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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

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ACS Applied Materials & Interfaces

Synergic Adsorption-Biodegradation by Advance Carrier for Enhanced Removal of High-strength Nitrogen and Refractory Organics Muhammad Ahmada, Sitong Liua, Nasir Mahmoodb, Asif Mahmoodc, Muhammad Alid, Maosheng Zhenge, and Jinren Nia* a

Department of Environmental Engineering, Peking University; Key Laboratory of Water and

Sediment Sciences, Ministry of Education, Beijing 100871, China. b

Key Laboratory for Green Chemical Technology of the Ministry of Education, School of

Chemical Engineering and Technology, Tianjin University; Collaborative Innovative Center of Chemical Science and Engineering (Tianjin), Tianjin 300072, China. c

Department of Physics, South University of Sciences and Technology, Shenzhen, P.R. China

d

Water Desalination and Reuse Center (WDRC), Biological and Environmental Science and

Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia. e

Resources and Environmental Research Academy, North China Electric Power University,

Beijing, China

KEYWORDS: Iron oxide, quinoline, adsorption-biodegradation, Anammox-AOB, Coking wastewater

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Abstract: Coking wastewater contains not only high-strength nitrogen but also toxic biorefractory organics. This study presents simultaneous removal of high-strength quinoline, carbon and ammonium in coking wastewater by immobilized bacterial communities composed of a heterotrophic strain Pseudomonas sp. QG6 (hereafter referred as QG6), ammonia-oxidizing bacteria (AOB) and anaerobic ammonium oxidation bacteria (Anammox). The bacterial immobilization was implemented with help of self-designed porous cubic carrier which created structured micro-environments including inner layer adaptive of anaerobic bacteria, middle layer suitable for co-aggregation of certain aerobic and anaerobic bacteria, and outer layer for heterotrophic bacteria. By coating of iron oxide nanoparticles (IONPs) on functional polyurethane foam (FPUF), the bio-carrier (IONPs-FPUF) could provide a good outer layer barrier for absorption and selective treatment of aromatic compounds by QG6, offer a conducive environment for anammox in the inner layer, and provided mutualistic environment for AOB in middle layer. Consequently, simultaneous nitrification and denitrification was reached with significant removal up to 322 mgL−1 (98%) NH4, 311 mgL−1 (99%) NO2 and 633 mgL−1 (97%) total nitrogen (8 mgL−1 averaged NO3 concentration was recorded in effluent), accompanied with an efficient removal of chemical oxygen demand by 3286 mgL−1 (98%) and 350 mgL-1 (100%) quinoline. This study provides an alternative way to promote synergic adsorption and biodegradation with help of modified bio-carrier which is of great potential for treatment of wastewater containing high-strength carbon, toxic organic pollutants and nitrogen.

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1. Introduction Coking wastewater has been widely noted for its severe pollution to environments. Coking wastewater contains various kinds of pollutants primarily composed of phenolics, cyanide, ammonia, aromatic hydrocarbons, and nitrogen-, oxygen-, and sulfur-containing heterocyclic compounds which pose severe threat to humankind.1-3 Quinoline, a heterogeneous aromatic compound is a notable organic pollutant among these compounds, which is highly toxic and mutagenic with very low biodegradability.4-5 Along with the toxic aromatic compounds, coking wastewater is also rich in nitrogen containing compounds (e.g. NH4, etc.) which promotes the growth of cyanobacteria and algae when coking wastewater is discharged into water bodies, ultimately leading to eutrophication.6 Therefore, to protect the environment and living organisms, there is a dire need to treat toxic coking wastewater prior to discharge into natural resources. Several strategies have been developed for the treatment of quinoline-containing coking wastewater, including physicochemical,7-9 biological,10-11 as well as biochemical,12-13 electrochemical,14-17 and multistep bio-physicochemical methods.18 Most of these techniques have been applied separately or integrated in a series of reactors/systems to remove multipollutants. Although physicochemical methods have been extensively reported with promising results19, limited application for nitrogen and carbon removal, high treatment cost, system complexity, and lack of proper management of toxic end-products are the main shortfalls that strongly limit their long-term application.4 Hence, biological methods are still preferable options because of the lower energy requirements and special capabilities in treatment and disposal of a variety of pollutants.20-24 However, most biological methods based on aerobic autotrophic (e.g. ammonia oxidizing bacteria AOB), anaerobic autotrophic (e.g. anaerobic ammonium oxidation, anammox) and

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aerobic/anaerobic heterotrophic bacterial communities have been reported as a treatment strategy but the sensitivity of these bacterial communities for refractory compounds (e.g. quinoline) and organic carbon,25-27 is a big hurdle in their efficient nitrogen removal performance. Contrarily, some functional bacterial strains have been reported that not only have ability to tolerate high level of refractory compounds but also can degrade them successfully.20,24 Pseudomonas sp. QG6 is one of them with excellent characteristics to efficiently biodegrade quinoline, but it could only partially convert ammonium to nitrogen gases. Hence, it is imperative to develop a novel synergistic adsorption−biodegradation treatment strategy that perform dual role by efficiently utilizing the functional adsorbents and bacterial strains for the successful treatment of coking wastewater. Synergistic adsorption−biodegradation treatment strategy can be developed by designing a carrier with functional bacteria (QG6, AOB and anammox) immobilized into selective layers of carrier. Immobilized QG6 bacteria in outer layer will adsorb and biodegrade refractory compounds (quinoline) and deliver toxin free wastewater to AOB and anammox in the inner layers. Hence, this pre-treatment strategy (immobilization of QG6 in outer layer of bacteria) would protect the later functional bacterial communities (AOB and anammox) from the lifethreatening effects by refractory compounds and organic carbon. Various traditional adsorbents such as fibrous silicates, Patagonian assonate, clay oxides, kaolinite and montmorillonite, activated carbon, and bagasse fly ash, etc., have been investigated for quinoline adsorption.28-31 In spite of versatile advantages of porosity, their desorption capacity hindered their real applications as a quinoline adsorbents. In contrast to traditional adsorbents, engineered structured-nanomaterials have received more attention due to their high surface area, easy and rapid adsorption-desorption rates.32-33 Among these smart nanomaterials, iron oxide nanoparticles (IONPs) and their composite has raised global attention due to unique

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and fascinating features such as high surface area and adsorption capabilities relative to other nanomaterials.34-36 However, IONPs have never been utilized as synergic adsorptionbiodegradation platform for functional bacterial communities growth and for the effective coking wastewater treatment. For effective bacterial propagation, the IONPs must be hybridized with a carrier having micro-characteristics (e.g. functional polyurethane foam, FPUF). This carrier will provide niche for the growth of bacterial communities that cannot be provided by IONPs alone. Therefore, combining micro-nano structured IONPs-FPUF together with immobilization of functional bacteria could provide the required novel synergistic adsorption−biodegradation treatment strategy for coking wastewater treatment. To achieve the best treatment protocol for coking wastewater, we combine the aforementioned functional bacteria in a single carrier for high-efficient treatment of coking wastewater containing high-strength toxic organics and nitrogen (Scheme 1). By coating IONPs on FPUF and further functionalizing with biotin, the synthesized IONPs-FPUF created excellent microenvironments friendly to synergy of QG6, ammonia-oxidizing bacteria AOB and anammox, which greatly enhanced the simultaneous removal of quinoline, carbonaceous material and ammonium.

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Scheme 1. Schematic illustration of IONPs-FPUF design and distribution of various bacterial communities; their working principal towards coking wastewater treatment. 2. Experimental Methods 2.1. Carrier synthesis and bacterial immobilization 2.1.1. Synthesis of FPUF. Functional Polyurethane Foam (FPUF), which has been previously designed by our research group (China Patent. 2005. CN1587106A) for the particular aim to create micro-environments for the subsequent growth of the multi-bacterial communities (aerobic and anaerobic). The porosity of the FPUF carrier was fashioned with a particular aim to inhabit the anaerobic bacterial communities in deep layers of the carrier where all bacterial communities could easily propagate their colonies. Similarly, the FPUF has been functionalized with additional groups which could maximize the adhesion of the bacterial communities (Table S1). By taking these

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advantages of the uniquely developed FPUF carrier, we further modified it for ultimate purpose of enhancing simultaneous adsorption-biodegradation. 2.1.1. Synthesis of IONPs. IONPs were prepared by using a solvothermal method. Typically, 1 g iron acetate, 15 mL NH4OH, 0.5 mL oleic acid, and 5 mL oleylamine were mixed for 1 h with the assistance of a magnetic stirrer. Subsequently, this mixture was transferred to a 25 mL Teflon-lined autoclave and the reaction was carried out at 200 °C for 12 h. Finally, the solid product was obtained by centrifugation and was washed thrice with water and ethanol. The product was then dried at 70 °C in a vacuum oven for 6 h. 2.1.2. Synthesis of IONPs-FPUFS. The IONPs-FPUF was fabricated through wet chemistry. Initially, a 15 mm cube of FPUF carrier which is self-made patented and have been successfully applied by our research group11 was cut and mounted in the IONPs solution (20 mg mL−1) that was mechanically stirred for one week at progressive mixing speeds and temperatures ranging from 80−200 rpm and 37−200 °C, respectively, to ensure homogeneous distribution and better adhesion of the IONPs. Furthermore, biocompatibility was conferred to the IONPs-FPUF by coating with biotin. 2.1.3. Bacterial strains. The strain QG6 was discovered and isolated by our research group.37 The sequence data for the strain QG6 has been deposited in the NCBI database under the accession number EF079075. The strain is also preserved in the Chinese Culture Collection Committee General Microbiology Centre under the accession number CGMCC No. 6813. The seed sludge of anammox and AOB bacteria was collected from the Shiyan Reservoir in Shenzhen City, located in southern China and was pre-enriched in a 5 L reactor in our laboratory.38-39

Anammox

bacteria

were

immobilized

on

the

IONPs-FPUF

carrier.

Approximately 25 mL of enriched anammox biomass was inoculated into the reactor using a

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syringe. Initially, the reactor was operated for 50 days to stabilize the anammox process and to establish an anammox bacterial biofilm on the carriers. Subsequently, the QG6 bacterial strain and AOB were inoculated into the reactor by using a syringe containing 25 mL of biomass with the aim to biodegrade quinoline and convert NH4 into NO2 by the respective species. 2.1.4. Experiment set-up and reactor operation. The whole experiment was performed in cylindrical Plexiglas reactor with an effective volume of 3 L filled with the IONPs-FPUF carriers (15 mm in size, filling ratio 40%) and was operated for 200 days for coking wastewater treatment. Whereas quinoline adsorption mechanisms in reactor was authenticated by separate batch adsorption experiment in Erlenmeyer glass flasks (250 mL) with three different types of carriers namely FPUF, IONPs-FPUF, and IONPs-FPUF@QG6 (the carrier with immobilized and developed biofilm of QG6 bacteria). The reactor was fed with synthetic wastewater and detail is given in Table S1. The quinoline containing wastewater was initiated after 50 days of stable reactor operation and supplied continuously for 200 days. The pollutants (NH4, NO2, quinoline and carbon) were provided separately in the influent throughout the reactor operation (The detail description of the synthetic wastewater has been provided in supporting information). 2.2. Adsorption experiments 2.2.1. Adsorption experiments. For adsorption experiments, 1g of 15 mm FPUF, IONPs-FPUF, and IONPs-FPUF@QG6 were shaken at 150 rpm with 200 mL of coking wastewater. For the adsorption kinetics experiments, batch experiment was performed at fixed quinoline concentration (50 mgL-1) with 1g of 15 mm FPUF, IONPs-FPUF, and IONPs-FPUF@QG6 in separate flasks (250 mL). Samples were taken out at specified time intervals i.e. 0, 15, 30, 60, 120, 240, 480, 1440, 2100 and 2800 min. For adsorption isotherm experiments, initial concentration of quinoline was varied from 25 to 350 mgL-1. All experiments were conducted at

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7.8 pH and 37 °C because of the suitability of these conditions for growth of anammox and AOB bacteria. 0.1 M NaOH and HCl solution was used to adjust the pH (7.8) of quinoline solution. All experiments were conducted in triplicate and results are expressed as mean±S.D. Samples were withdrawn after 4 h (HRT for reactor) and the concentration of remaining quinoline was determined (See schematic illustration in Figure S1). To determine the left over quinoline concentration in solution, centrifuged the solution at 10,000 rpm and the supernatant was analyzed using high performance liquid chromatography (HPLC). The adsorption capacity and removal efficiency were calculated by applying equation 1 and 2 respectively.40-42

q = R=

( )

(1)

( )

×100

(2)

Here, Ci and Ce are the initial and final concentrations of quinoline (mgL−1), qe is the adsorption capacity (mg g-1), R is the removal efficiency, W (g) is the dry weight of the adsorbent, and V is the volume (L) of the quinoline solution used.43 2.2.2. Quantitative analysis. Samples for quantitative analysis were collected twice per week from reactor. Quantitative analysis of quinoline (effluent concentration) was performed by using an HPLC system (Shimadzu LC10ADVP, SPD10AVP UV−Vis Detector; Rheodyne 7725i manual injector; Diamonsil C18 reverse-phase column, 250 mm, 4.6 mm, 5 mm). Methanol/water (volume ratio of 4:1) was used as the mobile phase at a flow rate of 1.0 mL min−1. The microbial growth of QG6 was monitored by measuring the optical density at 600 nm (OD600) and the concentrations of ammonium, nitrate, and nitrite were analyzed using a UVVisible (UV-Vis) spectrophotometer (UV-1750, SHIMADZU, Japan). The pH and dissolved

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oxygen (DO) were measured by using digital pH and DO meters, respectively (HACH, USA). All remaining measurements and methods used in this study were adopted from the protocol described in the Standard Methods for Examination of Water and Wastewater. 2.2.3. Microscopic analysis. For scanning electron microscope (SEM) and energy dispersive xray (EDX) analysis of samples from reactor, all of the samples were fixed with 2.5% glutaraldehyde in 0.1 M phosphate and dehydrated with increasing concentrations of ethanol, i.e. 50, 70, 80, 90, and 100%. After dehydration, the samples were dried by critical point drying or with hexamethyldisilizane (HMDS) and finally observed under SEM (Nova 200 NanoLab, USA). The topographic images were captured using multimode atomic force microscopic (AFM, Burker Nano, USA). Samples for fluorescence in-situ hybridization (FISH) analysis were fixed in 4% paraformaldehyde and dehydrated with increasing concentrations of ethanol. The 4,6-diamidino2-phenylindole (DAPI) and the oligonucleotide probes Pla46, AMX820, NmV and NSO190 were used for detection of all bacteria, planctomycetes, anammox, and AOB respectively; a confocal laser scanning microscope (A1R-si, Nikon) was used for the FISH analysis (probes details is provided in Table S2). 3. Results and Discussion 3.1. Characterizations of IONPs-FPUF. 3.1.1 Refinement of the microstructure. IONPs were coated over FPUF carrier to play a dual role i.e. adsorption-biodegradation. Hence the efficient coating was confirmed by using SEM and EDX analysis. Large sized pores of FPUF (Figure 1a), were reduced to relatively smaller pores after coating of IONPs on FPUF, which confirmed successful and uniform packing of the IONPs on FPUF (Figure 1b). Coating of IONPs on FPUF improved porosity (Table S4) that ultimately increased the water holding capacity of FPUF carrier that played a vital role for proper contact of

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wastewater with bacteria biofilm which could be clearly visualized by comparing structures of FPUF and IONPs-FPUF (Figure 1a, b). Moreover, after coating with the IONPs, the IONPsFPUF still possessed interconnected pores, and was wettable and permeable with an efficient mass diffusion capabilities. These properties helped to stimulate the growth of QG6, AOB and anammox by providing favorable environments for their mutualistic interactions and dynamics. To explore whether IONPs-FPUF efficiently form distinct zones for the growth of differential microbial communities, morphology of biofilm formed inside different layers of IONPs-FPUF was visualized using SEM. These results confirmed successful immobilization of functional bacterial communities in selective biofilms that could be clearly visualized in Figure 1c, d respectively. Rod and round shaped bacteria were grown in outer and middle layer of carrier confirming the growth of QG6 and AOB bacterial respectively (Figure 1c). On the other hand, growth of strongly aggregated coccoid shaped anammox bacteria in well-arranged colonies ensures efficient utilization of toxic quinoline by QG6 in preceding biofilm (Figure 1d). The dominant habitats of functional bacteria in sequential and differential zone of the IONPs-FPUF clearly confirmed the excellent refinement of the FPUF structure which adsorbed toxic quinoline on nanoparticles by acting as nanomebrane that ultimately diffused toxin free wastewater to AOB and anammox.

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Figure 1. SEM images: (a) blank FPUF, (b) IONPs-FPUF (the insets show the high magnification images of marked areas, representing efficient coating of IONPs), (c) immobilization of bacterial biomass (QG6) on IONPs-FPUF (the inset shows the high magnification images of marked areas exposing growth of rod shaped morphology of QG6, hereafter referred as IONPs-FPUF@QG6), and (d) formation of anammox biofilm in inner layer of the IONPs-FPUF (the insets show the high magnification images of marked which represent high co-aggregation and networking capabilities of bacterial communities).

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3.1.2. Topographical and porosity analysis. The topographic features (surface roughness, porosity and isotherm) of the IONPs-FPUF were further analyzed using AFM and BET to investigate the suitability of the IONPs-FPUF for adsorption and bacterial adhesion. The BET data indicated that the IONPs-FPUF is composed of a well-arranged network of IONPs with uniformly sized pores with an average pore size of ~3.17 nm (Figure 2a), which enhances the carrier adsorption properties (Table S4) and bacterial adhesion ability (Figure S6) and ultimately favors Langmuir-type adsorption, as indicated by the isotherm model applied herein (Figure 2b, S2 and Table S4). IONPs-FPUF possessed high roughness (1.42) and a uniform structure which ascertained high bacterial adhesion on the carrier surface by yielding refined membrane like biofilm with larger protected surface area (~610 m2 g-1) (Figure 2c). Along with roughness, IONPs-FPUF surface symmetry was also determined in terms of skewness and kurtosis. Negative skewness values and smaller kurtosis values show that surface is dominated by ridges thus providing space for bacterial adhesion over IONPs-FPUF (Figure 2c). From topographical analysis of biofilm formed over carrier surface it is clear that surface of biofilm is highly rough with more negative skewness value favoring further pollutants adsorption, bacteria adhesion and colonization (Figure 2d). Taken together these results demonstrated that coating of IONPs improved surface features of the IONPs-FPUF which ultimately boost up the adsorption and growth of microbial community into their selective environments.

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Figure 2. Carrier topographical and adsorption characteristics; (a) pore size distribution, (b) adsorption isotherm, (c) high roughness topography of IONPs-FPUF before bacteria immobilization, (d) high roughness topography of IONPs-FPUF after bacteria immobilization. (Ra, Ssk, Sku indicate surface roughness, skewness and kurtosis respectively) 3.1.2. Spectroscopic characterization. Surface elemental quantification of FPUF and IONPsFPUF was done using EDX analysis. The core level spectra of all the elements indicate high

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purity of FPUF as shown in Figure 3a. The inset of Figure 3a shows the weight and atomic percentages of all the detected elements. Figure 3b shows the presence of an additional peak corresponding to iron, which confirms the efficient coating of the IONPs on the FPUF surface.

Figure 3. EDX analysis of (a) FPUF (the inset shows elemental values in percent) and (b) IONPs-FPUF (the inset shows elemental values in percent and high resolution spectra of lower energy part with clear visualization of the peaks). 3.2. Adsorption experiments. SEM, AFM and BET characterization predict IONPs–FPUF to be a potential candidate for adsorption, therefore a comparative study to differentiate the adsorption capabilities of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 was done. A linear relationship was observed between the quinoline concentration and the adsorption capacity of the carriers where adsorption capacity increased with increase in quinoline concentration (Figure 4). The quinoline adsorption followed the following order on the developed carriers: IONPsFPUF@QG6 (90 mg g−1) ˃ IONPs-FPUF (80 mg g−1) ˃ FPUF (70 mg g−1). High adsorption on the surface of IONPs-FPUF@QG6 could be attributed to the suitable porosity and high surface

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area of the IONPs-FPUF@QG6 carrier (Table S4). Similarly, limited presence of surface functional groups on pure FPUF could possible lowered their adsorption capacity. Taken together, these results validate the efficiency of the IONPs-FPUF@QG6 carrier as a good adsorbent and the enhancing effect of IONPs. The adsorption capacity of the carrier increased quickly with increasing concentration of quinoline in the influent solution due to an increase in the driving force of the quinoline gradient. This ultimately enhanced the interactions between quinoline and the IONPs-FPUF@QG6 adsorbent. Further increase of quinoline concentration beyond 350 mgL-1 did not significantly enhance adsorption on the FPUF and IONPs-FPUF due to exhaustion in binding sites, whereas adsorption capacity of IONPs-FPUF@QG6 did increase with involvement of QG6 bacteria in adsorption process. To illustrate the fact that quinoline adsorption by IONPs-FPUF did not increased beyond 350 mgL-1, adsorption capacity of IONPsFPUF was evaluated at 500 mgL-1 and compared with IONPs-FPUF@QG6. No more adsorption could be seen in case of IONPs-FPUF (Figure 4) on further increment in quinoline concertation from 350 to 500 mgL-1, whereas adsorption capacity of IONPs-FPUF@QG6 continue to increase confirming the involvement of QG6 bacteria in simultaneous adsorption and biodegradation process which spontaneously provided vacant spaces in carrier to adsorb quinoline continuously.

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Figure 4. Comparison of adsorption capacity of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 at different quinoline concentrations. The inset represents the magnified adsorption capacity of IONPs-FPUF and IONPs-FPUF@QG6 in region of 60-100%. 3.2.1. Isothermal models. To understand the nature of the interaction between the adsorbate (quinoline) and adsorbent for removal of organic pollutants, the adsorption isotherms were applied. An adsorption isotherm describes the relationship between the amount of adsorbate taken up by the adsorbent and the adsorbate concentration remaining in solution. In the present study, the Freundlich and Langmuir adsorption nonlinear models were applied to further investigate the adsorption of quinoline on the FPUF, IONPs-FPUF and IONPs-FPUF@QG6 (Figure 5). The Freundlich isotherm model (Eq. 3)44 indicates heterogeneity of the surface and favorable multilayer adsorption:

=

(3)

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Here, (mg g−1) is the Freundlich equation constant related to the adsorption capacity, and n is the intensity factor. On the other hand, the Langmuir isotherm is applied considering the maximum adsorption of the solute with saturated monolayer coverage of the solute molecules over the adsorbent surface, with no transmigration of the solute/adsorbate in the plane of the adsorbent surface, and is represented by Eq. 4.45,46

=

(4)

Here, (mgL−1), (mg g−1) is the equilibrium concentration of quinoline and corresponds to equilibrium adsorption,

!

(mg g−1) is the maximum adsorption capacity, and b (L mg−1) is the

Langmuir constant that represents the affinity of quinoline for the adsorbents and is obtained from a plot of

against the equilibrium concentration . The results (simulated curves) of

Langmuir and Freundlich models are given in Figure 5. The Langmuir isotherm best described the adsorption characteristics of the FPUF, IONPs-FPUF and IONPs-FPUF@QG6, indicating the homogeneity of the surfaces of FPUF, IONPs-FPUF and IONPs-FPUF@QG6. The maximum theoretical adsorption capacity ( ! ) of the IONPs-FPUF@QG6 was 125 mg g−1 from the Langmuir model (Table 1). A strong correlation between experimental and theoretical adsorption capacities (!" ) and higher coefficients (R2) ˃0.9 values for FPUF, IONPs-FPUF and IONPs-FPUF@QG6 confirmed the validity of the Langmuir model. The applicability of the Langmuir isotherm model indicated that the adsorption of quinoline occur by monolayer coverage, i.e. quinoline is chemically adsorbed over the FPUF, IONPs-FPUF and IONPsFPUF@QG6 at a well-defined, fixed number of binding sites, with only one adsorbate species at each site, and without any type of interaction among the adsorbed quinoline molecules; all

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binding sites are energetically equivalent. These facts indicate that the mechanism of quinoline adsorption is chemosorptive.

Figure 5. Non-Linearized, Langmuir (dashed lines) and Freundlich (solid lines) isothermal models for quinoline adsorption. Furthermore, feasibility and spontaneity of adsorption of quinoline was determined by calculating value of Gibbs free energy (∆Go) using equation 5: ∆G% = &RT lnK +

(5)

Here, Kc is the adsorption equilibrium constant and T is the absolute temperature. The ∆Go values for the overall process were −10, −29, and −38 kJ·mol−1 for the FPUF, IONPs-FPUF and IONPs-FPUF@QG6, respectively. The negative value of ∆Go clearly confirmed that the adsorption process is spontaneous at room temperature and pressure. Moreover, negative values of ∆Go imply a greater driving force and show that the adsorption of quinoline by IONPsFPUF@QG6 is highly favorable. 19



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In addition to predicting the spontaneity of the reaction, the ∆Go values were also used to predict the mechanism of adsorption (e.g. physisorption, chemisorption, etc.,) on the FPUF, IONPs-FPUF and IONPs-FPUF@QG6 surface. It is well established that less negative ∆Go values (−20 kJ mol−1) for the adsorption reaction correspond to physisorption, whereas adsorption with highly negative ∆Go values (−40 kJ mol−1) follow chemisorption.47 The ∆Go values obtained for the present system (−10, −29, and −38 kJ mol−1) were more negative, which demonstrates that adsorption on the carrier surface followed the chemisorption mechanism and verifies the results presented above. A possible mechanism for chemisorption on the surface of the carrier may involve transfer of π-electrons from the organic molecules to the vacant d-orbital of the metal (iron) to form a bond. Chemisorption of the organic molecules on the carrier surface leads to strong binding and homogenous coating of the carrier surface, further confirming the validity of the Langmuir adsorption model for the present system.48-50 Table 1. Comparison of non-linearized Langmuir and Freundlich isotherm models for quinoline adsorption over FPUF, IONPs-FPUF and IONPs-FPUF@QG6 Model

IONPs-FPUF@QG6

IONPs-FPUF

FPUF

R2

*qmax (mg g-1)

R2

*qmax (mg g-1)

R2

*qmax (mg g-1)

Langmuir Isotherm

0.995

125

0.997

100

0.994

32

Freundlich Isotherm

0.886

69.84

0.785

57.66

0.927

30

**qexp (mg g-1) -1

∆G° (kJ·mol )

98.6

78.11

29.50

-38

-29

-10

* Equilibrium adsorption capacity calculated from Equations 3 & 4 ** Experimental adsorption capacity at equilibrium

20


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3.2.2. Kinetics experiments. The kinetics of quinoline adsorption on the surface of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 surface was further evaluated using time-dependent adsorption studies, and batch experiments were conducted from 0 to 2800 minutes (min). For the FPUF, equilibrium was attained within 360 min whereas the adsorption efficiency for IONPFPUF carrier increased consistently up to 480 min. After attaining equilibrium after 480 min, no more increase in adsorption capacity was observed up to 2800 min. In contrast, the IONPsFPUF@QG6 demonstrated relatively dominant removal performance which did not reach equilibrium up to 2800 min. Much faster adsorption of quinoline was observed up to 750 min (Figure 6) due to the availability of a large number of adsorption sites that quickly adsorb the molecules from the effluent solution. However, with time, the number of available sites on the carrier tends to decrease, leading to reduced adsorption (equilibrium phase) after the carrier is exposed to the effluent for longer durations.51-52 After 750 min adsorption process was slow down on the IONPs-FPUF@QG6 carrier because quinoline adsorbed by the IONPs-FPUF@QG6 moves inside the carrier and is degraded by the QG6 bacteria, making the adsorption sites available for further adsorption of quinoline. In contrast to other carriers, the removal efficiency of IONPs-FPUF@QG6 increased with time due to adsorption of quinoline and its subsequent degradation by the bacterial communities.

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Figure 6. Effect of time on quinoline adsorption by FPUF, IONPs-FPUF and IONPsFPUF@QG6 (pH = 7.8, temperature = 37 °C, Ci = 350 mgL-1, and stirring speed = 150 rpm. 3.2.3. Kinetics models. The kinetics data for quinoline adsorption was fitted to pseudo-first order and pseudo-second order kinetic models. The pseudo-first order model only describes the adsorption based on the concentration of quinoline in the solution, whereas the adsorption process involves reversibility in the form of an equilibrium between the adsorbate and adsorbent surface.53 In most cases, the pseudo-first order kinetic model is not applicable to the data and the following relationship is thus used: log(q ./ & q 0 )

1%2 /34 56

(6)

7.9:9 × 0

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Here, k1 (min−1), ; (mg g−1), and (mg g−1) are the pseudo-first-order adsorption rate constant, the amount adsorbed at time t (min), and the amount adsorbed at equilibrium, respectively. The k1 and values were obtained from the plot of

=

?@

@

A B C

(7)

Here, k2 (g mg−1 min−1) is the adsorption rate constant; k2 and qe can be obtained from the C

intercept and slope of the plot of D versus t.30, 55-56 The value of qe for a given initial quinoline concentration was determined, whereas the adsorption rate constants (k1 & k2) were evaluated from the intercepts of the graph (Figure 7) and are summarized in Table 2 along with the R2 values. The applicability of the kinetic models was determined in terms of the correlation coefficients (R2). The adsorption values obtained for the pseudo-second order kinetic model were consistent with the experimental values, as shown in Table 2. Mechanistically, the chemisorption of quinoline on carrier surface might be due to the interaction between heterocyclic nitrogen and hydroxylated surface of oxide. Another possibility for adsorption is the donor-acceptor relationship between iron and quinoline, given that the transition metal iron possesses vacant d-orbitals and quinoline possesses π-electrons and thus can act as an electron donor while iron acts as an acceptor.

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Table 2. Parameters of Pseudo-First-Order and Pseudo-Second-Order kinetic models for quinoline adsorption by FPUF, IONPs-FPUF and IONPs-FPUF@QG6. Kinetic model

Pseudo-first order

Pseudo-second order

Parameters

R2

k1

*qmax (mg g-1)

R2

*qmax (mg g-1)

k2

IONPs-FPUF

0.54

2.3×10 -04

42.01

0.999

30.13

3.0×10- 03

FPUF

0.43

4.6 × 10 -04

40.12

0.999

29.41

1.1×10- 03

IONPs-FPUF@QG6

0.57

2.1×10- 04

44

0.999

30

2.5×10- 03

**qexp (mg g-1)

28.6

28.6

* Equilibrium adsorption capacity calculated from equation 6 and 7 ** Experimental adsorption capacity at equilibrium

Figure 7. Linearized pseudo-first (a) and second order (b) kinetics model for quinoline adsorption by FPUF, IONPs-FPUF and IONPs-FPUF@QG6. 3.3. Spectroscopic analysis of adsorbents. Adsorption of quinoline was further confirmed using Fourier Transform Infrared (FTIR) and Raman spectra of FPUF, IONPs-FPUF and IONPsFPUF@QG6 with and without quinoline loading/adsorption at natural pH (Figure 8a). Peaks centered at 1594 cm-1 (C=O), 1302 cm-1 (C-O), 3435 cm-1 (O-H) confirmed the presence of

24


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oxygen containing functional groups in all types of adsorbents. Comparing the absorption bands of modified carriers with FPUF carrier, a clear suppression in peaks associated with C-O and C=O bond is observed that is clear representation of involvement of these two functional groups in adsorption of quinoline, maximum suppression in peak height was observed in case of IONPsFPUF@QG6 favored highest adsorption of quinoline over its surface. Surface elemental analysis of IONPs-FPUF@QG6 before and after the adsorption experiments was carried out using EDX elemental analysis to further confirm adsorption of quinoline. Figure 8b shows the EDX data for the IONPs-FPUF@QG6 after adsorption of quinoline, the detection of nitrogen (a part of the heterocyclic structure of quinoline) in addition to the original elements Figure 3b of the IONPs-FPUF indicates adsorption of quinoline on the IONPs-FPUF@QG6. These results were further authenticated by Raman spectra in which relatively high and clear peaks of quinoline were appeared at 1380 cm-1 in IONPs-FPUF@QG6 that consequently shifted in others adsorbents (Figure S3).

Figure 8. (a) FTIR spectra of FPUF, IONPs-FPUF and IONPs-FPUF@QG6 (before and after quinoline adsorption and (b) EDX analysis of IONPs-FPUF@QG6 (the inset shows the high resolution of lower energy area part of EDX spectra).

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3.4. Biodegradation capabilities of the functional bacteria (QG6) To investigate more specific functions and activities of the QG6, a batch experiment was performed in a flask for a period of 24 h. The results presented here, clearly indicate strong biodegradation ability of QG6 due to complete removal of 350 mgL-1 quinoline within 16 h (Figure 9a). Very interestingly, straightforward comparison between quinoline adsorption and biodegradation demonstrated that the QG6 has higher biodegradation rates than IONPs-FPUF adsorption which strongly verified the effectiveness of the synergic adsorption-biodegradation process for efficient removal of aromatic and nitrogenous compounds. On the other hand, QG6 also showed significant potential for transformation of NH4 into NO3, which again proves to be a readily available nutrient source for QG6 that helped to speed up QG6 metabolism and bioactivities (Figure S4). The rapid growth of QG6 was shown to be positively correlated with increased rate of quinoline biodegradation which was quite higher than that of AOB and anammox bacteria (Figure 9a). This correlation proven to be a very useful to enhance the favorable environments for the AOB and anammox communities by preventing the penetration of toxic quinoline in inner layers of the carrier (Figure 9b). For instance, QG6 and AOB require oxygen to biodegrade quinoline and NH4 into NO2; in this way, these bacteria provided nutrient support (NO2) to the anammox which is a necessary nutrient for complete removal of NH4 into N2 gas. In a similarly fashion, the development of thick adsorbent and QG6-AOB biofilms on outer layers kept strictly anaerobic environment for anammox, as anammox specific activities are totally dependent on anaerobic conditions. Such ideal environment is the basic reason behind ideal functionality of the anammox communities which otherwise have been proved very difficult to maintained such an efficient environment.

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Figure 9. (a) Biodegradation of quinoline by QG6 and growth of the bacteria with time, (b) quinoline profile within different layers (zones) of the carrier To witnessed the progressive growth of the QG6, FISH images were acquired by analyzing QG6 biofilm at different duration of the experiment. Figure 10a− −d is promptly evident of dynamic and continual growth of QG6 with passage of time which sequentially tend to strong

27



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co-aggregation on 200th day of the experiment (Figure 10d). These results strongly authenticate our batch experiment for quinoline adsorption and biodegradation. In fact, the effective structure of the carrier synergistically blocked aromatic pollutants and bear their heavy shock loads which ultimately given an excellent opportunity to QG6 for rapid biodegradation of quinoline into NH4 and distributed equal nutrients to the AOB and anammox bacterial communities.

Figure 10. Confocal laser scanning microscopy images showing continuous and progressive growth of QG6 within IONPs-FPUF, (a) 0 day (when inoculum was immobilized in carrier), (b) 65 days, (c) 100 days, (d) 200 days

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3.5

The protective role of the adsorbent; growth of the functional bacteria

The successive growth of AOB and anammox in the inner layers of IONPs-FPUF carrier was characterized using FISH analysis to assess the role of the adsorbent as a protective layer. Initial analysis of inoculum showed the dominant abundance of anammox bacterial communities inside carrier (Figure 11a) which gradually reached to stable growth within 50 days of reactor operation. The improved microbial community structure (Figure 1) and nitrogen removal performance (Figure 12, removal rate reached to 60 mgL-1) implied that the immobilization of the QG6 and AOB would be of primary importance to enhance the role of both adsorbent and functional bacteria by synergetic adsorptionbiodegradation. The significant removal of quinoline and nitrogen was achieved during 50−65 days of reactor operation which led us to confirm the relative growth of the newly immobilized bacterial communities. The microbial community analysis on 65th day of reactor operation provided clear indication of the successful immobilization of QG6 and AOB (Figure 10c and 11b). Furthermore, the reactor operation was extended to longer period to confirm the stable growth of microbial communities. A relatively higher concentration of the AOB and anammox was observed after 100 days of operation (Figure 11b). The further increasing growth of the AOB and anammox population clearly demonstrated that the poisonous quinoline is adsorbed on the outer layer prior to contact of the influent with them. The bacterial population continued to multiply, and after 200 days of operation, a much larger population of bacterial communities was observed (Figure 11d). In addition, these 3-dimensional (3D) images confirm that the segregated bacterial communities were present on the carrier surface. Thus, the existence of such differential bacterial communities effectively removes the toxic quinolone by degrading it into NH4 and NO2 which were further transformed by AOB and anammox bacterial communities (Figure S5) via

29



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well-organized teamwork without affecting the bacterial growth. This makes the unique carrier a

very strong candidate for efficient treatment of refractory compounds, organic carbon and ammonium from coking wastewater.

Figure 11. Confocal laser scanning microscopy images showing continuous and progressive growth of different bacterial communities within IONPs-FPUF, (a) 0 day, (b) after 65 days, (c) 100 days, (d) 200 days (red and green represent anammox and AOB bacteria, respectively). 3.6 Nitrogen conversion performance of functional bacteria (AOB and anammox) To further validate the efficacy of the AOB and anammox bacterial communities, nitrogen (resulted from the biodegradation of quinoline as well supplemented in wastewater e.g. NH4, NO2, NO3) conversion rates were monitored over the period of 200 days. The anammox showed limited initial capability for nitrogen removal (~15−17%), which can be attributed to the lower

30


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population of anammox bacteria in the carrier during start-up phase. However, a gradual increase in the anammox bacterial population resulted stability in the biological process which consequently enhanced nitrogen removal performance. The enhanced activity with passage of time is clear from the 60% removal of NH4 and NO2 achieved after few days of operation, which is approximately 3-times greater than most of the start-up process, providing clear indication of the good adsorption and bacterial adhesion capabilities of the IONPs-FPUF carrier. The improved performance further demonstrates that the anammox bacteria are free from quinoline poisoning, given that quinoline is adsorbed in the adjacent layer prior to contact of the effluent with anammox. The removal of nitrogen increased continuously with an increase of the anammox bacterial population, and after 100 days of operation, the NH4 and NO2 removal efficiencies exceeded 90% with a record hydraulic retention time (HRT) of 6 h (Figure 12). Furthermore, a high chemical oxygen demand (COD) removal rate was achieved (98% @ 3286 mgL−1) and was found to be consistent and stable to the end of experiment (200 days). Hence, the current design proved to be very beneficial for preservation of the anammox bacterial communities that were killed in other systems when exposed to organic carbon (Figure 12c). Previous literature reveals that carbon removal from wastewater is required before feeding the wastewater to anammox treatment systems that was done in-situ in present design (Scheme 1). The high removal performance (C, N, and quinoline) achieved herein is due to the combination of successful adsorption, carbon removal, quinoline biodegradation, and an absolute anaerobic habitat zone within the inner layers of this novel carrier. After 50 days, when quinoline was added in wastewater, negligible inhibition was observed on the performance of the bacterial community (Figure 12b, c), which was recovered steadily as QG6 growth increased that ultimately enhanced quinoline removal. In fact, quinoline removal increased steadily due to the

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adsorption layers inside the novel carrier that helped to offset sudden and toxic shocks to the bacteria by the inhibitors and pollutants.

Figure 12: Nitrogen removal performance over entire period of study: (a) removal rate (the inset shows zoomed removal rates of ammonium, nitrite and nitrate), (b) ammonium removal efficiency, (c) NO2 removal efficiency and (d) COD removal rate. Different colors represent different phases of the bioreactors operation as labelled in the Figures. In addition to the higher efficiency for removal of toxic organic and inorganic species from the contaminated water, the developed carrier also presents a plausible solution for overcoming the “granular floating issue”. Generally, the developed granules involving anammox species possess

32


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very low density due to entrapped nitrogen gas and float on the surface of water, which limits their activity. It is speculated that the increase in the density arising from the decomposition of quinoline and nitrogen species enhances the biomass of QG6, AOB, and anammox, and the proper creation of micro-channels facilitates regular emission of nitrogen gas. After 180 days of operation, the total nitrogen removal efficiency reached to 97%, which remained almost steady throughout the remaining period of the study (200 days). Although the nitrogen loading rate increased with a gradual decrease of the HRT, along with a subsequent increase of the influent nitrogen concentration, the performance of the reactor became progressively stable. According to our best knowledge, the removal rates of quinoline, carbon and nitrogen are better than previous literature documented for simultaneous adsorption and biodegradation (Table S5,6).57-60 CONCLUSIONS A unique strategy was established for highly efficient treatment of coking wastewater containing high-strength bio-refractory compounds, organic carbon and nitrogen by novel carrier with high surface area derived from the nanostructured IONPs coated on FPUF. As-synthesized IONPsFPUF acts as an effective support for the growth of functional bacterial communities for synergistic adsorption and biodegradation of quinoline. QG6 was incorporated on the outer surface of the carrier to convert the ammonium to nitrogen gas, AOB and anammox were incorporated in the inner layers of the carrier. This design successfully protected the functional bacterial communities from the toxic effects of quinoline and provides a highly favorable environment to enhance the simultaneous adsorption-biodegradation. The efficiently coupled adsorption and biodegradation process gave high removal of NH4, NO2, quinoline and chemical oxygen demand up to 322 mgL−1 (98%), 311 mgL−1 (99%), 350 mgL-1 (100%) and 3286 mgL−1 (98%), respectively, along with 633 mgL−1 (97%) total nitrogen (8 mgL-1 averaged NO3 33



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concentration was recorded in effluent). We strongly believe that the current work will add a new dimension to the search for highly active, biocompatible carriers for removal of mixed pollutants from different types of wastewater by enhancing synergic adsorption-biodegradation. ASSOCIATED CONTENT Supporting Information. The part of experimental design and FISH images. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author * Jinren Ni ([email protected]) Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. ACKNOWLEDGMENTS The authors highly appreciate the National Science Foundation of China (NO. 51539001) for providing financial support for this study.

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