Subscriber access provided by University of Newcastle, Australia

Article
Synergic Adsorption-Biodegradation by Advance Carrier for
Enhanced Removal of High-strength Nitrogen and Refractory Organics
Muhammad Ahmad, Sitong Liu, Nasir Mahmood, Asif
Mahmood, Muhammad Ali, Maosheng Zheng, and Jinren Ni
ACS Appl. Mater. Interfaces, Just Accepted Manuscript DOI: 10.1021/acsami.7b01251 Publication Date (Web): 29 Mar 2017
Downloaded from http://pubs.acs.org on March 31, 2017

Just Accepted

Just Accepted manuscripts have been peer-reviewed and accepted for publication. They are posted
online prior to technical editing, formatting for publication and author proofing. The American Chemical
Society provides Just Accepted as a free service to the research community to expedite the
dissemination of scientific material as soon as possible after acceptance. Just Accepted manuscripts
appear in full in PDF format accompanied by an HTML abstract. Just Accepted manuscripts have been
fully peer reviewed, but should not be considered the official version of record. They are accessible to all
readers and citable by the Digital Object Identifier (DOI). Just Accepted is an optional service offered
to authors. Therefore, the Just Accepted Web site may not include all articles that will be published
in the journal. After a manuscript is technically edited and formatted, it will be removed from the Just
Accepted Web site and published as an ASAP article. Note that technical editing may introduce minor
changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers
and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors
or consequences arising from the use of information contained in these Just Accepted manuscripts.

ACS Applied Materials & Interfaces is published by the American Chemical Society.
1155 Sixteenth Street N.W., Washington, DC 20036
Published by American Chemical Society. Copyright American Chemical Society.
However, no copyright claim is made to original U.S. Government works, or works
produced by employees of any Commonwealth realm Crown government in the course
of their duties.
Page 1 of 42 ACS Applied Materials & Interfaces

1
2
3
4
5
6
7
8
Synergic Adsorption-Biodegradation by Advance
9
10
11
12 Carrier for Enhanced Removal of High-strength
13
14
15
16 Nitrogen and Refractory Organics
17
18
19
20
21 Muhammad Ahmada, Sitong Liua, Nasir Mahmoodb, Asif Mahmoodc, Muhammad Alid, Maosheng
22
23
Zhenge, and Jinren Nia*
24
25
26 a
27 Department of Environmental Engineering, Peking University; Key Laboratory of Water and
28
29 Sediment Sciences, Ministry of Education, Beijing 100871, China.
30
31 b
32 Key Laboratory for Green Chemical Technology of the Ministry of Education, School of
33
34 Chemical Engineering and Technology, Tianjin University; Collaborative Innovative Center of
35
36 Chemical Science and Engineering (Tianjin), Tianjin 300072, China.
37
38 c
39 Department of Physics, South University of Sciences and Technology, Shenzhen, P.R. China
40
d
41 Water Desalination and Reuse Center (WDRC), Biological and Environmental Science and
42
43 Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal
44
45
46 23955-6900, Saudi Arabia.
47
48 e
Resources and Environmental Research Academy, North China Electric Power University,
49
50 Beijing, China
51
52
53
KEYWORDS: Iron oxide, quinoline, adsorption-biodegradation, Anammox-AOB, Coking
54
55
56 wastewater
57
58
59
60
1
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 2 of 42

1
2
3
Abstract: Coking wastewater contains not only high-strength nitrogen but also toxic bio-
4
5
6 refractory organics. This study presents simultaneous removal of high-strength quinoline, carbon
7
8 and ammonium in coking wastewater by immobilized bacterial communities composed of a
9
10
11
heterotrophic strain Pseudomonas sp. QG6 (hereafter referred as QG6), ammonia-oxidizing
12
13 bacteria (AOB) and anaerobic ammonium oxidation bacteria (Anammox). The bacterial
14
15 immobilization was implemented with help of self-designed porous cubic carrier which created
16
17
18 structured micro-environments including inner layer adaptive of anaerobic bacteria, middle layer
19
20 suitable for co-aggregation of certain aerobic and anaerobic bacteria, and outer layer for
21
22 heterotrophic bacteria. By coating of iron oxide nanoparticles (IONPs) on functional
23
24
25 polyurethane foam (FPUF), the bio-carrier (IONPs-FPUF) could provide a good outer layer
26
27 barrier for absorption and selective treatment of aromatic compounds by QG6, offer a conducive
28
29
environment for anammox in the inner layer, and provided mutualistic environment for AOB in
30
31
32 middle layer. Consequently, simultaneous nitrification and denitrification was reached with
33
34 significant removal up to 322 mgL1 (98%) NH4, 311 mgL1 (99%) NO2 and 633 mgL1 (97%)
35
36
37 total nitrogen (8 mgL1 averaged NO3 concentration was recorded in effluent), accompanied with
38
39 an efficient removal of chemical oxygen demand by 3286 mgL1 (98%) and 350 mgL-1 (100%)
40
41 quinoline. This study provides an alternative way to promote synergic adsorption and
42
43
44 biodegradation with help of modified bio-carrier which is of great potential for treatment of
45
46 wastewater containing high-strength carbon, toxic organic pollutants and nitrogen.
47
48
49
50
51
52
53
54
55
56
57
58
59
60
2
ACS Paragon Plus Environment
Page 3 of 42 ACS Applied Materials & Interfaces

1
2
3
1. Introduction
4
5
6
7 Coking wastewater has been widely noted for its severe pollution to environments. Coking
8
9 wastewater contains various kinds of pollutants primarily composed of phenolics, cyanide,
10
11
12 ammonia, aromatic hydrocarbons, and nitrogen-, oxygen-, and sulfur-containing heterocyclic
13
14 compounds which pose severe threat to humankind.1-3 Quinoline, a heterogeneous aromatic
15
16 compound is a notable organic pollutant among these compounds, which is highly toxic and
17
18
19 mutagenic with very low biodegradability.4-5 Along with the toxic aromatic compounds, coking
20
21 wastewater is also rich in nitrogen containing compounds (e.g. NH4, etc.) which promotes the
22
23 growth of cyanobacteria and algae when coking wastewater is discharged into water bodies,
24
25
26 ultimately leading to eutrophication.6 Therefore, to protect the environment and living organisms,
27
28 there is a dire need to treat toxic coking wastewater prior to discharge into natural resources.
29
30
31
Several strategies have been developed for the treatment of quinoline-containing coking
32
33 wastewater, including physicochemical,7-9 biological,10-11 as well as biochemical,12-13
34
35 electrochemical,14-17 and multistep bio-physicochemical methods.18 Most of these techniques
36
37
38 have been applied separately or integrated in a series of reactors/systems to remove multi-
39
40 pollutants. Although physicochemical methods have been extensively reported with promising
41
42 results19, limited application for nitrogen and carbon removal, high treatment cost, system
43
44
45 complexity, and lack of proper management of toxic end-products are the main shortfalls that
46
47 strongly limit their long-term application.4 Hence, biological methods are still preferable options
48
49
because of the lower energy requirements and special capabilities in treatment and disposal of a
50
51
52 variety of pollutants.20-24
53
54 However, most biological methods based on aerobic autotrophic (e.g. ammonia oxidizing
55
56
57
bacteria AOB), anaerobic autotrophic (e.g. anaerobic ammonium oxidation, anammox) and
58
59
60
3
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 4 of 42

1
2
3
aerobic/anaerobic heterotrophic bacterial communities have been reported as a treatment strategy
4
5
6 but the sensitivity of these bacterial communities for refractory compounds (e.g. quinoline) and
7
8 organic carbon,25-27 is a big hurdle in their efficient nitrogen removal performance. Contrarily,
9
10
11
some functional bacterial strains have been reported that not only have ability to tolerate high
12
13 level of refractory compounds but also can degrade them successfully.20,24 Pseudomonas sp.
14
15 QG6 is one of them with excellent characteristics to efficiently biodegrade quinoline, but it could
16
17
18 only partially convert ammonium to nitrogen gases. Hence, it is imperative to develop a novel
19
20 synergistic adsorptionbiodegradation treatment strategy that perform dual role by efficiently
21
22
23
utilizing the functional adsorbents and bacterial strains for the successful treatment of coking
24
25 wastewater. Synergistic adsorptionbiodegradation treatment strategy can be developed by
26
27 designing a carrier with functional bacteria (QG6, AOB and anammox) immobilized into
28
29
30 selective layers of carrier. Immobilized QG6 bacteria in outer layer will adsorb and biodegrade
31
32 refractory compounds (quinoline) and deliver toxin free wastewater to AOB and anammox in the
33
34
35
inner layers. Hence, this pre-treatment strategy (immobilization of QG6 in outer layer of bacteria)
36
37 would protect the later functional bacterial communities (AOB and anammox) from the life-
38
39 threatening effects by refractory compounds and organic carbon.
40
41
42 Various traditional adsorbents such as fibrous silicates, Patagonian assonate, clay oxides,
43
44 kaolinite and montmorillonite, activated carbon, and bagasse fly ash, etc., have been investigated
45
46 for quinoline adsorption.28-31 In spite of versatile advantages of porosity, their desorption
47
48
49 capacity hindered their real applications as a quinoline adsorbents. In contrast to traditional
50
51 adsorbents, engineered structured-nanomaterials have received more attention due to their high
52
53
surface area, easy and rapid adsorption-desorption rates.32-33 Among these smart nanomaterials,
54
55
56 iron oxide nanoparticles (IONPs) and their composite has raised global attention due to unique
57
58
59
60
4
ACS Paragon Plus Environment
Page 5 of 42 ACS Applied Materials & Interfaces

1
2
3
and fascinating features such as high surface area and adsorption capabilities relative to other
4
5
6 nanomaterials.34-36 However, IONPs have never been utilized as synergic adsorption-
7
8 biodegradation platform for functional bacterial communities growth and for the effective coking
9
10
11
wastewater treatment. For effective bacterial propagation, the IONPs must be hybridized with a
12
13 carrier having micro-characteristics (e.g. functional polyurethane foam, FPUF). This carrier will
14
15 provide niche for the growth of bacterial communities that cannot be provided by IONPs alone.
16
17
18 Therefore, combining micro-nano structured IONPs-FPUF together with immobilization of
19
20 functional bacteria could provide the required novel synergistic adsorptionbiodegradation
21
22
23
treatment strategy for coking wastewater treatment.
24
25 To achieve the best treatment protocol for coking wastewater, we combine the aforementioned
26
27 functional bacteria in a single carrier for high-efficient treatment of coking wastewater
28
29
30 containing high-strength toxic organics and nitrogen (Scheme 1). By coating IONPs on FPUF
31
32 and further functionalizing with biotin, the synthesized IONPs-FPUF created excellent micro-
33
34 environments friendly to synergy of QG6, ammonia-oxidizing bacteria AOB and anammox,
35
36
37 which greatly enhanced the simultaneous removal of quinoline, carbonaceous material and
38
39 ammonium.
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
5
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 6 of 42

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29 Scheme 1. Schematic illustration of IONPs-FPUF design and distribution of various bacterial
30
31
32 communities; their working principal towards coking wastewater treatment.
33
34 2. Experimental Methods
35
36
37
38
2.1. Carrier synthesis and bacterial immobilization
39
40 2.1.1. Synthesis of FPUF.
41
42 Functional Polyurethane Foam (FPUF), which has been previously designed by our research
43
44
45 group (China Patent. 2005. CN1587106A) for the particular aim to create micro-environments
46
47 for the subsequent growth of the multi-bacterial communities (aerobic and anaerobic). The
48
49 porosity of the FPUF carrier was fashioned with a particular aim to inhabit the anaerobic
50
51
52 bacterial communities in deep layers of the carrier where all bacterial communities could easily
53
54 propagate their colonies. Similarly, the FPUF has been functionalized with additional groups
55
56 which could maximize the adhesion of the bacterial communities (Table S1). By taking these
57
58
59
60
6
ACS Paragon Plus Environment
Page 7 of 42 ACS Applied Materials & Interfaces

1
2
3
advantages of the uniquely developed FPUF carrier, we further modified it for ultimate purpose
4
5
6 of enhancing simultaneous adsorption-biodegradation.
7
8 2.1.1. Synthesis of IONPs. IONPs were prepared by using a solvothermal method. Typically, 1 g
9
10
11
iron acetate, 15 mL NH4OH, 0.5 mL oleic acid, and 5 mL oleylamine were mixed for 1 h with
12
13 the assistance of a magnetic stirrer. Subsequently, this mixture was transferred to a 25 mL
14
15 Teflon-lined autoclave and the reaction was carried out at 200 C for 12 h. Finally, the solid
16
17
18 product was obtained by centrifugation and was washed thrice with water and ethanol. The
19
20 product was then dried at 70 C in a vacuum oven for 6 h.
21
22 2.1.2. Synthesis of IONPs-FPUFS. The IONPs-FPUF was fabricated through wet chemistry.
23
24
25 Initially, a 15 mm cube of FPUF carrier which is self-made patented and have been successfully
26
27 applied by our research group11 was cut and mounted in the IONPs solution (20 mg mL1) that
28
29
was mechanically stirred for one week at progressive mixing speeds and temperatures ranging
30
31
32 from 80200 rpm and 37200 C, respectively, to ensure homogeneous distribution and better
33
34 adhesion of the IONPs. Furthermore, biocompatibility was conferred to the IONPs-FPUF by
35
36
37 coating with biotin.
38
39 2.1.3. Bacterial strains. The strain QG6 was discovered and isolated by our research group.37
40
41 The sequence data for the strain QG6 has been deposited in the NCBI database under the
42
43
44 accession number EF079075. The strain is also preserved in the Chinese Culture Collection
45
46 Committee General Microbiology Centre under the accession number CGMCC No. 6813. The
47
48 seed sludge of anammox and AOB bacteria was collected from the Shiyan Reservoir in
49
50
51 Shenzhen City, located in southern China and was pre-enriched in a 5 L reactor in our
52
53 laboratory.38-39 Anammox bacteria were immobilized on the IONPs-FPUF carrier.
54
55
56
Approximately 25 mL of enriched anammox biomass was inoculated into the reactor using a
57
58
59
60
7
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 8 of 42

1
2
3
syringe. Initially, the reactor was operated for 50 days to stabilize the anammox process and to
4
5
6 establish an anammox bacterial biofilm on the carriers. Subsequently, the QG6 bacterial strain
7
8 and AOB were inoculated into the reactor by using a syringe containing 25 mL of biomass with
9
10
11
the aim to biodegrade quinoline and convert NH4 into NO2 by the respective species.
12
13 2.1.4. Experiment set-up and reactor operation. The whole experiment was performed in
14
15 cylindrical Plexiglas reactor with an effective volume of 3 L filled with the IONPs-FPUF carriers
16
17
18 (15 mm in size, filling ratio 40%) and was operated for 200 days for coking wastewater
19
20 treatment. Whereas quinoline adsorption mechanisms in reactor was authenticated by separate
21
22 batch adsorption experiment in Erlenmeyer glass flasks (250 mL) with three different types of
23
24
25 carriers namely FPUF, IONPs-FPUF, and IONPs-FPUF@QG6 (the carrier with immobilized and
26
27 developed biofilm of QG6 bacteria). The reactor was fed with synthetic wastewater and detail is
28
29
given in Table S1. The quinoline containing wastewater was initiated after 50 days of stable
30
31
32 reactor operation and supplied continuously for 200 days. The pollutants (NH4, NO2, quinoline
33
34 and carbon) were provided separately in the influent throughout the reactor operation (The detail
35
36
37 description of the synthetic wastewater has been provided in supporting information).
38
39 2.2. Adsorption experiments
40
41 2.2.1. Adsorption experiments. For adsorption experiments, 1g of 15 mm FPUF, IONPs-FPUF,
42
43
44 and IONPs-FPUF@QG6 were shaken at 150 rpm with 200 mL of coking wastewater. For the
45
46 adsorption kinetics experiments, batch experiment was performed at fixed quinoline
47
48 concentration (50 mgL-1) with 1g of 15 mm FPUF, IONPs-FPUF, and IONPs-FPUF@QG6 in
49
50
51 separate flasks (250 mL). Samples were taken out at specified time intervals i.e. 0, 15, 30, 60,
52
53 120, 240, 480, 1440, 2100 and 2800 min. For adsorption isotherm experiments, initial
54
55
56
concentration of quinoline was varied from 25 to 350 mgL-1. All experiments were conducted at
57
58
59
60
8
ACS Paragon Plus Environment
Page 9 of 42 ACS Applied Materials & Interfaces

1
2
3
7.8 pH and 37 C because of the suitability of these conditions for growth of anammox and AOB
4
5
6 bacteria. 0.1 M NaOH and HCl solution was used to adjust the pH (7.8) of quinoline solution.
7
8 All experiments were conducted in triplicate and results are expressed as meanS.D. Samples
9
10
11
were withdrawn after 4 h (HRT for reactor) and the concentration of remaining quinoline was
12
13 determined (See schematic illustration in Figure S1).
14
15 To determine the left over quinoline concentration in solution, centrifuged the solution at
16
17
18 10,000 rpm and the supernatant was analyzed using high performance liquid chromatography
19
20 (HPLC). The adsorption capacity and removal efficiency were calculated by applying equation 1
21
22 and 2 respectively.40-42
23
24
(  )
25 q = (1)
26 
27
28 (  )
29 R= 100 (2)

30
31
32 Here, Ci and Ce are the initial and final concentrations of quinoline (mgL1), qe is the adsorption
33
34 capacity (mg g-1), R is the removal efficiency, W (g) is the dry weight of the adsorbent, and V is
35
36
37 the volume (L) of the quinoline solution used.43
38
39
40 2.2.2. Quantitative analysis. Samples for quantitative analysis were collected twice per week
41
42 from reactor. Quantitative analysis of quinoline (effluent concentration) was performed by using
43
44
45
an HPLC system (Shimadzu LC10ADVP, SPD10AVP UVVis Detector; Rheodyne 7725i
46
47 manual injector; Diamonsil C18 reverse-phase column, 250 mm, 4.6 mm, 5 mm).
48
49 Methanol/water (volume ratio of 4:1) was used as the mobile phase at a flow rate of 1.0 mL
50
51
52 min1. The microbial growth of QG6 was monitored by measuring the optical density at 600 nm
53
54 (OD600) and the concentrations of ammonium, nitrate, and nitrite were analyzed using a UV-
55
56 Visible (UV-Vis) spectrophotometer (UV-1750, SHIMADZU, Japan). The pH and dissolved
57
58
59
60
9
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 10 of 42

1
2
3
oxygen (DO) were measured by using digital pH and DO meters, respectively (HACH, USA).
4
5
6 All remaining measurements and methods used in this study were adopted from the protocol
7
8 described in the Standard Methods for Examination of Water and Wastewater.
9
10
11
2.2.3. Microscopic analysis. For scanning electron microscope (SEM) and energy dispersive x-
12
13 ray (EDX) analysis of samples from reactor, all of the samples were fixed with 2.5%
14
15 glutaraldehyde in 0.1 M phosphate and dehydrated with increasing concentrations of ethanol, i.e.
16
17
18 50, 70, 80, 90, and 100%. After dehydration, the samples were dried by critical point drying or
19
20 with hexamethyldisilizane (HMDS) and finally observed under SEM (Nova 200 NanoLab, USA).
21
22 The topographic images were captured using multimode atomic force microscopic (AFM, Burker
23
24
25 Nano, USA). Samples for fluorescence in-situ hybridization (FISH) analysis were fixed in 4%
26
27 paraformaldehyde and dehydrated with increasing concentrations of ethanol. The 4,6-diamidino-
28
29
2-phenylindole (DAPI) and the oligonucleotide probes Pla46, AMX820, NmV and NSO190
30
31
32 were used for detection of all bacteria, planctomycetes, anammox, and AOB respectively; a
33
34 confocal laser scanning microscope (A1R-si, Nikon) was used for the FISH analysis (probes
35
36
37 details is provided in Table S2).
38
39
40 3. Results and Discussion
41
42
43 3.1. Characterizations of IONPs-FPUF.
44
45 3.1.1 Refinement of the microstructure. IONPs were coated over FPUF carrier to play a dual
46
47
48 role i.e. adsorption-biodegradation. Hence the efficient coating was confirmed by using SEM and
49
50 EDX analysis. Large sized pores of FPUF (Figure 1a), were reduced to relatively smaller pores
51
52
after coating of IONPs on FPUF, which confirmed successful and uniform packing of the IONPs
53
54
55 on FPUF (Figure 1b). Coating of IONPs on FPUF improved porosity (Table S4) that ultimately
56
57 increased the water holding capacity of FPUF carrier that played a vital role for proper contact of
58
59
60
10
ACS Paragon Plus Environment
Page 11 of 42 ACS Applied Materials & Interfaces

1
2
3
wastewater with bacteria biofilm which could be clearly visualized by comparing structures of
4
5
6 FPUF and IONPs-FPUF (Figure 1a, b). Moreover, after coating with the IONPs, the IONPs-
7
8 FPUF still possessed interconnected pores, and was wettable and permeable with an efficient
9
10
11
mass diffusion capabilities. These properties helped to stimulate the growth of QG6, AOB and
12
13 anammox by providing favorable environments for their mutualistic interactions and dynamics.
14
15 To explore whether IONPs-FPUF efficiently form distinct zones for the growth of differential
16
17
18 microbial communities, morphology of biofilm formed inside different layers of IONPs-FPUF
19
20 was visualized using SEM. These results confirmed successful immobilization of functional
21
22 bacterial communities in selective biofilms that could be clearly visualized in Figure 1c, d
23
24
25 respectively. Rod and round shaped bacteria were grown in outer and middle layer of carrier
26
27 confirming the growth of QG6 and AOB bacterial respectively (Figure 1c). On the other hand,
28
29
growth of strongly aggregated coccoid shaped anammox bacteria in well-arranged colonies
30
31
32 ensures efficient utilization of toxic quinoline by QG6 in preceding biofilm (Figure 1d). The
33
34 dominant habitats of functional bacteria in sequential and differential zone of the IONPs-FPUF
35
36
37 clearly confirmed the excellent refinement of the FPUF structure which adsorbed toxic quinoline
38
39 on nanoparticles by acting as nanomebrane that ultimately diffused toxin free wastewater to
40
41 AOB and anammox.
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
11
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 12 of 42

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45 Figure 1. SEM images: (a) blank FPUF, (b) IONPs-FPUF (the insets show the high magnification
46
47 images of marked areas, representing efficient coating of IONPs), (c) immobilization of bacterial biomass
48
49 (QG6) on IONPs-FPUF (the inset shows the high magnification images of marked areas exposing growth
50
51 of rod shaped morphology of QG6, hereafter referred as IONPs-FPUF@QG6), and (d) formation of
52
53
anammox biofilm in inner layer of the IONPs-FPUF (the insets show the high magnification images of
54
55
56 marked which represent high co-aggregation and networking capabilities of bacterial communities).
57
58
59
60
12
ACS Paragon Plus Environment
Page 13 of 42 ACS Applied Materials & Interfaces

1
2
3
3.1.2. Topographical and porosity analysis. The topographic features (surface roughness,
4
5
6 porosity and isotherm) of the IONPs-FPUF were further analyzed using AFM and BET to
7
8 investigate the suitability of the IONPs-FPUF for adsorption and bacterial adhesion. The BET
9
10
11
data indicated that the IONPs-FPUF is composed of a well-arranged network of IONPs with
12
13 uniformly sized pores with an average pore size of ~3.17 nm (Figure 2a), which enhances the
14
15 carrier adsorption properties (Table S4) and bacterial adhesion ability (Figure S6) and
16
17
18 ultimately favors Langmuir-type adsorption, as indicated by the isotherm model applied herein
19
20 (Figure 2b, S2 and Table S4). IONPs-FPUF possessed high roughness (1.42) and a uniform
21
22 structure which ascertained high bacterial adhesion on the carrier surface by yielding refined
23
24
25 membrane like biofilm with larger protected surface area (~610 m2 g-1) (Figure 2c). Along with
26
27 roughness, IONPs-FPUF surface symmetry was also determined in terms of skewness and
28
29
kurtosis. Negative skewness values and smaller kurtosis values show that surface is dominated
30
31
32 by ridges thus providing space for bacterial adhesion over IONPs-FPUF (Figure 2c). From
33
34 topographical analysis of biofilm formed over carrier surface it is clear that surface of biofilm is
35
36
37 highly rough with more negative skewness value favoring further pollutants adsorption, bacteria
38
39 adhesion and colonization (Figure 2d). Taken together these results demonstrated that coating of
40
41 IONPs improved surface features of the IONPs-FPUF which ultimately boost up the adsorption
42
43
44 and growth of microbial community into their selective environments.
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
13
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 14 of 42

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45 Figure 2. Carrier topographical and adsorption characteristics; (a) pore size distribution, (b)
46
47 adsorption isotherm, (c) high roughness topography of IONPs-FPUF before bacteria
48
49 immobilization, (d) high roughness topography of IONPs-FPUF after bacteria immobilization.
50
51
52 (Ra, Ssk, Sku indicate surface roughness, skewness and kurtosis respectively)
53
54
55 3.1.2. Spectroscopic characterization. Surface elemental quantification of FPUF and IONPs-
56
57 FPUF was done using EDX analysis. The core level spectra of all the elements indicate high
58
59
60
14
ACS Paragon Plus Environment
Page 15 of 42 ACS Applied Materials & Interfaces

1
2
3
purity of FPUF as shown in Figure 3a. The inset of Figure 3a shows the weight and atomic
4
5
6 percentages of all the detected elements. Figure 3b shows the presence of an additional peak
7
8 corresponding to iron, which confirms the efficient coating of the IONPs on the FPUF surface.
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32 Figure 3. EDX analysis of (a) FPUF (the inset shows elemental values in percent) and (b)
33
34 IONPs-FPUF (the inset shows elemental values in percent and high resolution spectra of lower
35
36
energy part with clear visualization of the peaks).
37
38
39
40 3.2. Adsorption experiments. SEM, AFM and BET characterization predict IONPsFPUF to be
41
42 a potential candidate for adsorption, therefore a comparative study to differentiate the adsorption
43
44 capabilities of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 was done. A linear relationship
45
46
47 was observed between the quinoline concentration and the adsorption capacity of the carriers
48
49 where adsorption capacity increased with increase in quinoline concentration (Figure 4). The
50
51
52
quinoline adsorption followed the following order on the developed carriers: IONPs-
53
54 FPUF@QG6 (90 mg g1) IONPs-FPUF (80 mg g1) FPUF (70 mg g1). High adsorption on
55
56 the surface of IONPs-FPUF@QG6 could be attributed to the suitable porosity and high surface
57
58
59
60
15
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 16 of 42

1
2
3
area of the IONPs-FPUF@QG6 carrier (Table S4). Similarly, limited presence of surface
4
5
6 functional groups on pure FPUF could possible lowered their adsorption capacity. Taken
7
8 together, these results validate the efficiency of the IONPs-FPUF@QG6 carrier as a good
9
10
11
adsorbent and the enhancing effect of IONPs. The adsorption capacity of the carrier increased
12
13 quickly with increasing concentration of quinoline in the influent solution due to an increase in
14
15 the driving force of the quinoline gradient. This ultimately enhanced the interactions between
16
17
18 quinoline and the IONPs-FPUF@QG6 adsorbent. Further increase of quinoline concentration
19
20 beyond 350 mgL-1 did not significantly enhance adsorption on the FPUF and IONPs-FPUF due
21
22 to exhaustion in binding sites, whereas adsorption capacity of IONPs-FPUF@QG6 did increase
23
24
25 with involvement of QG6 bacteria in adsorption process. To illustrate the fact that quinoline
26
27 adsorption by IONPs-FPUF did not increased beyond 350 mgL-1, adsorption capacity of IONPs-
28
29
FPUF was evaluated at 500 mgL-1 and compared with IONPs-FPUF@QG6. No more adsorption
30
31
32 could be seen in case of IONPs-FPUF (Figure 4) on further increment in quinoline concertation
33
34 from 350 to 500 mgL-1, whereas adsorption capacity of IONPs-FPUF@QG6 continue to increase
35
36
37 confirming the involvement of QG6 bacteria in simultaneous adsorption and biodegradation
38
39 process which spontaneously provided vacant spaces in carrier to adsorb quinoline continuously.
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
16
ACS Paragon Plus Environment
Page 17 of 42 ACS Applied Materials & Interfaces

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30 Figure 4. Comparison of adsorption capacity of FPUF, IONPs-FPUF and IONPs-FPUF@QG6
31
32 at different quinoline concentrations. The inset represents the magnified adsorption capacity of
33
34 IONPs-FPUF and IONPs-FPUF@QG6 in region of 60-100%.
35
36
37 3.2.1. Isothermal models.
38
39 To understand the nature of the interaction between the adsorbate (quinoline) and adsorbent for
40
41
42
removal of organic pollutants, the adsorption isotherms were applied. An adsorption isotherm
43
44 describes the relationship between the amount of adsorbate taken up by the adsorbent and the
45
46 adsorbate concentration remaining in solution. In the present study, the Freundlich and Langmuir
47
48
49 adsorption nonlinear models were applied to further investigate the adsorption of quinoline on
50
51 the FPUF, IONPs-FPUF and IONPs-FPUF@QG6 (Figure 5). The Freundlich isotherm model
52
53 (Eq. 3)44 indicates heterogeneity of the surface and favorable multilayer adsorption:
54
55 
56  =     (3)
57
58
59
60
17
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 18 of 42

1
2
3
Here,  (mg g1) is the Freundlich equation constant related to the adsorption capacity, and n
4
5
6 is the intensity factor. On the other hand, the Langmuir isotherm is applied considering the
7
8 maximum adsorption of the solute with saturated monolayer coverage of the solute molecules
9
10
11 over the adsorbent surface, with no transmigration of the solute/adsorbate in the plane of the
12
13 adsorbent surface, and is represented by Eq. 4.45,46
14
15   
16 =  (4)
  
17
18
19 Here,  (mgL1),  (mg g1) is the equilibrium concentration of quinoline and corresponds to
20
21 equilibrium adsorption,  ! (mg g1) is the maximum adsorption capacity, and b (L mg1) is the
22
23
24 Langmuir constant that represents the affinity of quinoline for the adsorbents and is obtained
25
26 
from a plot of 
against the equilibrium concentration  . The results (simulated curves) of
27
28
29 Langmuir and Freundlich models are given in Figure 5. The Langmuir isotherm best described
30
31
32 the adsorption characteristics of the FPUF, IONPs-FPUF and IONPs-FPUF@QG6, indicating
33
34 the homogeneity of the surfaces of FPUF, IONPs-FPUF and IONPs-FPUF@QG6. The
35
36 maximum theoretical adsorption capacity ( ! ) of the IONPs-FPUF@QG6 was 125 mg g1
37
38
39 from the Langmuir model (Table 1). A strong correlation between experimental and theoretical
40
41 adsorption capacities (!" ) and higher coefficients (R2) 0.9 values for FPUF, IONPs-FPUF and
42
43
44 IONPs-FPUF@QG6 confirmed the validity of the Langmuir model. The applicability of the
45
46 Langmuir isotherm model indicated that the adsorption of quinoline occur by monolayer
47
48 coverage, i.e. quinoline is chemically adsorbed over the FPUF, IONPs-FPUF and IONPs-
49
50
51 FPUF@QG6 at a well-defined, fixed number of binding sites, with only one adsorbate species at
52
53 each site, and without any type of interaction among the adsorbed quinoline molecules; all
54
55
56
57
58
59
60
18
ACS Paragon Plus Environment
Page 19 of 42 ACS Applied Materials & Interfaces

1
2
3
binding sites are energetically equivalent. These facts indicate that the mechanism of quinoline
4
5
6 adsorption is chemosorptive.
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33 Figure 5. Non-Linearized, Langmuir (dashed lines) and Freundlich (solid lines) isothermal
34
35 models for quinoline adsorption.
36
37
38
39 Furthermore, feasibility and spontaneity of adsorption of quinoline was determined by
40
41 calculating value of Gibbs free energy (Go) using equation 5:
42
43
G% = &RT lnK + (5)
44
45
46 Here, Kc is the adsorption equilibrium constant and T is the absolute temperature. The Go
47
48 values for the overall process were 10, 29, and 38 kJmol1 for the FPUF, IONPs-FPUF and
49
50
51 IONPs-FPUF@QG6, respectively. The negative value of Go clearly confirmed that the
52
53 adsorption process is spontaneous at room temperature and pressure. Moreover, negative values
54
55 of Go imply a greater driving force and show that the adsorption of quinoline by IONPs-
56
57
58 FPUF@QG6 is highly favorable.
59
60
19
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 20 of 42

1
2
3
In addition to predicting the spontaneity of the reaction, the Go values were also used to
4
5
6 predict the mechanism of adsorption (e.g. physisorption, chemisorption, etc.,) on the FPUF,
7
8 IONPs-FPUF and IONPs-FPUF@QG6 surface. It is well established that less negative Go
9
10
11
values (20 kJ mol1) for the adsorption reaction correspond to physisorption, whereas
12
13 adsorption with highly negative Go values (40 kJ mol1) follow chemisorption.47 The Go
14
15 values obtained for the present system (10, 29, and 38 kJ mol1) were more negative, which
16
17
18 demonstrates that adsorption on the carrier surface followed the chemisorption mechanism and
19
20 verifies the results presented above. A possible mechanism for chemisorption on the surface of
21
22 the carrier may involve transfer of -electrons from the organic molecules to the vacant d-orbital
23
24
25 of the metal (iron) to form a bond. Chemisorption of the organic molecules on the carrier surface
26
27 leads to strong binding and homogenous coating of the carrier surface, further confirming the
28
29
validity of the Langmuir adsorption model for the present system.48-50
30
31
32
33 Table 1. Comparison of non-linearized Langmuir and Freundlich isotherm models for quinoline
34
35 adsorption over FPUF, IONPs-FPUF and IONPs-FPUF@QG6
36
37
38
39 Model IONPs-FPUF@QG6 IONPs-FPUF FPUF
40
41 R2 *qmax (mg g-1) R2 *qmax (mg g-1) R2 *qmax (mg g-1)
42
43 Langmuir Isotherm 0.995 125 0.997 100 0.994 32
44
45 Freundlich Isotherm 0.886 69.84 0.785 57.66 0.927 30
46
**qexp (mg g-1) 98.6 78.11 29.50
47
48 -1
G (kJmol ) -38 -29 -10
49
50 * Equilibrium adsorption capacity calculated from Equations 3 & 4
51
52 ** Experimental adsorption capacity at equilibrium
53
54
55
56
57
58
59
60
20
ACS Paragon Plus Environment
Page 21 of 42 ACS Applied Materials & Interfaces

1
2
3
3.2.2. Kinetics experiments. The kinetics of quinoline adsorption on the surface of FPUF,
4
5
6 IONPs-FPUF and IONPs-FPUF@QG6 surface was further evaluated using time-dependent
7
8 adsorption studies, and batch experiments were conducted from 0 to 2800 minutes (min). For the
9
10
11
FPUF, equilibrium was attained within 360 min whereas the adsorption efficiency for IONP-
12
13 FPUF carrier increased consistently up to 480 min. After attaining equilibrium after 480 min, no
14
15 more increase in adsorption capacity was observed up to 2800 min. In contrast, the IONPs-
16
17
18 FPUF@QG6 demonstrated relatively dominant removal performance which did not reach
19
20 equilibrium up to 2800 min. Much faster adsorption of quinoline was observed up to 750 min
21
22 (Figure 6) due to the availability of a large number of adsorption sites that quickly adsorb the
23
24
25 molecules from the effluent solution. However, with time, the number of available sites on the
26
27 carrier tends to decrease, leading to reduced adsorption (equilibrium phase) after the carrier is
28
29
exposed to the effluent for longer durations.51-52 After 750 min adsorption process was slow
30
31
32 down on the IONPs-FPUF@QG6 carrier because quinoline adsorbed by the IONPs-FPUF@QG6
33
34 moves inside the carrier and is degraded by the QG6 bacteria, making the adsorption sites
35
36
37 available for further adsorption of quinoline. In contrast to other carriers, the removal efficiency
38
39 of IONPs-FPUF@QG6 increased with time due to adsorption of quinoline and its subsequent
40
41 degradation by the bacterial communities.
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
21
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 22 of 42

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33 Figure 6. Effect of time on quinoline adsorption by FPUF, IONPs-FPUF and IONPs-
34
35
36 FPUF@QG6 (pH = 7.8, temperature = 37 C, Ci = 350 mgL-1, and stirring speed = 150 rpm.
37
38
39 3.2.3. Kinetics models. The kinetics data for quinoline adsorption was fitted to pseudo-first order
40
41
42
and pseudo-second order kinetic models. The pseudo-first order model only describes the
43
44 adsorption based on the concentration of quinoline in the solution, whereas the adsorption
45
46 process involves reversibility in the form of an equilibrium between the adsorbate and adsorbent
47
48
49 surface.53 In most cases, the pseudo-first order kinetic model is not applicable to the data and the
50
51 following relationship is thus used:
52
53 1%2 /34 56
54 log(q ./ & q 0 ) (6)
7.9:9 0
55
56
57
58
59
60
22
ACS Paragon Plus Environment
Page 23 of 42 ACS Applied Materials & Interfaces

1
2
3
4
Here, k1 (min1), ; (mg g1), and  (mg g1) are the pseudo-first-order adsorption rate
5
6 constant, the amount adsorbed at time t (min), and the amount adsorbed at equilibrium,
7
8 respectively. The k1 and  values were obtained from the plot of <=( & ; ) versus t.54 The
9
10
11 pseudo-second order kinetic model described the adsorption depending upon both the quinoline
12
13 concentration and the availability active sites on the FPUF, IONPs-FPUF and IONPs-
14
15
16 FPUF@QG6 surface and supports the concept that the carrier surface and adsorbate interact via
17
18 electron sharing or transfer. The model has been quite useful for determining the rate-controlling
19
20 step for adsorption processes that follow the chemisorption mechanism.
21
22
23 The pseudo-second-order model was calculated by using the following relationship:
24
;  
=  A B C
25
@
(7)
26 > ?@  
27
28
29 Here, k2 (g mg1 min1) is the adsorption rate constant; k2 and qe can be obtained from the
30
31 C
intercept and slope of the plot of D versus t.30, 55-56 The value of qe for a given initial quinoline
32
33
34 concentration was determined, whereas the adsorption rate constants (k1 & k2) were evaluated
35
36
37 from the intercepts of the graph (Figure 7) and are summarized in Table 2 along with the R2
38
39 values. The applicability of the kinetic models was determined in terms of the correlation
40
41 coefficients (R2). The adsorption values obtained for the pseudo-second order kinetic model were
42
43
44 consistent with the experimental values, as shown in Table 2. Mechanistically, the
45
46 chemisorption of quinoline on carrier surface might be due to the interaction between
47
48
heterocyclic nitrogen and hydroxylated surface of oxide. Another possibility for adsorption is the
49
50
51 donor-acceptor relationship between iron and quinoline, given that the transition metal iron
52
53 possesses vacant d-orbitals and quinoline possesses -electrons and thus can act as an electron
54
55
56
donor while iron acts as an acceptor.
57
58
59
60
23
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 24 of 42

1
2
3
Table 2. Parameters of Pseudo-First-Order and Pseudo-Second-Order kinetic models for
4
5
6 quinoline adsorption by FPUF, IONPs-FPUF and IONPs-FPUF@QG6.
7
8
9
Kinetic model Pseudo-first order Pseudo-second order
10 Parameters R2 k1 *qmax (mg g-1) R2 *qmax (mg g-1) k2
11
12 IONPs-FPUF 0.54 2.310 -04 42.01 0.999 30.13 3.010- 03
13
14 FPUF 0.43 4.6 10 -04 40.12 0.999 29.41 1.110- 03
15
16
17 IONPs-FPUF@QG6 0.57 2.110- 04 44 0.999 30 2.510- 03
18
19 **qexp (mg g-1) 28.6 28.6
20
21
22 * Equilibrium adsorption capacity calculated from equation 6 and 7
23
24 ** Experimental adsorption capacity at equilibrium
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45 Figure 7. Linearized pseudo-first (a) and second order (b) kinetics model for quinoline
46
47 adsorption by FPUF, IONPs-FPUF and IONPs-FPUF@QG6.
48
49
50 3.3. Spectroscopic analysis of adsorbents. Adsorption of quinoline was further confirmed using
51
52 Fourier Transform Infrared (FTIR) and Raman spectra of FPUF, IONPs-FPUF and IONPs-
53
54 FPUF@QG6 with and without quinoline loading/adsorption at natural pH (Figure 8a). Peaks
55
56
57 centered at 1594 cm-1 (C=O), 1302 cm-1 (C-O), 3435 cm-1 (O-H) confirmed the presence of
58
59
60
24
ACS Paragon Plus Environment
Page 25 of 42 ACS Applied Materials & Interfaces

1
2
3
oxygen containing functional groups in all types of adsorbents. Comparing the absorption bands
4
5
6 of modified carriers with FPUF carrier, a clear suppression in peaks associated with C-O and
7
8 C=O bond is observed that is clear representation of involvement of these two functional groups
9
10
11
in adsorption of quinoline, maximum suppression in peak height was observed in case of IONPs-
12
13 FPUF@QG6 favored highest adsorption of quinoline over its surface.
14
15 Surface elemental analysis of IONPs-FPUF@QG6 before and after the adsorption experiments
16
17
18 was carried out using EDX elemental analysis to further confirm adsorption of quinoline. Figure
19
20 8b shows the EDX data for the IONPs-FPUF@QG6 after adsorption of quinoline, the detection
21
22 of nitrogen (a part of the heterocyclic structure of quinoline) in addition to the original elements
23
24
25 Figure 3b of the IONPs-FPUF indicates adsorption of quinoline on the IONPs-FPUF@QG6.
26
27 These results were further authenticated by Raman spectra in which relatively high and clear
28
29
peaks of quinoline were appeared at 1380 cm-1 in IONPs-FPUF@QG6 that consequently shifted
30
31
32 in others adsorbents (Figure S3).
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53 Figure 8. (a) FTIR spectra of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 (before and after
54
55 quinoline adsorption and (b) EDX analysis of IONPs-FPUF@QG6 (the inset shows the high
56
57 resolution of lower energy area part of EDX spectra).
58
59
60
25
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 26 of 42

1
2
3
3.4. Biodegradation capabilities of the functional bacteria (QG6)
4
5
6 To investigate more specific functions and activities of the QG6, a batch experiment was
7
8 performed in a flask for a period of 24 h. The results presented here, clearly indicate strong
9
10
11
biodegradation ability of QG6 due to complete removal of 350 mgL-1 quinoline within 16 h
12
13 (Figure 9a). Very interestingly, straightforward comparison between quinoline adsorption and
14
15 biodegradation demonstrated that the QG6 has higher biodegradation rates than IONPs-FPUF
16
17
18 adsorption which strongly verified the effectiveness of the synergic adsorption-biodegradation
19
20 process for efficient removal of aromatic and nitrogenous compounds. On the other hand, QG6
21
22 also showed significant potential for transformation of NH4 into NO3, which again proves to be a
23
24
25 readily available nutrient source for QG6 that helped to speed up QG6 metabolism and
26
27 bioactivities (Figure S4). The rapid growth of QG6 was shown to be positively correlated with
28
29
increased rate of quinoline biodegradation which was quite higher than that of AOB and
30
31
32 anammox bacteria (Figure 9a). This correlation proven to be a very useful to enhance the
33
34 favorable environments for the AOB and anammox communities by preventing the penetration
35
36
37 of toxic quinoline in inner layers of the carrier (Figure 9b). For instance, QG6 and AOB require
38
39 oxygen to biodegrade quinoline and NH4 into NO2; in this way, these bacteria provided nutrient
40
41 support (NO2) to the anammox which is a necessary nutrient for complete removal of NH4 into
42
43
44 N2 gas. In a similarly fashion, the development of thick adsorbent and QG6-AOB biofilms on
45
46 outer layers kept strictly anaerobic environment for anammox, as anammox specific activities are
47
48 totally dependent on anaerobic conditions. Such ideal environment is the basic reason behind
49
50
51 ideal functionality of the anammox communities which otherwise have been proved very
52
53 difficult to maintained such an efficient environment.
54
55
56
57
58
59
60
26
ACS Paragon Plus Environment
Page 27 of 42 ACS Applied Materials & Interfaces

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46 Figure 9. (a) Biodegradation of quinoline by QG6 and growth of the bacteria with time, (b)
47
48 quinoline profile within different layers (zones) of the carrier
49
50
51
52 To witnessed the progressive growth of the QG6, FISH images were acquired by analyzing
53
54 QG6 biofilm at different duration of the experiment. Figure 10a
d is promptly evident of
55
56
57 dynamic and continual growth of QG6 with passage of time which sequentially tend to strong
58
59
60
27
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 28 of 42

1
2
3
co-aggregation on 200th day of the experiment (Figure 10d). These results strongly authenticate
4
5
6 our batch experiment for quinoline adsorption and biodegradation. In fact, the effective structure
7
8 of the carrier synergistically blocked aromatic pollutants and bear their heavy shock loads which
9
10
11
ultimately given an excellent opportunity to QG6 for rapid biodegradation of quinoline into NH4
12
13 and distributed equal nutrients to the AOB and anammox bacterial communities.
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53 Figure 10. Confocal laser scanning microscopy images showing continuous and progressive
54
55 growth of QG6 within IONPs-FPUF, (a) 0 day (when inoculum was immobilized in carrier), (b)
56
57 65 days, (c) 100 days, (d) 200 days
58
59
60
28
ACS Paragon Plus Environment
Page 29 of 42 ACS Applied Materials & Interfaces

1
2
3
3.5 The protective role of the adsorbent; growth of the functional bacteria
4
5
6 The successive growth of AOB and anammox in the inner layers of IONPs-FPUF carrier was
7
8 characterized using FISH analysis to assess the role of the adsorbent as a protective layer. Initial
9
10
11
analysis of inoculum showed the dominant abundance of anammox bacterial communities inside
12
13 carrier (Figure 11a) which gradually reached to stable growth within 50 days of reactor
14
15 operation. The improved microbial community structure (Figure 1) and nitrogen removal
16
17
18 performance (Figure 12, removal rate reached to 60 mgL-1) implied that the immobilization
19
20 of the QG6 and AOB would be of primary importance to enhance the role of both adsorbent and
21
22 functional bacteria by synergetic adsorption-
23
24
25 biodegradation. The significant removal of quinoline and nitrogen was achieved during 5065
26
27 days of reactor operation which led us to confirm the relative growth of the newly immobilized
28
29
30 bacterial communities. The microbial community analysis on 65th day of reactor operation
31
32 provided clear indication of the successful immobilization of QG6 and AOB (Figure 10c and
33
34 11b). Furthermore, the reactor operation was extended to longer period to confirm the stable
35
36
37 growth of microbial communities. A relatively higher concentration of the AOB and anammox
38
39 was observed after 100 days of operation (Figure 11b). The further increasing growth of the
40
41
AOB and anammox population clearly demonstrated that the poisonous quinoline is adsorbed on
42
43
44 the outer layer prior to contact of the influent with them. The bacterial population continued to
45
46 multiply, and after 200 days of operation, a much larger population of bacterial communities was
47
48
49
observed (Figure 11d). In addition, these 3-dimensional (3D) images confirm that the segregated
50
51 bacterial communities were present on the carrier surface. Thus, the existence of such differential
52
53 bacterial communities effectively removes the toxic quinolone by degrading it into NH4 and NO2
54
55
56 which were further transformed by AOB and anammox bacterial communities (Figure S5) via
57
58
59
60
29
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 30 of 42

1
2
3
well-organized teamwork without affecting the bacterial growth. This makes the unique carrier a
4
5
6 very strong candidate for efficient treatment of refractory compounds, organic carbon and
7
8 ammonium from coking wastewater.
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39 Figure 11. Confocal laser scanning microscopy images showing continuous and progressive
40
41 growth of different bacterial communities within IONPs-FPUF, (a) 0 day, (b) after 65 days, (c)
42
43
44
100 days, (d) 200 days (red and green represent anammox and AOB bacteria, respectively).
45
46
47 3.6 Nitrogen conversion performance of functional bacteria (AOB and anammox)
48
49
50 To further validate the efficacy of the AOB and anammox bacterial communities, nitrogen
51
52
53 (resulted from the biodegradation of quinoline as well supplemented in wastewater e.g. NH4,
54
55 NO2, NO3) conversion rates were monitored over the period of 200 days. The anammox showed
56
57
limited initial capability for nitrogen removal (~1517%), which can be attributed to the lower
58
59
60
30
ACS Paragon Plus Environment
Page 31 of 42 ACS Applied Materials & Interfaces

1
2
3
population of anammox bacteria in the carrier during start-up phase. However, a gradual increase
4
5
6 in the anammox bacterial population resulted stability in the biological process which
7
8 consequently enhanced nitrogen removal performance. The enhanced activity with passage of
9
10
11
time is clear from the 60% removal of NH4 and NO2 achieved after few days of operation, which
12
13 is approximately 3-times greater than most of the start-up process, providing clear indication of
14
15 the good adsorption and bacterial adhesion capabilities of the IONPs-FPUF carrier. The
16
17
18 improved performance further demonstrates that the anammox bacteria are free from quinoline
19
20 poisoning, given that quinoline is adsorbed in the adjacent layer prior to contact of the effluent
21
22 with anammox. The removal of nitrogen increased continuously with an increase of the
23
24
25 anammox bacterial population, and after 100 days of operation, the NH4 and NO2 removal
26
27 efficiencies exceeded 90% with a record hydraulic retention time (HRT) of 6 h (Figure 12).
28
29
Furthermore, a high chemical oxygen demand (COD) removal rate was achieved (98% @ 3286
30
31
32 mgL1) and was found to be consistent and stable to the end of experiment (200 days). Hence,
33
34 the current design proved to be very beneficial for preservation of the anammox bacterial
35
36
37 communities that were killed in other systems when exposed to organic carbon (Figure 12c).
38
39 Previous literature reveals that carbon removal from wastewater is required before feeding the
40
41 wastewater to anammox treatment systems that was done in-situ in present design (Scheme 1).
42
43
44 The high removal performance (C, N, and quinoline) achieved herein is due to the combination
45
46 of successful adsorption, carbon removal, quinoline biodegradation, and an absolute anaerobic
47
48 habitat zone within the inner layers of this novel carrier. After 50 days, when quinoline was
49
50
51 added in wastewater, negligible inhibition was observed on the performance of the bacterial
52
53 community (Figure 12b, c), which was recovered steadily as QG6 growth increased that
54
55
56
ultimately enhanced quinoline removal. In fact, quinoline removal increased steadily due to the
57
58
59
60
31
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 32 of 42

1
2
3
adsorption layers inside the novel carrier that helped to offset sudden and toxic shocks to the
4
5
6 bacteria by the inhibitors and pollutants.
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
Figure 12: Nitrogen removal performance over entire period of study: (a) removal rate (the inset
42
43
44 shows zoomed removal rates of ammonium, nitrite and nitrate), (b) ammonium removal
45
46 efficiency, (c) NO2 removal efficiency and (d) COD removal rate. Different colors represent
47
48
49
different phases of the bioreactors operation as labelled in the Figures.
50
51
52 In addition to the higher efficiency for removal of toxic organic and inorganic species from the
53
54 contaminated water, the developed carrier also presents a plausible solution for overcoming the
55
56
57 granular floating issue. Generally, the developed granules involving anammox species possess
58
59
60
32
ACS Paragon Plus Environment
Page 33 of 42 ACS Applied Materials & Interfaces

1
2
3
very low density due to entrapped nitrogen gas and float on the surface of water, which limits
4
5
6 their activity. It is speculated that the increase in the density arising from the decomposition of
7
8 quinoline and nitrogen species enhances the biomass of QG6, AOB, and anammox, and the
9
10
11
proper creation of micro-channels facilitates regular emission of nitrogen gas. After 180 days of
12
13 operation, the total nitrogen removal efficiency reached to 97%, which remained almost steady
14
15 throughout the remaining period of the study (200 days). Although the nitrogen loading rate
16
17
18 increased with a gradual decrease of the HRT, along with a subsequent increase of the influent
19
20 nitrogen concentration, the performance of the reactor became progressively stable. According to
21
22 our best knowledge, the removal rates of quinoline, carbon and nitrogen are better than previous
23
24
25 literature documented for simultaneous adsorption and biodegradation (Table S5,6).57-60
26
27
28 CONCLUSIONS
29
30
31
32
A unique strategy was established for highly efficient treatment of coking wastewater containing
33
34 high-strength bio-refractory compounds, organic carbon and nitrogen by novel carrier with high
35
36 surface area derived from the nanostructured IONPs coated on FPUF. As-synthesized IONPs-
37
38
39 FPUF acts as an effective support for the growth of functional bacterial communities for
40
41 synergistic adsorption and biodegradation of quinoline. QG6 was incorporated on the outer
42
43 surface of the carrier to convert the ammonium to nitrogen gas, AOB and anammox were
44
45
46 incorporated in the inner layers of the carrier. This design successfully protected the functional
47
48 bacterial communities from the toxic effects of quinoline and provides a highly favorable
49
50
environment to enhance the simultaneous adsorption-biodegradation. The efficiently coupled
51
52
53 adsorption and biodegradation process gave high removal of NH4, NO2, quinoline and chemical
54
55 oxygen demand up to 322 mgL1 (98%), 311 mgL1 (99%), 350 mgL-1 (100%) and 3286 mgL1
56
57
58
(98%), respectively, along with 633 mgL1 (97%) total nitrogen (8 mgL-1 averaged NO3
59
60
33
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 34 of 42

1
2
3
concentration was recorded in effluent). We strongly believe that the current work will add a new
4
5
6 dimension to the search for highly active, biocompatible carriers for removal of mixed pollutants
7
8 from different types of wastewater by enhancing synergic adsorption-biodegradation.
9
10
11
ASSOCIATED CONTENT
12
13
14 Supporting Information. The part of experimental design and FISH images. This material is
15
16 available free of charge via the Internet at http://pubs.acs.org.
17
18
19
20 AUTHOR INFORMATION
21
22
23 Corresponding Author
24
25 * Jinren Ni (nijinren@iee.pku.edu.cn)
26
27
28 Author Contributions
29
30
31 The manuscript was written through contributions of all authors. All authors have given approval
32
33 to the final version of the manuscript.
34
35
36 ACKNOWLEDGMENTS
37
38 The authors highly appreciate the National Science Foundation of China (NO. 51539001)
39
40
for providing financial support for this study.
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58 REFERENCES
59
60
34
ACS Paragon Plus Environment
Page 35 of 42 ACS Applied Materials & Interfaces

1
2
3
(1) Wu, Z.; Zhu, L., Removal of Polycyclic Aromatic Hydrocarbons and Phenols from Coking
4
5
6 Wastewater by Simultaneously Synthesized Organobentonite in A One-Step Process. J.
7
8 Environ. Sci. 2012; 24, 248-253.
9
10
11
(2) Burmistrz, P.; Burmistrz, M., Distribution of Polycyclic Aromatic Hydrocarbons in Coke
12
13 Plant Wastewater. Water Sci. Technol. 2013, 68, 2414-2420.
14
15 (3) Burmistrz, P.; Rozwadowski, A.; Burmistrz, M.; Karcz, A., Coke Dust Enhances Coke Plant
16
17
18 Wastewater Treatment. Chemosphere 2014, 117, 278-284.
19
20 (4) Fu, Z.; Zhao, J., Impact of Quinoline on Activity and Microbial Culture of Partial
21
22 Nitrification Process. Bioresour. Technol. 2015, 197, 113-119.
23
24
25 (5) Padoley, K.; Rajvaidya, A.; Subbarao, T.; Pandey, R., Biodegradation of Pyridine in a
26
27 Completely Mixed Activated Sludge Process. Bioresour. Technol. 2006, 97, 1225-1236.
28
29
(6) Ge, S.; Agbakpe, M.; Wu, Z.; Kuang, L.; Zhang, W.; Wang, X., Influences of Surface
30
31
32 Coating, UV Irradiation and Magnetic Field on the Algae Removal using Magnetite
33
34 Nanoparticles. Environ. Sci. Technol. 2014, 49, 1190-1196.
35
36
37 (7) Liu, Z. J.; Yang, Y. L. In Coking Wastewater Physico-Chemical Treatment Technology
38
39 Evolvement Review, Advanced Materials Research, Trans Tech. Publ: 2014, 88-95.
40
41 (8) Kumar, R.; Chakrabortty, S.; Pal, P., Membrane-Integrated Physico-Chemical Treatment of
42
43
44 Coke-Oven Wastewater: Transport Modelling and Economic Evaluation. Environ. Sci.
45
46 Pollut. Res. 2015, 22, 6010-6023.
47
48 (9) Gao, L.; Li, S.; Wang, Y.; Sun, H., Organic Pollution Removal from Coke Plant Wastewater
49
50
51 using Coking Coal. Water Sci. Technol. 2015, 72, 158-163.
52
53 (10) Zhang, S.; Zheng, J.; Chen, Z., Combination of Ozonation and Biological Aerated Filter
54
55
56
(BAF) for Bio-Treated Coking Wastewater. Sep. Purif. Tech. 2014, 132, 610-615.
57
58
59
60
35
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 36 of 42

1
2
3
(11) Huang, Y.; Hou, X.; Liu, S.; Ni, J., Correspondence Analysis of Bio-Refractory Compounds
4
5
6 Degradation and Microbiological Community Distribution in Anaerobic Filter for Coking
7
8 Wastewater Treatment. Chem. Eng. J. 2016, 304, 864-872.
9
10
11
(12) Pan, L. T.; Han, Y.; Wu, J. F., Advanced Treatment of Biologically Pretreated Coking
12
13 Wastewater by Intensified Zero-Valent Iron Process (IZVI) Combined with Anaerobic Filter
14
15 and Biological Aerated Filter (AF/BAF). J. Cent. South Univ. 2015, 22, 3781-3787.
16
17
18 (13) Sharma, N. K.; Philip, L., Combined Biological and Photocatalytic Treatment of Real Coke
19
20 Oven Wastewater. Chem. Eng. J. 2016, 295, 20-28.
21
22 (14) Chunhu, Z.; Peidong, S.; Jiawei, T.; Hangyin, S.; Weidong, J.; Shan, J., Study on Coke
23
24
25 Powder Bipolar Three-Dimensional Electrode Reactor Applied to Treat Coking Wastewater.
26
27 Coal Sci. Technol. 2015, 11, 34.
28
29
(15) Wang, C.; Zhang, M.; Liu, W.; Ye, M.; Su, F., Effluent Characteristics of Advanced
30
31
32 Treatment for Biotreated Coking Wastewater by Electrochemical Technology using BDD
33
34 Anodes. Environ. Sci. Pollut. Res. 2015, 22, 6827-6834.
35
36
37 (16) Zhao, J. J.; Wang, J.; Liu, Q. F.; Yan, S. H.; Li, F. Z.; Fan, B. Q.; Feng, H. B.; Cao, W. W.
38
39 In A Review of Hybrid Process to Treat Coking Wastewater, Advanced Materials Research,
40
41 Trans. Tech. Publ: 2014, 2234-2237.
42
43
44 (17) Jiang, B.; Shi, S.; Song, L.; Tan, L.; Li, M.; Liu, J.; Xue, L., Efficient Treatment of Phenolic
45
46 Wastewater with High Salinity using a Novel Integrated System of Magnetically
47
48 Immobilized Cells Coupling with Electrodes. Bioresour. Technol. 2016, 218, 108-114.
49
50
51 (18) Liu, J.; Ou, H. S.; Wei, C. H.; Wu, H. Z.; He, J. Z.; Lu, D.-H., Novel Multistep
52
53 Physical/Chemical and Biological Integrated System for Coking Wastewater Treatment:
54
55
56
Technical and Economic Feasibility. J. Water Process Eng. 2016, 10, 98-103.
57
58
59
60
36
ACS Paragon Plus Environment
Page 37 of 42 ACS Applied Materials & Interfaces

1
2
3
(19) Wang, P.; Wang, X.; Yu, S.; Zou, Y.; Wang, J.; Chen, Z.; Alharbi, N. S.; Alsaedi, A.; Hayat,
4
5
6 T.; Chen, Y.; Wang, X., Silica Coated Fe3O4 Magnetic Nanospheres for High Removal of
7
8 Organic Pollutants from Wastewater. Chem. Eng. J. 2016, 306, 280-288.
9
10
11
(20) Xu, P.; Ma, W.; Han, H.; Hou, B.; Jia, S., Biodegradation and Interaction of Quinoline and
12
13 Glucose in Dual Substrates System. Bull. Environ. Contam. Toxicol. 2015, 94, 365-369.
14
15 (21) Wang, C.; Zhang, M.; Cheng, F.; Geng, Q., Biodegradation Characterization and
16
17
18 Immobilized strains Potential for Quinoline Degradation by Brevundimonas sp. K4 isolated
19
20 from Activated Sludge of Coking Wastewater. Biosci. Biotechnol. Biochem. 2015, 79, 164-
21
22 170.
23
24
25 (22) Ramette, A., Multivariate Analyses in Microbial Ecology. FEMS Microbiol. Ecol. 2007, 62,
26
27 142-160.
28
29
(23) Ali, M.; Chai, L. Y.; Min, X. B.; Tang, C. J.; Afrin, S.; Liao, Q.; Wang, H. Y.; Peng, C.;
30
31
32 Song, Y. X.; Zheng, P., Performance and Characteristics of a Nitritation Air-Lift Reactor
33
34 under Long-Term HRT Shortening. Int. Biodeterior. Biodegrad. 2016, 111, 45-53.
35
36
37 (24) Zhang, P.; Jia, R.; Zhang, Y.; Shi, P.; Chai, T., Quinoline-Degrading Strain Pseudomonas
38
39 Aeruginosa KDQ4 isolated from Coking Activated Sludge is Capable of the Simultaneous
40
41 Removal of Phenol in a Dual Substrate System. J. Environ. Sci. Health, Part A:
42
43
44 Toxic/Hazard. Subst. Environ. Eng. 2016, 13, 1139-1148.
45
46 (25) Ali, M.; Okabe, S., Anammox-Based Technologies for Nitrogen Removal: Advances in
47
48 Process Start-up and Remaining Issues. Chemosphere 2015, 141, 144-153.
49
50
51 (26) Jetten, M. S.; Wagner, M.; Fuerst, J.; van Loosdrecht, M.; Kuenen, G.; Strous, M.,
52
53 Microbiology and Application of the Anaerobic Ammonium Oxidation (Anammox)
54
55
56
Process. Curr. Opin. Biotechnol. 2001, 12, 283-288.
57
58
59
60
37
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 38 of 42

1
2
3
(27) Tang, C. J.; Zheng, P.; Wang, C. H.; Mahmood, Q.; Zhang, J. Q.; Chen, X. G.; Zhang, L.;
4
5
6 Chen, J. W., Performance of High-Loaded ANAMMOX UASB Reactors Containing
7
8 Granular Sludge. Water Res. 2011, 45, 135-144.
9
10
11
(28) Helmy, A.; De Bussetti, S.; Ferreiro, E., Adsorption of Quinoline from Aqueous Solutions
12
13 by Some Clays and Oxides. Clays Clay Miner. 1983, 31, 29-36.
14
15 (29) Burgos, W. D.; Pisutpaisal, N.; Mazzarese, M. C.; Chorover, J., Adsorption of Quinoline to
16
17
18 Kaolinite and Montmorillonite. Environ. Eng. Sci. 2002, 19, 59-68.
19
20 (30) Rameshraja, D.; Srivastava, V. C.; Kushwaha, J. P.; Mall, I. D., Quinoline Adsorption onto
21
22 Granular Activated Carbon and Bagasse Fly Ash. Chem. Eng. J. 2012, 181, 343-351.
23
24
25 (31) Vico, L.; Acebal, S., Some Aspects about the Adsorption of Quinoline on Fibrous Silicates
26
27 and Patagonian Saponite. Appl. Clay Sci. 2006, 33, 142-148.
28
29
(32) He, H. B.; Li, B.; Dong, J. P.; Lei, Y. Y.; Wang, T. L.; Yu, Q. W.; Feng, Y. Q.; Sun, Y. B.,
30
31
32 Mesostructured Nanomagnetic Polyhedral Oligomeric Silsesquioxanes (POSS) Incorporated
33
34 with Dithiol Organic Anchors for Multiple Pollutants Capturing in Wastewater. ACS Appl.
35
36
37 Mater. Interfaces 2013, 5, 8058-8066.
38
39 (33) Zhang, L.; Li, X.; Wang, M.; He, Y.; Chai, L.; Huang, J.; Wang, H.; Wu, X.; Lai, Y., Highly
40
41 Flexible and Porous Nanoparticle-Loaded Films for Dye Removal by Graphene Oxide-
42
43
44 Fungus Interaction. ACS Appl. Mater. Interfaces 2016, 8, 34638-34647.
45
46 (34) Hu, H.; Wang, Z.; Pan, L., Synthesis of Monodisperse Fe3O4@silica CoreShell
47
48 Microspheres and their Application for Removal of Heavy Metal Ions from Water. J. Alloys
49
50
51 Compd. 2010, 492, 656-661.
52
53 (35) Chen, D.; Zhu, H.; Yang, S.; Li, N.; Xu, Q.; Li, H.; He, J.; Lu, J., Micro-Nanocomposites in
54
55
56
Environmental Management. Adv. Mater. 2016, 28, 10443-10458.
57
58
59
60
38
ACS Paragon Plus Environment
Page 39 of 42 ACS Applied Materials & Interfaces

1
2
3
(36) Zou, Y.; Wang, X.; Khan, A.; Wang, P.; Liu, Y.; Alsaedi, A.; Hayat, T.; Wang, X.,
4
5
6 Environmental Remediation and Application of Nanoscale Zero-Valent Iron and Its
7
8 Composites for the Removal of Heavy Metal Ions: A Review. Environ. Sci. Technol. 2016,
9
10
11
50, 7290-7304.
12
13 (37) Long, G.; Zhu, P.; Shen, Y.; Tong, M., Influence of Extracellular Polymeric Substances
14
15 (EPS) on Deposition Kinetics of Bacteria. Environ. Sci. Technol. 2009, 43, 2308-2314.
16
17
18 (38) Tang, X.; Liu, S.; Zhang, Z.; Zhuang, G., Identification of the Release and Effects of AHLs
19
20 in Anammox Culture for Bacteria Communication. Chem. Eng. J. 2015, 273, 184-191.
21
22 (39) Chen, Q.; Qu, L.; Tong, G.; Ni, J., Simultaneous Nutrients and Carbon removal from Low-
23
24
25 Strength Domestic Wastewater with an Immobilised-Microorganism Biological Aerated
26
27 Filter. Water Sci. Technol. 2011, 63, 885-890.
28
29
(40) Li, G.; Zhu, W.; Zhang, C.; Zhang, S.; Liu, L.; Zhu, L.; Zhao, W., Effect of a Magnetic Field
30
31
32 on the Adsorptive Removal of Methylene Blue onto Wheat Straw biochar. Bioresour.
33
34 Technol. 2016, 206, 16-22.
35
36
37 (41) Cui, L.; Wang, Y.; Gao, L.; Hu, L.; Yan, L.; Wei, Q.; Du, B., EDTA Functionalized
38
39 Magnetic Graphene Oxide for Removal of Pb (II), Hg (II) and Cu (II) in Water Treatment:
40
41 Adsorption Mechanism and Separation Property. Chem. Eng. J. 2015, 281, 1-10.
42
43
44 (42) Ge, H.; Wang, C.; Liu, S.; Huang, Z., Synthesis of Citric Acid Functionalized Magnetic
45
46 Graphene Oxide Coated Corn Straw for Methylene Blue Adsorption. Bioresour. Technol.
47
48 2016, 221, 419-429.
49
50
51 (43) Wang, T.; Liu, W.; Xu, N.; Ni, J., Adsorption and Desorption of Cd (II) onto Titanate
52
53 Nanotubes and Efficient Regeneration of Tubular Structures. J. Hazard. Mater. 2013, 250,
54
55
56
379-386.
57
58
59
60
39
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 40 of 42

1
2
3
(44) Schulz, B., Ueber die Adsorption in Lsungen. Kmmel: 1908.
4
5
6 (45) Langmuir, I., The Adsorption of Gases on Plane Surfaces of Glass, Mica and Platinum. J.
7
8 Am. Chem. Soc. 1918, 40, 1361-1403.
9
10
11
(46) Bulut, Y., Removal of Heavy Metals from Aqueous Solution by Sawdust Adsorption. J.
12
13 Environ. Sci. 2007, 19, 160-166.
14
15 (47) Moretti, G.; Guidi, F.; Grion, G., Tryptamine as a Green Iron Corrosion Inhibitor in 0.5 M
16
17
18 Deaerated Sulphuric Acid. Corros. Sci. 2004, 46, 387-403.
19
20 (48) Morrison Jr, W. H.; Ho, E. Y.; Hendrickson, D. N., Reaction of Ferrocene with
21
22 Polyaromatic Molecules.. Pi.-Arene Bis ((.Pi.-Cyclopentadienyl) Iron) Dications. I.
23
24
25 Molecular Structures. J. Am. Chem. Soc. 1974, 96, 3603-3608.
26
27 (49) Ye, J.; Zhao, L.; Bogale, R. F.; Gao, Y.; Wang, X.; Qian, X.; Guo, S.; Zhao, J.; Ning, G.,
28
29
30
Highly Selective Detection of 2, 4, 6Trinitrophenol and Cu2+ Ions Based on a Fluorescent
31
32 CadmiumPamoate MetalOrganic Framework. Chem. - A Eur. J. 2015, 21, 2029-2037.
33
34 (50) Ma, Z. Y.; Guan, Y. P.; Liu, X. Q.; Liu, H. Z., Preparation and Characterization of
35
36
37 MicronSized NonPorous Magnetic Polymer Microspheres with Immobilized Metal
38
39 Affinity Ligands by Modified Suspension Polymerization. J. Appl. Polym. Sci. 2005, 96,
40
41
42 2174-2180.
43
44 (51) Singh, V.; Sharma, A.; Tripathi, D.; Sanghi, R., Poly (Methylmethacrylate) Grafted
45
46 Chitosan: An Efficient Adsorbent for Anionic aAzo Ayes. J. Hazard. Mater. 2009, 161,
47
48
49 955-966.
50
51 (52) Chen, J. P.; Wang, L., Characterization of Metal Adsorption Kinetic Properties in Batch and
52
53 Fixed-Bed Reactors. Chemosphere 2004, 54, 397-404.
54
55
56
57
58
59
60
40
ACS Paragon Plus Environment
Page 41 of 42 ACS Applied Materials & Interfaces

1
2
3
(53) Kausar, A.; Bhatti, H. N.; MacKinnon, G., Re-use of Agricultural Wastes for the Removal
4
5
6 and Recovery of Zr (IV) from Aqueous Solutions. J. Taiwan Inst. Chem. Eng. 2016, 59,
7
8 330-340.
9
10
11
(54) Reddy, M. S.; Sivaramakrishna, L.; Reddy, A. V., The Use of an Agricultural Waste
12
13 Material, Jujuba Seeds for the Removal of Anionic Dye (Congo Red) from Aqueous
14
15 Medium. J. Hazard. Mater. 2012, 203, 118-127.
16
17
18 (55) Mahmood, A.; Xia, W.; Mahmood, N.; Wang, Q.; Zou, R., Hierarchical Heteroaggregation
19
20 of Binary Metal-Organic Gels with Tunable Porosity and Mixed Valence Metal Sites for
21
22 Removal of Dyes in Water. Sci. Rep. 2015, 5.
23
24
25 (56) Liu, W.; Zhang, J.; Jin, Y.; Zhao, X.; Cai, Z., Adsorption of Pb (II), Cd (II) and Zn (II) by
26
27 Extracellular Polymeric Substances Extracted from Aerobic Granular Sludge: Efficiency of
28
29
Protein. J. Environ. Chem. Eng. 2015, 3, 1223-1232.
30
31
32 (57) Bai, Y.; Sun, Q.; Sun, R.; Wen, D.; Tang, X., Bioaugmentation and Adsorption Treatment of
33
34 Coking Wastewater Containing Pyridine and Quinoline Using Zeolite-Biological Aerated
35
36
37 Filters. Environ. Sci. Technol. 2011, 45, 1940-1948.
38
39 (58) Zhuang, H.; Han, H.; Xu, P.; Hou, B.; Jia, S.; Wang, D.; Li, K., Biodegradation of Quinoline
40
41 by Streptomyces sp. N01 Immobilized on Bamboo Carbon Supported Fe3O4 nanoparticles.
42
43
44 Biochem. Eng. J. 2015, 99, 44-47.
45
46 (59) Liu, Y.; Liu, J.; Zhang, A.; Liu, Z., Treatment Effects and Genotoxicity Relevance of the
47
48 Toxic Organic Pollutants in Semi-Coking Wastewater by Combined Treatment Process.
49
50
51 Environ. Pollut. 2017, 220, 13-19.
52
53 (60) Thomsen, A. B.; Henriksen, K.; Grn, C.; Mldrup, P., Sorption, Transport, and
54
55
56
Degradation of Quinoline in Unsaturated Soil. Environ. Sci. Technol. 1999, 33, 2891-2898.
57
58
59
60
41
ACS Paragon Plus Environment
 ACS Applied Materials & Interfaces Page 42 of 42

1
2
3
Table of Content (TOC):
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
1
ACS Paragon Plus Environment