guangzhou (2012J2200045), the National Natural
Science Foundation of China (No. 51478487) and the Fundamental
Research Funds for the Central Universities (No. 15lgjc14).
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.watres.2016.10.065.
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