jen00214_prn 148..156 - Journal of Environmental Sciences

Journal of Environmental Sciences
Volume 30 2015
www.jesc.ac.cn
Highlight articles
129
Rice: Reducing arsenic content by controlling water irrigation
Ashley M. Newbigging, Rebecca E. Paliwoda and X. Chris Le
132
Apportioning aldehydes: Quantifying industrial sources of carbonyls
Sarah A. Styler
Review articles
30
Application of constructed wetlands for wastewater treatment in tropical and subtropical regions
(2000–2013)
Dong-Qing Zhang, K.B.S.N. Jinadasa, Richard M. Gersberg, Yu Liu, Soon Keat Tan and Wun Jern Ng
47
Stepwise multiple regression method of greenhouse gas emission modeling in the energy sector in Poland
Alicja Kolasa-Wiecek
113
Mini-review on river eutrophication and bottom improvement techniques, with special emphasis on
the Nakdong River
Andinet Tekile, Ilho Kim and Jisung Kim
Regular articles
1
Effects of temperature and composite alumina on pyrolysis of sewage sludge
Yu Sun, Baosheng Jin, Wei Wu, Wu Zuo, Ya Zhang, Yong Zhang and Yaji Huang
9
Numerical study of the effects of local atmospheric circulations on a pollution event over
Beijing–Tianjin–Hebei, China
Yucong Miao, Shuhua Liu, Yijia Zheng, Shu Wang and Bicheng Chen, Hui Zheng and Jingchuan Zhao
21
Removal kinetics of phosphorus from synthetic wastewater using basic oxygen furnace slag
Chong Han, Zhen Wang, He Yang and Xiangxin Xue
55
Abatement of SO2–NOx binary gas mixtures using a ferruginous active absorbent: Part I. Synergistic
effects and mechanism
Yinghui Han, Xiaolei Li, Maohong Fan, Armistead G. Russell, Yi Zhao, Chunmei Cao, Ning Zhang
and Genshan Jiang
65
Adsorption of benzene, cyclohexane and hexane on ordered mesoporous carbon
Gang Wang, Baojuan Dou, Zhongshen Zhang, Junhui Wang, Haier Liu and Zhengping Hao
74
Flux characteristics of total dissolved iron and its species during extreme rainfall event in the
midstream of the Heilongjiang River
Jiunian Guan, Baixing Yan, Hui Zhu, Lixia Wang, Duian Lu and Long Cheng
81
Sodium fluoride induces apoptosis through reactive oxygen species-mediated endoplasmic
reticulum stress pathway in Sertoli cells
Yang Yang, Xinwei Lin, Hui Huang, Demin Feng, Yue Ba, Xuemin Cheng and Liuxin Cui
90
Roles of SO2 oxidation in new particle formation events
He Meng, Yujiao Zhu, Greg J. Evans, Cheol-Heon Jeong and Xiaohong Yao
102
Biological treatment of fish processing wastewater: A case study from Sfax City (Southeastern Tunisia)
Meryem Jemli, Fatma Karray, Firas Feki, Slim Loukil, Najla Mhiri, Fathi Aloui and Sami Sayadi
CONTENTS
122
Bioreduction of vanadium (V) in groundwater by autohydrogentrophic bacteria: Mechanisms and
microorganisms
Xiaoyin Xu, Siqing Xia, Lijie Zhou, Zhiqiang Zhang and Bruce E. Rittmann
135
Laccase-catalyzed bisphenol A oxidation in the presence of 10-propyl sulfonic acid phenoxazine
Rūta Ivanec-Goranina, Juozas Kulys, Irina Bachmatova, Liucija Marcinkevičienė and Rolandas Meškys
140
Spatial heterogeneity of lake eutrophication caused by physiogeographic conditions: An analysis of
143 lakes in China
Jingtao Ding, Jinling Cao, Qigong Xu, Beidou Xi, Jing Su, Rutai Gao, Shouliang Huo and Hongliang Liu
148
Anaerobic biodegradation of PAHs in mangrove sediment with amendment of NaHCO3
Chun-Hua Li, Yuk-Shan Wong, Hong-Yuan Wang and Nora Fung-Yee Tam
157
Achieving nitritation at low temperatures using free ammonia inhibition on Nitrobacter and real-time
control in an SBR treating landfill leachate
Hongwei Sun, Yongzhen Peng, Shuying Wang and Juan Ma
164
Kinetics of Solvent Blue and Reactive Yellow removal using microwave radiation in combination with
nanoscale zero-valent iron
Yanpeng Mao, Zhenqian Xi, Wenlong Wang, Chunyuan Ma and Qinyan Yue
173
Environmental impacts of a large-scale incinerator with mixed MSW of high water content from a
LCA perspective
Ziyang Lou, Bernd Bilitewski, Nanwen Zhu, Xiaoli Chai, Bing Li and Youcai Zhao
180
Quantitative structure–biodegradability relationships for biokinetic parameter of polycyclic aromatic
hydrocarbons
Peng Xu, Wencheng Ma, Hongjun Han, Shengyong Jia and Baolin Hou
191
Chemical composition and physical properties of filter fly ashes from eight grate-fired biomass
combustion plants
Christof Lanzerstorfer
198
Assessment of the sources and transformations of nitrogen in a plain river network region using a
stable isotope approach
Jingtao Ding, Beidou Xi, Qigong Xu, Jing Su, Shouliang Huo, Hongliang Liu, Yijun Yu and Yanbo Zhang
207
The performance of a combined nitritation–anammox reactor treating anaerobic digestion
supernatant under various C/N ratios
Jian Zhao, Jiane Zuo, Jia Lin and Peng Li
215
Coagulation behavior and floc properties of compound bioflocculant–polyaluminum chloride dualcoagulants and polymeric aluminum in low temperature surface water treatment
Xin Huang, Shenglei Sun, Baoyu Gao, Qinyan Yue, Yan Wang and Qian Li
223
Accumulation and elimination of iron oxide nanomaterials in zebrafish (Danio rerio ) upon chronic
aqueous exposure
Yang Zhang, Lin Zhu, Ya Zhou and Jimiao Chen
231
Impact of industrial effluent on growth and yield of rice (Oryza sativa L. ) in silty clay loam soil
Mohammad Anwar Hossain, Golum Kibria Muhammad Mustafizur Rahman, Mohammad Mizanur Rahman,
Abul Hossain Molla, Mohammad Mostafizur Rahman and Mohammad Khabir Uddin
241
Molecular characterization of microbial communities in bioaerosols of a coal mine by 454
pyrosequencing and real-time PCR
Min Wei, Zhisheng Yu and Hongxun Zhang
252
Risk assessment of Giardia from a full scale MBR sewage treatment plant caused by membrane
integrity failure
Yu Zhang, Zhimin Chen, Wei An, Shumin Xiao, Hongying Yuan, Dongqing Zhang and Min Yang
186
Serious BTEX pollution in rural area of the North China Plain during winter season
Kankan Liu, Chenglong Zhang, Ye Cheng, Chengtang Liu, Hongxing Zhang, Gen Zhang, Xu Sun
and Yujing Mu
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S 30 (2 0 1 5 ) 1 48–1 5 6
Available online at www.sciencedirect.com
ScienceDirect
www.journals.elsevier.com/journal-of-environmental-sciences
Anaerobic biodegradation of PAHs in mangrove sediment with
amendment of NaHCO3
Chun-Hua Li1,2 , Yuk-Shan Wong3 , Hong-Yuan Wang5 , Nora Fung-Yee Tam2,4,⁎
1. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012,
China. E-mail: lich@craes.org.cn
2. Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China
3. Department of Biology, The Hong Kong University of Science and Technology, Hong Kong, China
4. State Key Laboratory on Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China
5. Key Laboratory of Nonpoint Source Pollution Control, Ministry of Agriculture/Institute of Agricultural Resources and Regional Planning,
Chinese Academy of Agricultural Sciences, Beijing 100081, China
AR TIC LE I N FO
ABS TR ACT
Article history:
Mangrove sediment is unique in chemical and biological properties. Many of them suffer
Received 30 May 2014
polycyclic aromatic hydrocarbon (PAH) contamination. However, the study on PAH
Revised 1 September 2014
biological remediation for mangrove sediment is deficient. Enriched PAH-degrading
Accepted 5 September 2014
microbial consortium and electron acceptor amendment are considered as two effective
Available online 27 January 2015
measures. Compared to other electron acceptors, the study on CO2, which is used by
Keywords:
the anaerobic biodegradation of four mixed PAHs, namely fluorene (Fl), phenanthrene (Phe),
Anaerobic biodegradation
fluoranthene (Flua) and pyrene (Pyr), with or without enriched PAH-degrading microbial
Electron acceptor amendment
consortium in mangrove sediment slurry. The trends of various parameters, including PAH
Mangrove sediment
concentrations, microbial population size, electron-transport system activities, electron
NaHCO3 amendment
acceptor and anaerobic gas production were monitored. The results revealed that the
Polycyclic aromatic hydrocarbon
inoculation of enriched PAH-degrading consortium had a significant effect with half lives
methanogens, is still seldom. This study investigated the effect of NaHCO3 amendment on
shortened by 7–13 days for 3-ring PAHs and 11–24 days for 4-ring PAHs. While NaHCO3
amendment did not have a significant effect on the biodegradation of PAHs and other
parameters, except that CO2 gas in the headspace of experimental flasks was increased.
One of the possible reasons is that mangrove sediment contains high concentrations of
other electron acceptors which are easier to be utilized by anaerobic bacteria, the other one
is that the anaerobes in mangrove sediment can produce enough CO2 gas even without
adding NaHCO3.
© 2015 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences.
Published by Elsevier B.V.
Introduction
Polycyclic aromatic hydrocarbon (PAH) has been shown to induce
a number of toxic effects, such as respiratory stimulation, genotoxicity, mutagenic, tumorigenicity and carcinogenicity (USEPA,
1993). Because of their low water solubility and hydrophobicity,
PAHs are persistent in the environment and tend to adsorb
readily onto particulate matter in air and water, with sediments
becoming their ultimate repository. High PAH concentrations have
been found near urban and industrialized coastal regions (Ke et al.,
2005). Mangrove ecosystems commonly found in the inter-tidal
zone of tropical and subtropical regions are often under pollution
⁎ Corresponding author. E-mail: bhntam@cityu.edu.hk (Nora Fung-Yee Tam).
http://dx.doi.org/10.1016/j.jes.2014.09.028
1001-0742/© 2015 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.
J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 30 (2 0 1 5 ) 1 4 8–1 5 6
stress and are sinks, or receivers, of various man-made pollutants
(Zheng et al., 2002). In addition to contaminated tidal water, inputs
from rivers or streams, storm-water run-off, sewage discharges and
atmospheric deposition are possible sources of PAHs (Ke et al.,
2005).
Although many PAHs are known to be biodegraded under oxic
conditions, most contaminated sediments are anoxic. Hence,
anaerobic bacteria should play a more important role in biodegradation of PAHs in the natural environment (Levett, 1990). With
recent results demonstrating that some PAHs could be degraded
without oxygen, anaerobic electron acceptors, such as NO−3, SO2−
4
and Fe(III) could be used by bacteria to biodegrade PAH contaminants (Coates et al., 1996; Ambrosoli et al., 2005; Chang et al.,
2008). Furthermore, anaerobic biodegradation seems to make a
complete breakdown by converting PAHs to CO2 (Hutchins et al.,
1991; Macrae and Hall, 1998; Nieman et al., 2001), while most
aerobic biodegradation would leave incomplete breakdown products in the polluted environment (Chang et al., 2008).
Biodegradation could also be enhanced with the amendment
of electron acceptors. Recent studies have demonstrated that anaerobic biodegradation of PAHs can be improved by adding electron acceptors, which are utilized by anaerobes (Coates et al., 1996;
Chang et al., 2003). As for methanogens, they use CO2 or carbonate
as a terminal electron acceptor. And CO2/bicarbonate (Genthner
et al., 1997) or sodium bicarbonate (Chang et al., 2008) is often
used as an electron acceptor source. The latter was chosen in the
present study because it can produce CO2 easily when dissolves in
water and it is more applicable in in-situ remediation.
The present study aims to: (1) evaluate the effect of NaHCO3
amendment on the anaerobic biodegradation of mixed PAHs comprising fluorene (Fl), phenanthrene (Phe), fluoranthene (Flua) and
pyrene (Pyr) in mangrove sediment slurry; (2) examine the effect
of enriched PAH-degrading microbial consortium and (3) monitor
the trend of various parameters during the biodegradation period,
including PAH concentrations, microbial population size, electrontransport system (ETS) activities, electron acceptor and anaerobic
gas production.
149
was about 5 μg/g dry weight (dw) and the dominant electron
acceptors were sulfate (1939.9 μg/g dw), followed by Fe(III)
(333.5 μg/g dw), nitrate (20.3 μg/g dw) and Mn(IV) (2.5 μg/g dw).
The sediment was sieved through a 2 mm sieve to remove
materials, such as stones and plant debris, before use.
1.4. Microbial growth medium
The mineral salt medium (MSM) was used as the medium for
microbial growth. It contains the following compounds (g/L):
K2HPO4, 0.27; KH2PO4, 0.35; NH4Cl, 2.7; MgCl2·6H2O, 0.1;
CaCl2·2H2O, 0.1; FeCl2·4H2O, 0.009; MnCl2·4H2O, 0.004; ZnCl2,
0.0014; CoCl4·6H2O, 0.001; and (NH4)6 Mo7O24·4H2O, 0.001. The
medium pH and salinity were adjusted to 7.2 and 25‰, respectively. The freshly prepared 0.8 mL Na2S·9H20 (0.5 mol/L)
solution was aseptically added into 1000 mL autoclaved MSM
through a 0.25 μm pore size filter.
1.5. Electron acceptor amendment
Sodium bicarbonate (1.68 g) was added to 1 L MSM to form
20 mmol/L, and the CO2 gas concentration developed in the
headspace was 13.3% (0.65 mmol per flask) at the beginning of
experiment.
1.6. PAH biodegradation experiment
The four PAH compounds (Fl, Phe, Flua and Pyr) used in this
study were purchased from Sigma Chemicals, USA (purity >
96%). A stock solution containing 5 g/L of each PAH was
dissolved in distilled acetone.
Five treatments were included, they were (1) indigenous
bacteria (IB): without sodium bicarbonate amendment and
inoculums of enriched consortium, only PAHs, MSM and
sediment; (2) indigenous bacteria plus sodium bicarbonate
amendment (IB + NaHCO3): sodium bicarbonate amendment
was applied to IB treatment; (3) enriched bacteria (EB): the
enriched PAH-degrading consortium was inoculated in to IB
treatment; (4) EB + NaHCO3: sodium bicarbonate amendment
was applied to EB treatment and (5) sterile control (SC): same
as IB but the sediment was sterilized by autoclaving at 121°C
and a pressure of 1 bar for one hour, for three consecutive
days; 0.2 mL NaN3 (0.15 g/mL) was added to ensure the microorganisms in the sediment were inactive.
Quickfit conical flasks (100 mL), with silicone suba-seal
septa (Sigma-Aldrich) and wrapped with aluminum foil, were
used to perform the biodegradation experiment. Mixed PAH
stock (50 μL; 5000 mg/L for each PAH) was spiked into the
flask and placed in a sterile fume hood for 30 min for acetone
vaporization. Fresh sediment (25 g) was transferred into the
flask to obtain an initial concentration of 10 mg/kg (fresh
weight) for each PAH. MSM (25 mL) was then added to the
flask. The flasks were shaken at 150 r/min and 28°C for
125 days under non-oxygen condition, which was maintained
following the same method described in our former publication (Li et al., 2009). In brief, the gas in the headspace of flask
was replaced with high purified N2 gas. The flasks were shaken
at 150 r/min and 28°C for 125 days.
1.3. Collection of sediments
1.7. Analytical methodology
Subsurface sediment was freshly collected by PVC cores from
a depth of 10–15 cm in Ma Wan mangrove swamp, Hong Kong,
China. The total concentration of the 16 US EPA priority PAHs
Six replicates of samples were sacrificed every 25 days, three
of which were used for PAH analysis and the others for the
determination of the population sizes of different microbial
1. Materials and methods
1.1. Enriched anaerobic PAH-degrading microbial consortium
The enriched anaerobic PAH-degrading microbial consortium
was used. The dominant microbial species included Bacillus
sp., Clostridium sp., Geobacillus sp., Methanobacterium formicium,
Delftia sp., and Bacillus acidicola sp. The enriched consortium
was incubated at 28°C under non-oxygen condition, until
a microbial population size of about 106 mL−1 was reached.
The suspension was used as inoculums in some treatments
described below.
1.2. Chemicals
150
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S 30 (2 0 1 5 ) 1 48–1 5 6
groups, the microbial activity under PAH stress, concentrations of electron acceptors used by anaerobic bacteria. Sediment
slurries in the flasks were freeze-dried, extracted and concentrated to determine the residual PAHs following the standard
method described by Li et al. (2009). The PAHs were quantified
by a Hewlett Packard 7890ATHB gas chromatography with a
flame ionization detector (GC-FID), using a HP-5MS fused
silica capillary column (30 m × 0.25 mm × 0.25 μm) (Restek,
Bellefonte, Pennsylvania, USA). The chromatographic conditions
were as follows: carrier gas: helium (1 mL/min); injection mode:
splitless; injector and detector temperature: 280°C and 300°C,
respectively. The oven temperature program was as follows: held
at 80°C for 1 min, increased to 190°C at 30°C/min, increased to
225°C at 1.8°C/min and then increased to 280°C at 30°C/min and
held at 280°C for 3 min. The recovery rates of Fl, Phe, Flua and Pyr
using this analytical approach were 92.2%, 99.4%, 99.1% and
100.1% respectively. Their detection limits were 0.23, 0.23, 0.49
and 0.45 ng/g dry sediment, respectively.
A modified most probable number (MPN) method (Li et al., 2009)
was used to estimate the population sizes of total heterotrophic
anaerobic bacteria (THB) and PAH-degrading bacteria (PDB) grown
on brewer agar (Fluka, BioChemika, Steinheim, Germany) plates and
R2A plates coated with Phe film, respectively. The positive growth of
THB was based on the presence of a colony on the agar plate, and
that for PDB was identified by the colony surrounded by a clear zone
on the white PAH film, respectively. The plates were placed inside
an anaerobic jar (Becton, Dickinson and Company, Franklin Lakes,
New Jersey, USA) and incubated at 28°C in an incubator (BD240,
Binder, Ulm, Germany) for 4–6 weeks. The population size of
methanogen was enumerated according to MPN method described by Jain et al. (1991) with PBBM medium containing
0.7 g KH2PO4, 0.9 g K2HPO4, 0.9 g NaCl, 0.2 g MgCl2·6H2O,
0.1 g CaCl2·2H2O, 1.0 g NH4Cl, trace mineral solution
(FeCl2·4H2O, 0.009 mg/L; MnCl2·4H2O, 0.004 mg/L; ZnCl2,
0.0014 mg/L; CoCl4·6H2O, 0.001 mg/L; (NH4)6 Mo7O24·4H2O,
0.001 mg/L) 10 mL, DI water 1000 mL. The pH was adjusted
to 7.2. After autoclaving, 10 mL vitamin solution and 0.8 mL
Na2S·9H20 (0.5 mol/L) solution was added into 1000 mL
autoclaved PBBM medium aseptically by injecting the
solution through a 0.25 μm pore size filter. The composition
of vitamin solution (per liter) was: 0.002 g biotin, 0.002 g
folic acid, 0.010 g B6 (pyridoxine) HCl, 0.005 g B1 (thiamine)
HCl, 0.005 g B2 (riboflavin), 0.005 g nicotinic acid, 0.005 g
pantothenic acid, 0.001 g B12 crystalline, 0.005 g PABA
(p-aminobenzoic acid), 0.005 g lipoic acid, DI water
1000 mL. Five-tube MPN method was applied. Cultivation
was performed using 20 mL screw tubes sealed with
butyl-rubber stoppers and aluminum caps, the gas phase
in these sealed tubes was replaced with N2:CO2 (80:20, V/V).
These tubes were incubated at 37°C for 30 days. Methane
gas production in the gas phase of each tube was measured
for the detection of methanogens. Methane gas determination
followed the method described in the following paragraph.
The microbial activity under PAH stress was evaluated by
a modified electron-transport system (ETS) method (Li et al., 2009)
with 2-(p-iodophenyl)-3-(p-nitrophenyl)-5-phenyltetrazoliumchloride
(INT) as the electron acceptor. The detailed method has been
described in another paper (Li et al., 2011). The PAH-stress was also
produced by adding 20 μL (5000 mg/L in distilled acetone) mixed PAHs
comprising Fl, Phe, Flua and Pyr.
The concentrations of different electron acceptors, includ−
ing Fe(III), Mn(IV), sulfate (SO2−
4 ) and nitrate (NO3) were measured according to Lovley and Li (Lovley and Phillips, 1986; Li
et al., 2009).
The gas (10 μL) in the headspace of each Quickfit conical
flask or MPN tube was sampled by an air-tight syringe, and the
concentrations of CH4 and CO2 were determined by a Hewlett
Packard 5890A gas chromatography with a thermal conductance detector (GC-TCD), equipped with a Porapak Q column
(80–100 mesh; 6′ × 1/8″; stainless steel) (Alltech, Chicago,
Illinois, USA). The chromatographic conditions were as follows:
carrier gas: helium (20 mL/min); reference gas: helium (30 mL/
min); injector and detector temperature: 80°C. The oven
temperature program was as follows: held at 50°C for 2.5 min.
Oxidation–reduction potential (ORP) and pH values were
measured with ORP & pH meter (TPS WP-81, Brisbane, Australia)
by inserting the probe into the flask immediately after moving
off its septum and sealing with parafilm.
1.8. Biodegradation kinetics
The biodegradation of all four PAHs was described by the first
order kinetics (Chen et al., 2008):
C ¼ C 0 e−kt
ð1Þ
where, C0 (μg/g) is the concentration of PAH at time zero, C (μg/g)
is the concentration of PAH after subtracting the abiotic loss at
time t (day) and k is the first order rate constant (biodegradation
rate in the present study) of the reaction.
t1/2, the half life for each PAH compound, was calculated by
the formula:
t 1=2 ¼ ðln 2Þ=k:
ð2Þ
1.9. Statistical analyses
A two-way multiple analysis of covariance (MANCOVA)
method at p ≤ 0.05, with NaHCO3 amendment and inoculums
as two fixed factors, biodegradation time as the covariate,
the lnC values of Fl, Phe, Flua and Pyr as the multivariates,
was used to test any significant differences from NaHCO3 and
inoculums on the biodegradation rate (k). Their effects on
other parameters, including microbial population sizes, ETS,
electron acceptors and anaerobic gases were analyzed by a
two-way analysis of covariance (ANCOVA) method at p ≤ 0.05,
with NaHCO3 amendment and inoculums as two fixed factors,
biodegradation time as the covariate, ln(parameter value) as
the independent variable. All statistical analyses were conducted using the software of SPSS 16.0 (SPSS Inc., Chicago, IL,
USA).
2. Results
2.1. PAH biodegradation
The anaerobic biodegradation of the four PAHs all followed
the same temporal pattern (Fig. 1). The abiotic losses of the
four PAHs were relatively few, ranging from 6% to 14%. The
biodegradation kinetics was best fitted by the first-order rate
151
J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 30 (2 0 1 5 ) 1 4 8–1 5 6
SC
IB+NaHCO3
IB
EB
10
Residual Phe concentration (µg/g)
Residual Fl concentration (µg/g)
10
EB+NaHCO3
8
6
4
2
0
0
25
50
75
100
8
6
4
2
0
125
0
25
Biodegradation time (day)
Residual Pyr concentration (µg/g)
10
Residual Flua concentration (µg/g)
50
75
100
125
Biodegradation time (day)
8
6
4
10
8
6
4
2
2
0
0
25
50
75
100
0
125
25
0
Biodegradation time (day)
50
75
100
125
Biodegradation time (day)
Fig. 1 – Polycyclic aromatic hydrocarbon (PAH) biodegradation and the best fit kinetic models under methanogenic condition
(mean and standard deviation of triplicates are shown; the lines show the best fit kinetic models C = C0e−kt; SC: sterile control;
IB: with indigenous bacteria; IB + NaHCO3: with indigenous bacteria and NaHCO3 addition; EB: with enriched consortium
addition and EB + NaHCO3: with enriched consortium and NaHCO3 addition).
model, with regression coefficients (r2) varying from 0.8319 to
0.9895 (p < 0.05). The biodegradation rates and the half-lives
of the four PAHs are shown in Table 1. The half lives of the
3-ring PAHs varied between 29.8 and 43.1 days, while the
respective values of the 4-ring PAHs were 59.8–86.6 days.
These findings indicated that the low molecular weight PAHs
(Fl, Phe) had faster biodegradation than the high molecular
weight ones (Flua, Pyr).
According to MANCOVA analysis results, the inoculation
of the enriched PAH-degrading consortium significantly enhanced the biodegradation rates of all four PAHs, with F =
14.916, p = 0.001 for Fl, F = 18.596, p = 0.000 for Phe, F = 11.633,
p = 0.003 for Flua, and F = 5.473, p = 0.030 for Pyr; while the
amendment of NaHCO3 had no significant effect (p > 0.05).
The inoculation of enriched PAH-degrading consortium
had significant effect with half lives shortened by 7–
13 days for 3-ring PAHs and 11–24 days for 4-ring PAHs.
While with the amendment of NaHCO 3 , the anaerobic
biodegradation half lives of PAHs of IB + NaHCO 3 and
EB + NaHCO 3 treatments were either shorten very few
days or even prolonged (Fl) comparing with IB and EB
treatments, respectively.
Table 1 – The first order rate constant (k, day− 1) of PAH degradation, half-lives (t1/2, days) and r2 (correlation coefficient).
Fl
IB
IB+ NaHCO3
EB
EB + NaHCO3
Phe
2
Flua
2
Pyr
2
k
t1/2
r
k
t1/2
r
k
t1/2
r
k
t1/2
r2
0.0166
0.0161
0.0223
0.0233
41.8
43.1
31.1
29.8
0.9659
0.9060
0.9642
0.9424
0.018
0.0185
0.0226
0.0232
38.5
37.5
30.7
29.9
0.9886
0.9895
0.9803
0.9566
0.0087
0.0095
0.0114
0.0116
79.7
73.0
60.8
59.8
0.9692
0.8945
0.9324
0.8319
0.008
0.0095
0.0108
0.0111
86.6
73.0
64.2
62.5
0.9429
0.8987
0.9078
0.9663
152
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S 30 (2 0 1 5 ) 1 48–1 5 6
IB
6
Total heterotrophic bacteria (THB)
IB+NaHCO3
EB
EB+NaHCO3
Methanogen
8
5
4
3
2
7
log(MPN)
log(MPN)
5
log(MPN)
PAH-degrading bacteria (PDB)
6
6
4
3
2
5
1
0
1
0
25
50
75
100
125
4
0
Biodegradation time (day)
25
50
75
100
125
0
0
25
50
75
100
125
Biodegradation time (day)
Biodegradation time (day)
Fig. 2 – Population sizes of heterotrophic anaerobic bacteria (THB), methanogen and PAH-degrading bacteria (PDB) during
polycyclic aromatic hydrocarbon (PAH) biodegradation (mean and standard deviation of triplicates are shown).
about one order of magnitude higher than those of IB and
IB + NaHCO3 (Fig. 2). The population sizes of the PDB were
significantly enhanced with the inoculation of the enriched
consortium (Table 2). The sizes of treatments EB and EB +
NaHCO3 declined from 106 MPN/mL slurry at day 0 to about
104 MPN/mL slurry at day 25, then kept at 103–104 MPN/mL
slurry from day 50 to day 125. These values were still higher
than those in the treatments without inoculums. However,
the amendment of NaHCO3 had no significant effect on the
population sizes of PDB (Table 2).
PAH biodegradation rates of all the four treatments with
amendment of NaHCO3 were relative lower than those of
nitrate, sulfate and Fe(III) amendments according to our
previous published or un-published results (Li et al., 2010).
However, compared to other studies on PAH biodegradation
under methanogenic condition, the mangrove sediment
slurry used in the present experiment demonstrate much
higher biodegradation ability. For example, Kraig (2000) found
that under methanogenic condition low molecular weight
PAHs were biodegraded, but high molecular weight ones did
not decreased, even two six-ring PAHs increased in concentration almost 50%. Genthner et al. (1997) detected active
methanogenesis in creosote-contaminated sediment but only
limited degradation of a few PAHs was observed and none of
the 4, 5-ring PAHs was degraded.
2.3. Microbial activity under PAH stress
The inoculation of enriched consortium had significant
effect on ETS activity, but the amendment of NaHCO3 had
no significant effect (Table 2). EB and EB + NaHCO3 treatments always maintained higher microbial activities (100–
160 μg/(mL·hr) INTF) compared to the treatments without
inoculums. They had comparable trends, with slight decreases
from day 0 to day 25, then some increases until day 75, followed
by declines thereafter. In the treatments without inoculums,
IB and IB + NaHCO3, ETS activities were very low in the first
50 days, reaching the peak at day 75 then declined towards to
the end of experiment (Fig. 3).
2.2. Microbial population sizes
The population sizes of THB, methanogen and PDB during
the biodegradation period are shown in Fig. 2. THB had relative stable population sizes for all treatments (ranged from
103 to 104 MPN/mL slurry), and the inoculation of enriched
consortium significantly increased THB population size, especially at the beginning period, but NaHCO3 amendment had
no significant effect according to ANCOVA analysis (Table 2).
Large population sizes of the methanogen were found in all
treatments, ranging from 106 to 108 MPN/mL slurry (Fig. 2).
Similar to THB, the inoculation of enriched consortium also
significantly increased the population size of methanogen
but the amendment of NaHCO3 had no significant effect.
The population sizes of treatments EB and EB + NaHCO3 had
2.4. Electron acceptors
As enough reducing reagent (Na2S) was added in the experimental slurry, Fe(III) and Mn(IV) react with it and form FeS
and MnS, respectively, and almost no Fe(III) and Mn(IV) were
detected during biodegradation. Fig. 4 shows the sulfate
Table 2 – Two-way analysis of covariance (ANCOVA) analysis results showing the effects of NaHCO3 amendments,
inoculation of enriched PAH-degrading consortium on the population sizes of total anaerobic heterotrophic bacteria (THB),
methanogen and PAH-degrading bacteria (PDB), and bacterial activity under PAH stress [electron-transport system (ETS)],
with time as the covariate.
Factors
Bacterial population sizes
THB
NaHCO3
Inoculum
ETS activity
Methanogen
PDB
F
p
F
p
F
p
F
p
0.020
17.977
0.890
0.000
0.842
41.175
0.370
0.000
0.011
75.996
0.918
0.000
0.086
101.784
0.772
0.000
153
J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 30 (2 0 1 5 ) 1 4 8–1 5 6
IB
IB+NaHCO3
EB
EB+NaHCO3
NaHCO3 whatever for the whole biodegradation and the time
after day 50.
For nitrate concentration, similar temporal trends among
all treatments were displayed and the result of two-way
ANCOVA indicated that both the inoculation of enriched
consortium and the NaHCO3 amendment had no significant
effects on the utilization of nitrate (Table 3). The nitrate
concentrations of the experimental treatments reached their
peak values at Day 50 because some water soluble nitrate
was released from sediment due to continuous shaking and
microbial activity. The values then declined rapidly until day
100 and remained almost unchanged till day 125.
INTF (mg/(mL.hr))
160
120
80
40
0
0
25
50
75
100
125
2.5. Anaerobic gases
Biodegradation time (day)
Fig. 3 – Microbial activities of PAH-degrading microbes
during polycyclic aromatic hydrocarbon (PAH)
biodegradation (mean and standard deviation of triplicates
are shown).
concentration, with peak concentrations of all the treatments
at day 50, about 1500 mg/L slurry for IB and IB + NaHCO3
treatments, and around 700 mg/L slurry for EB and EB +
NaHCO3 treatments. The lower peak values in the treatments
with inoculums indicated faster utilization rate of sulfate
than without inoculums. These results also suggested that
the sulfate concentrations in the first 50 days were due to
the combined effect of both utilization by anaerobic microbes
and the release of sulfate from sediment matrix. After day
50, microbial utilization became the dominant activity. The
effects of the inoculums and NaHCO3 amendment on sulfate
concentration were examined under two periods, the whole
experimental period (0–125 days) and after day 50 (50–125 days),
using the two-way ANCOVA analysis. The results showed that
the inoculums had significant effect on the utilization of sulfate
after day 50, but not for the whole experimental period (Table 3).
No significant effects were detected with the amendment of
IB
The temporal changes of CH4 gas were similar between IB and
IB + NaHCO3, as well as between EB and EB + NaHCO3 (Fig. 5).
According to two-way ANCOVA results, the amendment of
NaHCO3 had no significant effect on the residual concentration of CH4 gas (p > 0.05) but significantly higher amounts of
CH4 were found in the treatments with inoculums during the
biodegradation period (F = 173.782, p = 0.000). More and more
CH4 gas was detected in the headspace as time proceeded,
with 0 at day 0, and about 0.67 mmol per culture flask at day
125 for EB and EB + NaHCO3 treatments. The treatments IB
and IB + NaHCO3 showed relative low CH4 gas production,
around 0.21 mmol per culture flask at day 50 and then
remained from 0.06 to 0.16 mmol per culture flask until the
end of the experiment (Fig. 5).
The residual CO2 gas in the flask was mainly influenced
by two factors, the final production of anaerobic respiration
and the electron acceptor utilized by methanogens. With the
same initial CO2 concentration, the flask with less residual
CO2 concentration indicates it has higher utilization rate by
methanogens. Both the inoculums and the amendment of
NaHCO3 had significant effects on the residual gas in flasks
with F = 4.932, p = 0.042 for inoculums and F = 10.798, p =
0.004 for NaHCO3, respectively. Fig. 5 shows that with the
amendment of NaHCO3, the treatments IB + NaHCO3 and
EB + NaHCO3 had significant higher initial CO2 gas concentration (0.65 mmol per flask) in the headspace at the
IB+NaHCO3
EB
EB+NaHCO3
Nitrate concentration (mg/L)
Sulfate concentration (mg/L)
1500
1200
900
600
300
0
0
25
50
75
100
Biodegradation time (day)
125
50
40
30
20
10
0
0
25
50
75
100
125
Biodegradation time (day)
Fig. 4 – Electron acceptor concentrations in the slurry during polycyclic aromatic hydrocarbon (PAH) biodegradation (mean and
standard deviation of triplicates are shown).
154
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S 30 (2 0 1 5 ) 1 48–1 5 6
Table 3 – Two-way analysis of covariance (ANCOVA)
analysis results showing the effects of NaHCO3
amendment and inoculation of enriched PAH-degrading
microbial consortium on the concentrations of electron
acceptors (nitrate and sulfate) with time as the covariate.
Factors
Electron acceptors
Nitrate
NaHCO3
Inoculum
Sulfate
(0–125 days)
Sulfate
(50–125 days)
F
p
F
p
F
p
0.038
0.051
0.847
0.823
0.000
3.161
0.994
0.091
0.001
53.000
0.973
0.000
sampling time. The addition of NaHCO3 had relative lower pH
values compared to other treatments (Fig. 6).
ORP values showed some decreases as biodegradation
proceeded but the decrease was relatively small. ORP values
declined from − 280 mV to around − 330 mV (Fig. 6). Both the
inoculation of enriched consortium and NaHCO3 amendment
had no significant effects on ORP changes according to ANCOVA
analysis (p > 0.05).
3. Discussion
3.1. Effect of NaHCO3 amendment on PAH-degrading ability
beginning time. The CO2 gas of EB + NaHCO3 treatment had a
rapid decrease from day 0 to day 100, and kept at a similar
level till day 125. However, the CO2 gas of IB + NaHCO3
treatment did not change so much until day 75, followed by
a sharp decline (Fig. 5). On the other hand, IB and EB
treatments showed different trends with IB + NaHCO3 and
EB + NaHCO3 treatments, their CO2 gas reached peak values at
day 50, followed by a marked decrease at day 75, then kept at
similar values till the end of the experiment. The peak value
of EB treatment was more than two times higher than that of
IB treatment, and always had higher CO2 gas concentration
until day 125.
2.6. pH and ORP
The pH values in all treatments decreased from about 7.0
to 5.0–6.0 with the increase of biodegradation time (Fig. 6).
At the same sampling date, IB treatment showed the highest
pH values. Both the inoculums of enriched consortium and
NaHCO3 amendment had significant effects on the change
of pH, with F = 16.350, p = 0.001, and F = 13.941, p = 0.001,
respectively. The inoculation of enriched consortium showed
lower pH values than the treatments without it at the same
IB
The amendment of NaHCO3 did not have any statistically
significant on the biodegradation of PAHs and other parameters except CO2 gas in the headspace of experimental flasks.
These results suggested that NaHCO3 could not improve
PAH-degrading ability when added as electron acceptor (CO2
from NaHCO3) for methanogens in the mangrove sediment
with high concentrations of other electron acceptors. Because
methanogenic process is known to be the least exergonic
microbial reaction that produces only a limited amount of
energy when compared to aerobic or other anaerobic respiration processes (Schink, 1997). When other efficient terminal
electron acceptors, such as sulfate, nitrate and oxidized forms
of metals, are present in the environments, methanogenesis
occurs in a very low rate (Zehnder, 1988). In the present study,
other electron acceptors, including sulfate, nitrate, Fe(III) and
Mn(IV), were present in different amounts. All of them are
more preferred by anaerobes than CO2. What is more, sulfate
was the dominant electron acceptor from initial till the end of
the experiment (Fig. 4), and it could be an important electron
acceptor source for anaerobes. Another possible reason was
that with large population sizes of anaerobic bacteria and
methanogens (Fig. 2), large amount of CO2 gas was produced
IB+NaHCO3
EB
0.8
Production of CO2 (mmol/culture flask)
Production of CH4 (mmol/culture flask)
0.8
0.6
0.4
0.2
0.0
EB+NaHCO3
0
25
50
75
100
Biodegradation time (day)
125
0.6
0.4
0.2
0.0
0
25
50
75
100
125
Biodegradation time (day)
Fig. 5 – Anaerobic gas production during polycyclic aromatic hydrocarbon (PAH) biodegradation (mean and standard deviation
of triplicates are shown; IB: with indigenous bacteria; IB + NaHCO3: with indigenous bacteria and NaHCO3 addition; EB: with
enriched consortium addition and EB + NaHCO3: with enriched consortium and NaHCO3 addition).
155
J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 30 (2 0 1 5 ) 1 4 8–1 5 6
IB
IB+NaHCO3
EB
EB+NaHCO3
-250
7.0
ORP (mV)
pH
6.5
6.0
-300
5.5
-350
5.0
4.5
0
25
50
75
100
125
Biodegradation time (day)
0
25
50
75
100
125
Biodegradation time (day)
Fig. 6 – pH and oxidation-reduction potential (ORP) in the slurry during polycyclic aromatic hydrocarbon (PAH) biodegradation
(mean and standard deviation of triplicates are shown).
in a very short time (Fig. 5) and it can provide enough electron
acceptor for the respiration of methanogens.
3.2. Effect of enriched PAH-degrading microbial consortium on
PAH-degrading ability with NaHCO3 amendment
The positive effect of enriched PAH-degrading microbial consortium had already been demonstrated in previous studies
(Tam and Wong, 2008; Li et al., 2011), and this effect was also
observed in the present study. The biodegradation rates of
PAHs, especially for 4-ring PAHs were significantly enhanced
by the inoculation of enriched PAH-degrading consortium.
The enriched consortium had higher microbial activity under
PAH-stress and larger population sizes of THB, methanogen
and PDB compared to IB and IB + NaHCO3 treatments. The
inoculation of enriched consortium caused a significantly faster
utilization of sulfate than other electron acceptors, suggesting
that the consortium was sulfate-dependent. Besides, the treatments with inoculums showed significantly higher CH4 concentration in the headspace, further suggesting a higher efficiency
and more completeness of the decomposition of PAHs and other
organic matter in the slurry.
3.3. Influence of pH and ORP
The decrease of pH value was due to the production of some
anaerobic products, including CO2 gas, H2S and simple
organic acids, during anaerobic biodegradation (Levett, 1990;
Jain et al., 1991). Additionally, NaHCO3 amendment also
caused a lower pH value, which could be explained by the
following equilibrium in slurry system: HCO−3 = H+ + CO23 −. pH
values decreased to near 5.0 at the end of experiment, but no
significant correlation was found between pH and microbial
activity or the population size of total anaerobic heterotrophic bacteria according to Pearson correlation coefficient
analysis (2-tailed test), suggesting that the microbes in the
mangrove sediment slurry had a good adaptability to lower
pH range.
ORP values in the present experiment decreased to some
extent but not so dramatically as the Fe-reducing or Mnreducing conditions (Li et al., 2010, 2011), probably because
the initial ORP values were already very low (−280 mV), much
lower than those initial values in Fe-reducing or Mn-reducing
conditions, which were 120–130 mV. According to Pearson
correlation coefficient analysis (2-tailed test), no significant
correlation was found between ORP and microbial activity or
the population size of total anaerobic heterotrophic bacteria,
indicating that the change of ORP had no significant effect
on the anaerobic bacteria. Similar results were observed by
previous publications (Onderdonk et al., 1976; Chang et al.,
2008). For instance, Chang et al. (2008) reported that ORP value
decreased from an initial − 310 mV to a steady range of − 400 to
−420 mV between days 20 and 50 of the incubation period
under methanogenic condition, but no significant relationship was found between ORP value and bacteria activity.
4. Conclusions
On the basis of the results we conclude that: (1) NaHCO3
amendment did not improve PAH-degrading ability in the
mangrove sediment. The probable reason could be that concentrations of other electron acceptors in mangrove sediment
are high, and enough CO2 was produced because of the
activity of anaerobes even without adding NaHCO3. (2) The
inoculation of the enriched PAH-degrading consortium supported higher microbial activity and larger population sizes
of the PAH-degrading bacteria than the treatments without
inoculums, leading to more rapid and complete biodegradation with the half lives of the target PAHs being shortened
significantly. (3) The pH value decreased during anaerobic
biodegradation because of the production of some anaerobic
156
J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S 30 (2 0 1 5 ) 1 48–1 5 6
products, including CO2 gas, H2S and simple organic acids.
However, the microbes in the mangrove sediment had a good
adaptability to lower pH range. (4) ORP values decreased to
some extent but its change had no significant effect on the
anaerobic bacteria in mangrove sediment.
Acknowledgments
This research was supported by a grant from the Strategic
Research Grant of the City University of Hong Kong
(No. 7002847) and the National Science Foundation of China
(No. 41101487). The authors would like to thank Dr. Qingtan Gao
and Dr. Guangcheng Chen for their assistance in sediment
sampling.
REFERENCES
Ambrosoli, R., Petruzzelli, L., Minati, J.L., Marsan, F.A., 2005.
Anaerobic PAH degradation in soil by a mixed bacterial
consortium under denitrifying conditions. Chemosphere 60
(9), 1231–1236.
Chang, B.V., Chang, S.W., Yuan, S.Y., 2003. Anaerobic degradation
of polycyclic aromatic hydrocarbons in sludge. Adv. Environ.
Res. 7 (3), 623–628.
Chang, B.V., Chang, I.T., Yuan, S.Y., 2008. Anaerobic degradation
of phenanthrene and pyrene in mangrove sediment. Bull.
Environ. Contam. Toxicol. 80 (2), 145–149.
Chen, J.L., Wong, M.H., Wong, Y.S., Tam, N.F.Y., 2008.
Multi-factors on biodegradation kinetics of polycyclic
aromatic hydrocarbons (PAHs) by Sphingomonas sp., a
bacterial strain isolated from mangrove sediment. Mar.
Pollut. Bull. 57 (6–12), 695–702.
Coates, J.D., Anderson, R.T., Woodward, J.C., Phillips, J.C., Lovely,
D.R., 1996. Anaerobic hydrocarbon degradation in
petroleum-contaminated harbor sediments under
sulphate-reducing and artificially imposed iron-reducing
conditions. Environ. Sci. Technol. 30 (9), 2784–2789.
Genthner, B.R.S., Townsend, G.T., Lantz, S.E., Mueller, J.G., 1997.
Persistence of polycyclic aromatic hydrocarbon components
of creosote under anaerobic enrichment conditions. Arch.
Environ. Contam. Toxicol. 32 (1), 99–105.
Hutchins, S.R., Sewell, G.W., Kovacs, D.A., Smith, G.A., 1991.
Biodegradation of aromatic hydrocarbons by aquifer
microorganisms under denitrifying conditions. Environ. Sci.
Technol. 25 (1), 68–76.
Jain, M.K., Zeikus, J.G., Bhatnagar, L., 1991. Methanogens. In:
Levett, P.N. (Ed.), Anaerobic Microbiology: A Practical
Approach. Oxford University Press, Oxford, pp. 223–245.
Ke, L., Yu, K.S.H., Wong, Y.S., Tam, N.F.Y., 2005. Spatial and
vertical distribution of polycyclic aromatic hydrocarbons in
mangrove sediments. Sci. Total Environ. 340 (1–3), 177–187.
Kraig, J., 2000. Anaerobic Biodegradation of Polycyclic Aromatic
Hydrocarbons in Dredged Material. (PhD. thesis). University of
Utah.
Levett, P.N., 1990. Anaerobic Bacteria: A Functional Biology. Open
University Press, Milton Keynes, UK, pp. 15–26.
Li, C.H., Zhou, H.W., Wong, Y.S., Tam, N.F.Y., 2009. Vertical
distribution and anaerobic biodegradation of polycyclic
aromatic hydrocarbons in mangrove sediments in Hong Kong.
South China. Sci. Total Environ. 407 (10), 5772–5779.
Li, C.H., Wong, Y.S., Tam, N.F.Y., 2010. Anaerobic biodegradation
of polycyclic aromatic hydrocarbons with amendment of
iron(III) in mangrove sediment slurry. Bioresour. Technol. 101
(21), 8083–8092.
Li, C.H., Ye, C., Wong, Y.S., Tam, N.F.Y., 2011. Effect of Mn(IV) on
the biodegradation of polycyclic aromatic hydrocarbons under
low-oxygen condition in mangrove sediment slurry. J. Hazard.
Mater. 190 (1–3), 786–793.
Lovley, D.R., Phillips, E.J.P., 1986. Organic matter mineralization
with reduction of ferric iron in anaerobic sediments. Appl.
Environ. Microbiol. 51 (4), 683–689.
MacRae, J.D., Hall, K.J., 1998. Biodegradation of polycyclic aromatic
hydrocarbons (PAH) in marine sediments under denitrifying
conditions. Water Sci. Technol. 38 (11), 177–185.
Nieman, J.K.C., Sims, R.C., McLean, J.E., Sims, J.L., Sorensen, D.L.,
2001. Fate of pyrene in contaminated soil amended with
alternate electron acceptors. Chemosphere 44 (8), 1265–1271.
Onderdonk, A.B., Johnston, J., Mayhew, J.W., Gorbach, S.L., 1976.
Effect of dissolved oxygen and Eh and Bacteroides fragilis during
continuous culture. Appl. Environ. Microbiol. 31 (2), 168–172.
Schink, B., 1997. Energetics of syntrophic cooperation in
methanogenic degradation. Microbiol. Mol. Biol. Rev. 61 (2),
262–280.
Tam, N.F.Y., Wong, Y.S., 2008. Effectiveness of bacterial inoculum
and mangrove plants on remediation of sediment contaminated
with polycyclic aromatic hydrocarbons. Mar. Pollut. Bull. 57
(6–12), 716–726.
USEPA (US Environmental Protection Agency), 1993. Provisional
Guidance for Quantitative Risk Assessment of Polycyclic
Aromatic Hydrocarbons, EPA/600/R-93/089.
Zehnder, A.J.B., 1988. Biology of Anaerobic Microorganisms. Wiley,
New York.
Zheng, G.J., Man, B.K.W., Lam, J.C.W., Lam, M.H.W., Lam, P.K.S.,
2002. Distribution and sources of polycyclic aromatic
hydrocarbons in the sediment of a sub-tropical coastal
wetland. Water Res. 36 (6), 1457–1468.
Editorial Board of Journal of Environmental Sciences
Editor-in-Chief
X. Chris Le
University of Alberta, Canada
Associate Editors-in-Chief
Jiuhui Qu
Shu Tao
Nigel Bell
Po-Keung Wong
Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, China
Peking University, China
Imperial College London, UK
The Chinese University of Hong Kong, Hong Kong, China
Editorial Board
Aquatic environment
Baoyu Gao
Shandong University, China
Maohong Fan
University of Wyoming, USA
Chihpin Huang
National Chiao Tung University
Taiwan, China
Ng Wun Jern
Nanyang Environment &
Water Research Institute, Singapore
Clark C. K. Liu
University of Hawaii at Manoa, USA
Hokyong Shon
University of Technology, Sydney, Australia
Zijian Wang
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Zhiwu Wang
The Ohio State University, USA
Yuxiang Wang
Queen’s University, Canada
Min Yang
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Zhifeng Yang
Beijing Normal University, China
Han-Qing Yu
University of Science & Technology of China,
China
Terrestrial environment
Christopher Anderson
Massey University, New Zealand
Zucong Cai
Nanjing Normal University, China
Xinbin Feng
Institute of Geochemistry,
Chinese Academy of Sciences, China
Hongqing Hu
Huazhong Agricultural University, China
Kin-Che Lam
The Chinese University of Hong Kong
Hong Kong, China
Erwin Klumpp
Research Centre Juelich, Agrosphere Institute
Germany
Peijun Li
Institute of Applied Ecology,
Chinese Academy of Sciences, China
Michael Schloter
German Research Center for Environmental Health
Germany
Xuejun Wang
Peking University, China
Lizhong Zhu
Zhejiang University, China
Atmospheric environment
Jianmin Chen
Fudan University, China
Abdelwahid Mellouki
Centre National de la Recherche Scientifique
France
Yujing Mu
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Min Shao
Peking University, China
James Jay Schauer
University of Wisconsin-Madison, USA
Yuesi Wang
Institute of Atmospheric Physics,
Chinese Academy of Sciences, China
Xin Yang
University of Cambridge, UK
Environmental biology
Yong Cai
Florida International University, USA
Henner Hollert
RWTH Aachen University, Germany
Jae-Seong Lee
Sungkyunkwan University, South Korea
Christopher Rensing
University of Copenhagen, Denmark
Bojan Sedmak
National Institute of Biology, Slovenia
Lirong Song
Institute of Hydrobiology,
Chinese Academy of Sciences, China
Chunxia Wang
National Natural Science Foundation of China
Gehong Wei
Northwest A & F University, China
Daqiang Yin
Tongji University, China
Zhongtang Yu
The Ohio State University, USA
Environmental toxicology and health
Jingwen Chen
Dalian University of Technology, China
Jianying Hu
Peking University, China
Guibin Jiang
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Sijin Liu
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Tsuyoshi Nakanishi
Gifu Pharmaceutical University, Japan
Willie Peijnenburg
University of Leiden, The Netherlands
Bingsheng Zhou
Institute of Hydrobiology,
Chinese Academy of Sciences, China
Environmental catalysis and materials
Hong He
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Junhua Li
Tsinghua University, China
Wenfeng Shangguan
Shanghai Jiao Tong University, China
Ralph T. Yang
University of Michigan, USA
Environmental analysis and method
Zongwei Cai
Hong Kong Baptist University,
Hong Kong, China
Jiping Chen
Dalian Institute of Chemical Physics,
Chinese Academy of Sciences, China
Minghui Zheng
Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, China
Municipal solid waste and green chemistry
Pinjing He
Tongji University, China
Editorial office staff
Managing editor
Editors
English editor
Qingcai Feng
Zixuan Wang
Suqin Liu
Catherine Rice (USA)
Kuo Liu
Zhengang Mao
Copyright© Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V. and Science Press. All rights reserved.
JOURNAL OF ENVIRONMENTAL SCIENCES
环境科学学报(英文版)
www.jesc.ac.cn
Aims and scope
Journal of Environmental Sciences is an international academic journal supervised by Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. The journal publishes original, peer-reviewed innovative research and
valuable findings in environmental sciences. The types of articles published are research article, critical review, rapid
communications, and special issues.
The scope of the journal embraces the treatment processes for natural groundwater, municipal, agricultural and industrial
water and wastewaters; physical and chemical methods for limitation of pollutants emission into the atmospheric environment; chemical and biological and phytoremediation of contaminated soil; fate and transport of pollutants in environments;
toxicological effects of terrorist chemical release on the natural environment and human health; development of environmental catalysts and materials.
For subscription to electronic edition
Elsevier is responsible for subscription of the journal. Please subscribe to the journal via http://www.elsevier.com/locate/jes.
For subscription to print edition
China: Please contact the customer service, Science Press, 16 Donghuangchenggen North Street, Beijing 100717, China.
Tel: +86-10-64017032; E-mail: journal@mail.sciencep.com, or the local post office throughout China (domestic postcode:
2-580).
Outside China: Please order the journal from the Elsevier Customer Service Department at the Regional Sales Office
nearest you.
Submission declaration
Submission of the work described has not been published previously (except in the form of an abstract or as part of a
published lecture or academic thesis), that it is not under consideration for publication elsewhere. The publication should
be approved by all authors and tacitly or explicitly by the responsible authorities where the work was carried out. If the
manuscript accepted, it will not be published elsewhere in the same form, in English or in any other language, including
electronically without the written consent of the copyright-holder.
Editorial
Authors should submit manuscript online at http://www.jesc.ac.cn. In case of queries, please contact editorial office, Tel:
+86-10-62920553, E-mail: jesc@rcees.ac.cn. Instruction to authors is available at http://www.jesc.ac.cn.
Journal of Environmental Sciences (Established in 1989)
Volume 30 2015
Supervised by
Chinese Academy of Sciences
Sponsored by
Research Center for Eco-Environmental
Sciences, Chinese Academy of Sciences
Edited by
Editorial Office of Journal of
Published by
Elsevier Limited, The Netherlands
Distributed by
Domestic
North Street, Beijing 100717, China
P. O. Box 2871, Beijing 100085, China
Local Post Offices through China
Foreign
E-mail: jesc@rcees.ac.cn
CN 11-2629/X
Science Press, 16 Donghuangchenggen
Environmental Sciences
Tel: 86-10-62920553; http://www.jesc.ac.cn
Editor-in-chief
Science Press, Beijing, China
X. Chris Le
Domestic postcode: 2-580
Elsevier Limited
http://www.elsevier.com/locate/jes
Printed by
Beijing Beilin Printing House, 100083, China
Domestic price per issue
RMB ¥ 110.00