Anaerobic nano zero-valent iron granules for hexavalent chromium removal from aqueous solution

Environmental Technology & Innovation 16 (2019) 100495

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Anaerobic nano zero-valent iron granules for hexavalent chromium removal from aqueous solution Ravikumar Konda Venkata Giri a , Liji Susan Raju a , Yarlagadda Venkata Nancharaiah b,c , Mrudula Pulimi a , Natarajan Chandrasekaran a , ∗ Amitava Mukherjee a , a

Centre for Nanobiotechnology, VIT University, Vellore, Tamil Nadu, India Biofouling and Biofilm Processes Section, Water and Steam Chemistry Division, Bhabha Atomic Research Centre, Kalpakkam, 603102, Tamil Nadu, India c HomiBhabha National Institute, Anushakti Nagar, Mumbai 400 094, India b

article

info

Article history: Received 31 March 2019 Received in revised form 19 September 2019 Accepted 21 September 2019 Available online 23 September 2019 Keywords: Anaerobic NZVI granules Box–Behnken design Pseudo-second-order Residual toxicity Cr (VI)-spiked natural water

a b s t r a c t The current study reports environmental application of zero-valent iron nanoparticles (NZVI)-laden anaerobic microbial granules for the removal of a major environmental pollutant, Cr (VI), from aqueous solutions. The anaerobic NZVI granules were characterized using X-ray diffraction, SEM, EDX, and FTIR analyses. For Cr (VI) removal experiments, Box–Behnken Design (BBD) with three-level factors was applied. The three operating variables, with the highest influence on Cr(VI) removal were initial concentration of Cr(VI), reaction time, and anaerobic NZVI granule dry weight. A very high removal capacity of 296.7 ± 1.82 mg/g was observed with the optimized conditions (Cr (VI) Initial concentration: 10 mg/L; anaerobic NZVI granule weight dry weight: 50 mg; reaction time: 90 min). The reduction kinetics followed pseudo-second-order model. The residual toxicity of the effluent solution after treating with the anaerobic NZVI granules was examined using microalgae, artemia, and Allium bioassays, proving a significant detoxification obtained using the process. The feasibility of using the anaerobic NZVI granules for removal of Cr (VI) from real water systems was further confirmed using groundwater and lake water samples spiked with Cr (VI). The Cr (VI) removal was noted at 88 ± 1.56 % with 231.7 ± 1.21 mg/g capacity, whereas in the lake water, they were estimated to be 79 ± 1.94 % and 217 ± 0.91 mg/g respectively, with the optimized conditions (Cr (VI) concentration added in real water system: 10 mg/L; anaerobic NZVI granule dry weight: 50 mg; reaction time: 90 min). © 2019 Elsevier B.V. All rights reserved.

1. Introduction The prevalence of heavy metals in natural water is a matter of serious concern because of their detrimental impact on the environment and human health (Zeitoun and Mehana, 2014; Khalid et al., 2018). Among them, hexavalent chromium [Cr(VI)] is a known carcinogenic and considered to be a serious hazard to human health (DeFilippi, 2018). The World Health Organization (WHO) has declared the permissible limit of Cr(VI) in potable water to be 0.05 mg/L (Kitkaew et al., 2018). A considerable amount of effort has already gone into designing various conventional Cr (VI) removal techniques using ∗ Correspondence to: Centre for Nanobiotechnology, Vellore Institute of Technology, Vellore 632014, India. E-mail addresses: [email protected], [email protected] (A. Mukherjee). https://doi.org/10.1016/j.eti.2019.100495 2352-1864/© 2019 Elsevier B.V. All rights reserved.

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different processes, such as filtration, electrochemical, precipitation, ion exchange, adsorption, and reduction (Kitkaew et al., 2018; Suksabye et al., 2008; Benito and Ruiz, 2002; Kongsricharoern and Polprasert, 1995; Rengaraj et al., 2001). Recently nano particles like alumina-supported copper aluminium oxide (Bhusari et al., 2019), Ti3+ self-doped TiO2 nanoparticles (Hao et al., 2019), ZnO-TiO2 doped polyacrylonitrile nano fibre-Mat (Parlayıcı et al., 2019), and diatomite supported NZVI (Zhang et al., 2019) were used for removing Cr(VI) from the aqueous solutions to improve the efficiency of the conventional methods (Leblebici et al., 2018). In the past few years, nZVI is extensively used for removing contaminants like heavy metal [Cr(VI)] by precipitation (Cao and Zhang, 2006) and nitrates by reduction (Wang et al., 2006). nZVI has several advantages over micron sized ZVI particles, as they are smaller in size and hence possess higher specific surface area, higher density of reactive sites, and this would significantly improve the removal efficiency of target contaminants (Deng et al., 2018; Eljamal et al., 2018). NZVI is also known to possess sufficient environmental mobility, very good reactive longevity, and quite low toxicity (Zou et al., 2016). Additionally, nZVI can be injected directly into contaminated aquifers (Jang et al., 2014). Therefore, the nZVI has been widely used in on-site treatment processes for removal of Cr(VI) (Mueller et al., 2012). Hence for environmental applications, nanoscale zero-valent iron (NZVI) is considered as a forerunner among the other materials. Hence nZVI-based environmental technologies provide promising and efficient alternative for traditional ground water remediation techniques (Diao et al., 2018; Dong et al., 2018; Song et al., 2019; Lefevre et al., 2016). Bioremediation, a potential process for in-situ remediation of the subsurface contaminants, is cost effective and does not generally cause secondary contamination (Wei et al., 2017; Lacina et al., 2015). The anaerobic microorganisms prevalent in the subsurface environment could oxidize the carbon sources and co-metabolize on the contaminant metal ions during this process (Lacina et al., 2015; Němeček et al., 2015). However, low removal rate for persistent organic contaminants and inadequate energy sources often limit the large-scale application of this technology (Liu et al., 2018). The methodology of coupling anaerobic microorganism with NZVI is considered to be a promising recent technique for ground water remediation (Chen et al., 2012). This kind of adsorption and reduction based methods possess several advantages like cost effectiveness; simple design; ease of operation, and industrial scale-up capacity than the other Cr(VI) removal techniques (Kitkaew et al., 2018; Abussaud et al., 2016). There have been lately concerns about long term toxicity of the nanomaterials in environment. Also, no reports are available so far on developing an integrated remediation technique that would couple the benefits of nZVI, with environmental sustainable nature of the biogenic granules. The current technique using NZVI granules can be considered as an integrated nanobiotechnological approach in this direction. Primarily, NZVI corrosion could lower the oxidation–reduction potential in the system, providing a conducive environment for the growth of anaerobic microorganisms (Kirschling et al., 2010). Secondly, the H+ ions produced during the corrosion of NZVI can favour hydrogenotrophic microorganisms with electrons, and thus, may enhance the rate of removal of the contaminants (Xiu et al., 2010; Honetschlägerová et al., 2018). Finally, this nano bio-remediation approach, incorporating microorganisms in NZVI treatment framework could totally remove or degrade the pollutants into nontoxic materials (Xu et al., 2014). Response surface methodology (RSM), a statistical technique to develop an empirical model based on Box–Behnken design (BBD), is considered to be an effective approach to: (i) assess the composite systems performance; (ii) understand the parameters interaction; (iii) examine the relationship of an input with an output; and (iv) optimize the input parameters (Guo et al., 2011; Baş and Boyacı, 2007; Asif et al., 2017). Furthermore, BBD is also apt for its rotatable design highlights (Bezerra et al., 2008). BBD requires less number of experiments to study and analyse interaction of different independent factors and it has been effectively implemented to optimize different wastewater treatment processes (Hanrahan and Lu, 2006; Ravikumar et al., 2016). In our previous study, nZVI-laden anaerobic granular sludge (Bio-nZVI) was applied for the removal of textile dye (methyl orange) from waste water (Ravikumar et al., 2018). From a detailed literature survey on contaminant removal using NP-laden granular sludge, it was noted that there were no prior attempts on removal of Cr (VI) using zerovalent iron-incorporated anaerobic granular sludge, i.e. a nano biomaterial. Zero-valent iron and granular sludge, both being well-known reductants, may efficiently reduce Cr (VI) through redox process to a less toxic form, Cr (III). Keeping this hypothesis in mind, the current study was aimed to examine the removal process(es) of Cr (VI) by the anaerobic NZVI granules. RSM technique was employed to select the optimal experimental conditions for the removal. X-ray diffraction, SEM-EDX, and FT-IR spectroscopy were done for the characterization of anaerobic NZVI granules before and after interaction with the target contaminant. The process developed was also tested in real water systems to validate the applicability in real conditions. 2. Materials and methods The anaerobic granule preparation and NZVI synthesis using anaerobic granules in anaerobic conditions was explained in our past publication (Ravikumar et al., 2018). In brief, 0.01 M of FeSO4 was added to the glucose-fermented granules in an anaerobic condition. Anaerobic condition was maintained using an anaerobic chamber (Model: AW A-500, IMSET). The solution colour turned black within 10 min of interaction, representing the NZVI formation (Ren et al., 2019). For the as-synthesized NZVI, crystallinity was confirmed using XRD [Bruker Advanced D8, Germany; CuKα radiation (λ = 1.5418 A◦ )]; morphology and size using scanning electron microscopic images (SEM); elemental distribution by the Energydispersive X-ray spectroscopy (EDS); and surface chemical groups through Fourier-transform infrared spectroscopy (FTIR) (IR Affinity-1, Shimadzu, Japan). Iron and total chromium content in the solid samples and solutions were analysed by Flame Atomic Absorption Spectrophotometer (Analyst400/HGA 900, PerkinElmer, USA).

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2.1. Batch studies for Cr (VI) removal The design of experiments was made to optimize the useful parameters efficiently for the Cr (VI) removal process to enhance the characteristic performance and minimize experimental error, which was also beneficial to choose the essential factors with a limited number of runs. The effects of the different parameters like Cr (VI) initial concentration (10–30 mg/L), anaerobic NZVI granule weight (10–50 mg), and reaction time (30–90 min) were studied in detail on the batch removal process. In this work, the threelevel Box–Behnken Design (BBD), a typical response surface methodology (RSM) design, was employed for Cr(VI) removal. To investigate the interactional effects of the operating factors on Cr(VI) removal efficiency, three crucial variables were selected: Cr(VI) initial concentration (mg/L), anaerobic NZVI granule weight, and reaction time (min). A total of 18 runs were employed for Cr (VI) removal optimization process. Cr (VI) removal percentage was calculated using the following equation (Eq. (1)), and the removal capacity [qe (mg/g)] was calculated using Eq. (2) (Ravikumar et al., 2016) Cr(VI)removal (%) =

qe =

C0 − Ce C0

× 100

(1)

C0 − Ce

×V (2) m where, C0 : the Cr (VI) initial concentration, Ce: equilibrium Cr (VI) concentration (mg/L); V: experimental solution volume (L); and m: mass of the anaerobic NZVI granules (dry). 2.2. Cr (VI) kinetic modelling Cr (VI) kinetic analyses after interaction with anaerobic NZVI granules was further estimated by the pseudo-first and second-order models. The kinetic model equations are provided in Table S1. 2.3. Cellular viability assessment of algae, artemia, and Alium cepa The marine algae (Chlorella sp.), Artemia salina, and Alium cepa were utilized as the test systems for Cr (VI) (1 mg/L) toxicity assessment for anaerobic NZVI granule-treated Cr (VI). Algal cultures were grown in artificial seawater (ASW) enriched with Conway medium at a 16/8 h day/night rhythm at 23 ◦ C and was illuminated with white light (3000 lux intensity) using TL-D super 80 linear fluorescent tube (Philips, India). Using a centrifuge at 7000 rpm for 10 min, the exponential stage cultures were harvested. The collected pellet was washed with freshly prepared sterile ASW. Algal cells of 0.1 OD (105 cells) interacted with Cr(VI) and anaerobic NZVI granules were treated with Cr(VI) under visible light condition (72 h). After interaction, the hemocytometer was loaded with a sample suspension and undamaged cells were enumerated by an optical microscope (Make: Zeiss Axiostar Microscope, USA). The control cells without any treatment were considered to be viable (100%), and the treated cell viability (%) was measured by maintaining the control as a Ref. Thiagarajan et al. (2019). Artemia cysts were procured from Ocean Star International Inc., USA, and preserved at 4 ◦ C until further use. Before hatching, the brine shrimp cysts were hydrated in deionized water at 4 ◦ C for 12 h. Sinking cysts have been washed with distilled water. Pre-cleared cysts (approximately 1 g) were incubated in sterilized natural seawater (2 L) in a round-bottom glass tank at 30 ± 1 ◦ C . Light illumination was provided by a fluorescence lamp (10 W, 0.44 mW/cm2 ) and aeration using an aquarium air pump. Hatching of cysts of Artemia brine shrimp began within 24 h of incubation, and after hatching, they were transferred to a fresh seawater medium. Toxicity studies were carried out with the 48-h-old nauplii. The 48-h-old hatched Artemia nauplii was interacted with Cr (VI) before and after interaction with anaerobic NZVI granules (1 mg L −1 ) for 48 h. The number of live nauplii was counted using an optical microscope after the interaction period (Zeiss Axiostar Optical Microscope, USA) (Bhuvaneshwari et al., 2018). During the experiment, Artemia was not supplied any feed. Allium cepa, a common onion bulb (30 to 35 g each onion bulb), was grown on moist sand in an earthen pot at 28 ± 2 ◦ C under 12 h light/ dark cycle (De et al., 2016). When the A. cepa root attained length of 2–3 cm, these roots were treated with 1 mg/L of Cr (VI) under dark at room temperature for 4 h. The cell viability loss was estimated by the Evan’s blue staining process (Ghosh et al., 2015). The treated and controlled roots were stained for 15 min with Evan’s blue aqueous solution of 0.25 percent (w/v), and then washed for 30 min with distilled water. For a quantitative estimate, 5 root tips having the same size (1-cm length) were cut out and soaked in 4 mL of N, N – dimethylformamide at room temperature for 1 h. The Evan’s blue released was recorded at 600 nm. 2.4. Cr (VI) removal experiments in natural water samples The application of prepared anaerobic NZVI granules was tested by conducting the experiments using Cr (VI) (10 mg/L)spiked ground water (collected from Sipcot, Vellore, India) and lake water samples (from VIT lake Vellore, India). Table S2 showed the physiochemical characterization of groundwater and lake water. The Cr (VI) removal experiments were performed at optimized conditions (Initial Cr (VI) concentration: 10 mg/L; anaerobic NZVI granule weight: 50 mg; reaction time: 90 min) in distilled deionized water in anaerobic conditions.

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Fig. 1. (A) XRD graph of anaerobic NZVI granules (B) FT-IR spectra of anaerobic NZVI granules.

Fig. 2. (A) SEM images of anaerobic NZVI granules and (B) surface of anaerobic NZVI granules (C) EDX results of anaerobic NZVI granules.

2.5. Statistical analysis The complete set of Cr (VI) removal tests was done in triplicate, and the statistical significance of the results was analysed using Design expert software (version-11) and one-way ANOVA software. 3. Results and discussion 3.1. Characterization of anaerobic NZVI granules The XRD results of anaerobic NZVI granules showed an intense characteristic peak at 44.11◦ (Fig. 1A), and the JCPDS: 006–0696 data confirmed that the formation of Fe particles in zerovalent state, i.e., Fe0 .

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Table 1 Independent variables description used in BBD. Factor

Name

Units

Minimum

Maximum

Coded low

Coded high

A B C

Cr(VI) conc. Anaerobic NZVI granules wt Time

mg/L mg min

10.00 10.00 45.00

50.00 50.00 90.00

−1 ↔ 10.00 −1 ↔ 10.00 −1 ↔ 45.00

+1 ↔ 50.00 +1 ↔ 50.00 +1 ↔ 90.00

Table 2 Response surface methodology experimental design. Run

Factor 1 A: Cr(VI) conc. mg/L

Factor 2 B: Anaerobic NZVI granules wt (mg)

Factor 3 C: time min

Experimental removal (%)

Predicted removal (%)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

10 30 30 50 30 10 30 50 50 30 30 30 50 30 10 30 10

10 50 30 30 30 30 50 30 10 10 10 30 50 30 30 30 50

67.5 45 67.5 90 67.5 45 90 45 67.5 45 90 67.5 67.5 67.5 90 67.5 67.5

48.29 ± 1.21 60.00 ± 1.32 49.28 ± 1.04 39.54 ± 0.41 49.28 ± 1.04 59.01 ± 0.83 73.41 ± 1.22 26.13 ± 0.42 15.41 ± 0.11 25.15 ± 0.87 38.56 ± 0.61 49.28 ± 1.04 50.26 ± 1.11 49.28 ± 1.04 72.42 ± 1.40 49.28 ± 1.10 98.56±±0.87

45.42 62.77 50.17 38.55 50.17 61.79 76.18 25.14 16.31 24.16 37.57 50.17 47.39 50.17 75.20 50.17 91.56

The surface chemical groups of the anaerobic NZVI granules were determined from FTIR spectra (Fig. 1B). The major absorption bands in the as-synthesized NZVI-laden granules were at 3232, 2885, 1621, 1495, and 997 cm−1 . The wide and strong band from 3600 to 3200 cm−1 represents the OH and NH stretching (Sun et al., 2009; Panda et al., 2008). The region 2885 cm−1 exhibited the C–H stretching vibrations of functional groups, –CH3 and > CH2 , which attributed to the fatty acid present in membrane phospholipids (Yee et al., 2004). The peaks appear at 1621, and 1495 for amide I and II respectively (Tigini et al., 2011). The peak at 997 cm−1 corresponds to C-O stretching and this confirms the carbohydrate moieties (Tigini et al., 2011) present due to anaerobic granules. Fig. 2A shows the SEM image of anaerobic NZVI granules, wherein the size of the granule was found to be around 760 µm. The NZVI formed on the granules were spherical in shape, and the average size of the particles was determined to be 101 ± 3.22 nm Fig. 2B. The EDX results also corroborated the presence of Fe on the surface of the anaerobic NZVI granules (Fig. 2C). 3.2. Cr (VI) removal using anaerobic NZVI granules through BBD design The description of independent factor used in BBD, experimental data and ANOVA (analysis of variance) results for the removal of Cr (VI) using anaerobic NZVI granules are represented in Tables 1–3. From Table 2, the predicted Cr(VI) removal response and the experimental responses were observed to be close, the applied model is satisfactory in predicting the response variables for the removal experiments. The BBD terms, A: initial Cr(VI) concentration, B: anaerobic NZVI granules weight, C: reaction time, and AB: initial Cr(VI) concentration and anaerobic NZVI granules weight, were found to be significant (p < 0.05). The F-value and non-significant F- value for lack of fit were found to be 101.46 and 16.66, which indicate that the BBD model fitted well (Table 3). The R2 of the model was found to be 0.98, and the adjusted R2 (0.97) and predicted R2 (0.91) were in reasonable agreement, i.e., the variation is > 0.2. The adequate precision determines the signalto-noise ratio (a ratio > 4 are advantageous). The ratio for the current experiments was found to be 37.09, indicating a suitable signal. The regression analysis for Cr (VI) removal reaction followed a second-order polynomial equation (Eq. (3)), which predicts the reduction process within the present conditions. R1 = 20.11173 − 0.633871 A. + 1.24751

B + 0.298000 C − 0.009406 A∗ B − 2.96059E−18

A C − 9.86865E−18 B C. ∗

∗

(3)

where R1 denotes predicted response for Cr (VI) removal in the treatment process. 3.3. Three-dimensional (3D) surface model plots: effect of experimental factors The 3D RSM and contour plots represented the Cr (VI) removal behaviour following the experimental design (Fig. 3). The combined effect of weight of anaerobic NZVI granules and initial Cr (VI) concentration on chromium removal is

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R.K.V. Giri, L.S. Raju, Y.V. Nancharaiah et al. / Environmental Technology & Innovation 16 (2019) 100495 Table 3 ANOVA for response surface quadratic model. ANOVA for 2FI model Response 1: R1 Source

Sum of squares

df

Mean square

F-value

p-value

Model A-Cr(VI) conc. B-granules wt C-time AB AC BC Residual Lack of Fit Pure Error Cor Total Fit Statistics Std. Dev. Mean C.V. %

6083.50 2685.36 2981.86 359.66 56.63 9.095E−13 9.095E−13 99.93 99.93 0.0000 6183.43

6 1 1 1 1 1 1 10 6 4 16

1013.92 2685.36 2981.86 359.66 56.63 9.095E−13 9.095E−13 9.99 16.66 0.0000

101.46 268.72 298.39 35.99 5.67 9.101E−14 9.101E−14

< 0.0001 < 0.0001 < 0.0001

R2 Adjusted R2 Predicted R2 Adeq precision

0.9838 0.9741 0.9195 37.0989

Time 90.000

R1 98.265

Solutions Number 1

3.16 50.17 6.30

Cr(VI) conc. 10.000

Granules wt 50.000

Significant

0.0001 0.0386 1.0000 1.0000

Desirability 1.000

Selected

displayed in Fig. 3A. The removal of Cr (VI) was observed to increase as the weight of anaerobic NZVI granules increased. This may be attributed to the increased accessibility of more adsorption sites. A decline in the removal was observed as the initial Cr (VI) concentration increased. Similar results was noted in previous reports on the removal of Cr (VI) using the green-synthesized NZVI (Yirsaw et al., 2016). As the contact time increased, the percentage of Cr (VI) removal was increased, and the maximum response was achieved at 90 min (Fig. 3B). At the same time, a decrease in the removal of Cr (VI) was noted when the initial concentration of Cr (VI) in the solution exceeded 10 mg L−1 . The interactive effects of adsorbent dosage, and interaction time on chromium removal is shown in Fig. 3C. The percentage of Cr (VI) removal increased with the dosage of the adsorbent and the contact time of the adsorbent (Fig. 1C). The maximum removal was achieved in 90 min when the weight of the anaerobic NZVI granules was 50 mg. The surface plots, and p-values < 0.05 implied that the interaction between Cr (VI) concentration and anaerobic NZVI granule weight was significant. Using the desirability factor, the optimized conditions were found to be Cr (VI) initial concentration: 10 mg/L, anaerobic NZVI granules weight: 50 mg, and interaction time: 90 min. Under the optimized conditions, the predicted removal of Cr (VI) was observed to be 98.26%, and that obtained from the experiments was found to be 98.79 ± 0.86%. From these results, it can be concluded that the BBD model was valid since the predicted Cr (VI) removal and experimental Cr (VI) removal were close. 3.4. Cr (VI) removal kinetics Kinetic data was obtained for three different Cr (VI) initial concentrations of: 10, 30. 50 mg/L and anaerobic NZVI granules weight: 50 mg. The pseudo-first-order and pseudo-second-order kinetic models were fitted to analyse the kinetics of Cr (VI) sorption on the anaerobic NZVI granules. KL (1/min) and k′ (min g /mg) are the pseudo-first-order and pseudo-second-order kinetic models rate constants. Fig. 4 shows the plots of experimental data for pseudo-first order (Fig. 4A) and second-order models (Fig. 4B) at various Cr (VI) initial concentrations. The kinetic parameters calculated are represented in Table S1. The pseudo first order rate constant (KL ) was found to be decreased with increase in the initial Cr (VI) concentration. Similar trend was found in the MB adsorption using pine tree leaves (Yagub et al., 2012). Among the two models, pseudo-second-order fitted the experimental data with higher R2 than pseudo first order (did not obey the experimental data). The approximate equality of the experimentally observed qe (qe exp) values and the calculated qe values (qe cal) were indicators for the selection of the appropriate model. The adsorption capacity (qe ) estimated from pseudo-second-order equation was in concurrence with the experimental (Lv et al., 2012). Compared to other studies using PAC- Fe0 /Ag (Kakavandi et al., 2014), Fe0 decorated on graphene nanosheets (Li et al., 2016), Fe0 grown carbon nanofibers containing porous carbon microbeads (Talreja et al., 2014) and chitosan beadssupported Fe0 -nanoparticles (Liu et al., 2012) for Cr(VI) removal, the current study shows high removal percentage and removal capacities [Table S3 (supplementary information)].

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Fig. 3. The response surface plots: (A) Effect of Cr(VI) concentration and weight of anaerobic NZVI granules, (B) Effect of Interaction time and Cr(VI) concentration, (C) Effect of weight of anaerobic NZVI granules and interaction time.

3.5. Cr (VI) removal mechanism(s) The pH of the reaction solution was observed to decrease from 7.9 to 5.8. This decline in the solution pH might be due to Cr (VI) reduction to Cr (III) and consequent NZVI corrosion, which results in the OH− discharge and precipitation of Cr (III) and Fe (III) utilizing the OH− ions in the solution (Sheng et al., 2016). As the reaction progressed, NZVI surface passivation would lead to decline in the release of OH− , and the pH of the solution would become slightly acidic. The ORP was also found to be decreased from 314 to 149 mV during the interaction. The decrease in the ORP may be related to

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Fig. 4. Kinetic model for Cr (VI) removal using anaerobic NZVI granules: (A) Pseudo-first-order (B) Pseudo-second-order.

Fig. 5. (A) XRD graph of Cr(VI)- interacted anaerobic NZVI granules (B) FT-IR spectra of Cr(VI)-interacted anaerobic NZVI granules.

the redox processes happening in the system, i.e., Cr (VI) to Cr (III) reduction and Fe0 to Fe (III) oxidation (Lu et al., 2012). From the previous reports related to the Cr (VI) reduction process, it was concluded that Cr (VI) was first adsorbed by the anaerobic NZVI granules, and then Cr (VI) is reduced to Cr (III) by Fe0 oxidation (Lu et al., 2012; Chrysochoou et al., 2012). After reaction with Cr (VI), some additional peaks were noted at 32.21◦ , 37.05◦ and 58.33◦ (Fig. 5A), corresponding to iron oxide (II) and iron oxide (III). This firmly corroborates the redox interaction in the system between Fe0 and Cr (VI). This fact is supported by various previous investigations, in which NZVI particles were used to reduce the violet red acid B, Pb (II), and Cr (VI) and help in their removal from water medium (Ponder et al., 2000; Lin et al., 2014). The wide and strong band at 3232 cm−1 represents the OH stretching (Sun et al., 2009; Panda et al., 2008). The peak at 1585 cm−1 associated to N–H bending moves to 1621 cm−1 after the interaction with Cr (VI). This change may be ascribed to the interactions between the amino groups present on the anaerobic granular sludge and Cr(VI) ions (Sun et al., 2011). At 1307 cm−1 , the symmetric vibrational COO-characteristic peak may be attributed to the terminal amino acid on the biomass (Sun et al., 2009). Additionally, new peak appeared in the fingerprint region, which confirmed the Cr–O and iron oxide (Fe–O) vibration at 877 and 682 cm−1 in the Cr(VI)-reacted anaerobic NZVI granules (Fig. 5B) (Gotić and Musić, 2007; He et al., 2018; Paul et al., 2015; Ravikumar et al., 2019a). These results confirm the possibility of Fe0 surface oxidation during Cr (VI) removal process. Summarizing the surface chemical analyses, it can be suggested that the redox processes played an important part in the process. The size of the anaerobic NZVI granules after interaction with Cr (VI) was 752 µm, and the particles were completely aggregated (Fig. 6A &B). This may be due to the co-precipitation of Fe(III) and Cr(III) on the surface of the anaerobic NZVI

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Fig. 6. (A) SEM images of Cr(VI)-interacted anaerobic NZVI granules (B) surface of Cr(VI)-interacted anaerobic NZVI granules (C) EDX results of Cr(VI)-interacted anaerobic NZVI granules.

granules (Ponder et al., 2000; Shi et al., 2011). Further, EDX results also corroborated the conscious presence of Cr ions on the surface of the Cr(VI)-interacted anaerobic NZVI granules (Fig. 6C). SEM and EDX confirmed that both sorption and reduction played significant parts in the removal process. A control test was carried out to check the contribution from the anaerobic granules in the removal of Cr (VI) using bare anaerobic granules (without Fe) in anaerobic conditions, employing the optimized experimental conditions as mentioned in the previous section. The Cr (VI) removal was observed to be less (13.55 ± 0.42%) when compared to the removal using anaerobic NZVI granules, which showed that NZVI plays a pivotal role in the removal process. The contribution through the granules alone can be in the form of biosorption of Cr (VI). Taking these results into account, it can be concluded that both reduction and adsorption contributed primarily to the removal of Cr (VI). 3.6. Residual toxicity of the treated solution Fig. 7 shows the viability of Alium cepa, Artemia salina, and Chlorella sp. after interaction with the untreated Cr (VI) solution, and that after treatment with anaerobic NZVI granules. Artemia salina showed a mortality rate of 70% and 8% upon interaction with untreated Cr (VI) solution and that obtained after treatment, respectively (Fig. 7A). The cell viability (%) of Alium cepa with untreated Cr (VI) was 16%, while anaerobic NZVI granules reacted with Cr(VI) showed a steep increase in viability to 75% (Fig. 7B). Upon adding untreated Cr(VI) to Chlorella sp., the cell viability was down to 58%, while the addition of treated solution showed an increase to 75% (Fig. 7C). From the previous reports, it can be concluded that Cr (VI) is more toxic than Cr (III) (Ravikumar et al., 2016; Ma et al., 2019). In this work, Cr(VI) was adsorbed over the granules and reduced to Cr(III) thus removing it from the liquid phase. This could have helped in reducing toxicity of the effluent solutions. The tests clearly demonstrated that treatment with anaerobic NZVI granules had considerably reduced the toxicity of Cr (VI) to these well-known biomarkers of ecotoxicity evaluation of nanomaterials, Ravikumar et al. (2019b). The remediation process also can be termed as a successful detoxification exercise, generating less residual toxicity to the environment. 3.7. Cr (VI) removal from environmental water matrices by anaerobic NZVI granules In ground water, the Cr (VI) removal and removal capacity was experimentally found to be 88 ± 1.56% and 231.7 ± 1.21 mg/g, whereas in lake water, they were estimated to be 79 ± 1.94% and 217 ± 0.91 mg/g in optimized conditions. The Cr (VI) removal in samples of Cr (VI)-spiked ground water and lake water was less as compared to that obtained using distilled deionized water in the preceding sections. The decline in Cr(VI) removal capacity can be attributed to the presence of the natural colloids and co-occurring interfering solutes in the real water samples competing for the sorption sites (Ravikumar et al., 2016). These results clearly suggested that anaerobic NZVI granules can be an apt candidate for Cr (VI) removal from polluted natural water. 4. Conclusions The Cr (VI) removal by anaerobic NZVI granules in anaerobic conditions were optimized using BBD experimental design. The removal (%) of Cr(VI) were observed to be enhanced as compared with bare anaerobic granules through NZVI

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Fig. 7. Residual toxicity of Cr(VI) and by-components of Cr(VI) after interaction of anaerobic NZVI granules towards (A) Artemia, (B) Allium cepa, and (C) algae.

formation on the surface. The residual toxicity of the by-products (Cr (VI) after interacting with anaerobic NZVI granules) was examined with A. Cepa, artemia, and microalgae, which served as bioindicators of environmental toxicity. The significant increase in viability in all the cases after interacting with the treated solution, when compared to the treatments with Cr (VI) contaminated water, confirmed the detoxification through anaerobic NZVI granule-based remediation process. The NZVI granules was also successfully employed for the detoxification of natural water samples spiked with Cr (VI).

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