Microbial Adaptation to Ionic Liquids Increases the âTalentâ to Treat

Research Article pubs.acs.org/journal/ascecg

Microbial Adaptation to Ionic Liquids Increases the “Talent” to Treat Contaminants María S. Á lvarez, Francisco J. Deive,* M. Á ngeles Sanromán, and Ana Rodríguez* Department of Chemical Engineering, Campus Lagoas Marcosende, University of Vigo, 36310 Vigo, Spain ABSTRACT: Pseudomonas stutzeri strains are able to remediate different persistent contaminants, although they fail to treat efficiently industrial dyes. In this work, we have demonstrated that the acclimation of a Pseudomonas strain to the presence of the ionic liquid 1-ethyl-3-methyl imidazolium ethylsulfate can be a solution to remove two synthetic dyes widely found in wastewater effluents from textile industry: Acid Black 48 (AB48) and Reactive Black 5 (RB5), as model anthraquinone and diazo dyes, respectively. The remediation values achieved at small scale for both contaminants (individually and mixed) were higher than 75% in just 2 days. The process was scaled-up in a stirred tank bioreactor, and the levels of removal (greater than 80%) allowed confirming the suitability of the selected bioreactor configuration. All the obtained biomass and dye removal data were modeled by fitting to well-known equations in order to shed more light on the characteristics of the biotreatment process. The present work is the basis for the use of this microorganism at industrial scale, where different pollutants are found simultaneously in the same effluent. KEYWORDS: Textile dyes, Bioremediation, Pseudomonas stutzeri, Biosorption, Acclimation

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INTRODUCTION Nowadays, an increasing number of hazardous organic compounds are being discharged into the environment. More specifically, the textile industry generates polluted aqueous streams containing different contaminants, namely, surfactants, acids or bases, aromatics, heavy metals, salts, suspended solids and dyes.1 The latter usually have a synthetic origin and complex aromatic molecular structures, which make them highly stable and recalcitrant. These molecules are classified according to several features, but one typical consideration is related to chromophore group.2 The most common group of direct dyes is the azo-type, which makes up to 60−70%3 of all dye waste produced, followed by the anthraquinone type, which are extensively used for green, blue or violet hues.4,5 Reactive dyes cannot be easily removed by conventional wastewater treatment systems because they are stable to light, heat and oxidizing agents and display low biodegradability. Therefore, they have been identified as persistent compounds in textile effluents, and their impact and toxicity has been addressed in numerous research studies.6 Hence, the search of efficient alternatives allowing the bioremediation of this kind of polluted effluents is a subject in the limelight. Various physicochemical and biological processes have been employed to remove dyes from industrial wastewater, for instance, ozonation,7 adsorption on activated carbon or other adsorptive materials,8 electrochemical,9 flocculation10 and nanofiltration,11 but these are sometimes inefficient, costly and not adaptable to a wide range of dye wastewater.12 Biological processes, such as biodegradation,13 bioaccumulation and biosorption14 offer attractive options for dye remediation © 2016 American Chemical Society

due to many microorganisms such as bacteria, yeasts, algae and fungi are able to accumulate and degrade different dyes,15,16 and may represent a low-cost and environmentally friendly alternative. Among the microbial candidates, strains belonging to Pseudomonas genus have been highlighted in different research works17 as viable bioremediation agents. In this line, we have previously demonstrated the potential of Pseudomonas stutzeri for the removal of different persistent contaminants such as metal working fluids, pesticides or polycyclic aromatic hydrocarbons.18−20 However, its potential for dyes removal was extremely low, so we have bet in acclimation as a suitable strategy for improving its bioremediation ability, as demonstrated by other authors.21 To widen the applicability of this bacterium, imidazolium-based ionic liquids have been chosen since they make up a group of neoteric contaminants with recalcitrant moieties like the nitrogen heteroatom inserted in the aromatic ring and displaying high toxicity.22 Then, after a 2 month period of acclimation in a stirred tank bioreactor containing the ionic liquid 1-ethyl-3-methylimidazolium ethylsulfate (C2C1imC2SO4),23 the obtained strain was chosen for assessing its potential as dye bioremediation agent. The selection of this ionic liquid is based on the fact that it is one of the few produced at an industrial scale (more than one ton per annum) and it can be synthesized in an atom efficient and halide-free way, at a reasonable cost. Received: November 26, 2015 Revised: January 27, 2016 Published: February 15, 2016 1637

DOI: 10.1021/acssuschemeng.5b01581 ACS Sustainable Chem. Eng. 2016, 4, 1637−1642

Research Article

ACS Sustainable Chemistry & Engineering

Analytical Methods. Biomass Determination. Cells were harvested by centrifugation (10 min, 9300g and 4 °C), and the supernatant was reserved for decolorization analysis. Biomass concentration was measured by turbidimetry at 600 nm in a UV−vis spectrophotometer (UV-630 Jasco), and the obtained-values were converted to grams of cell dry weight per liter using a calibration curve. In brief, 200 mL from a submerged culture at the stationary phase was recovered, and 10 mL was reserved to prepare different dilutions. The turbidimetry of these dilutions at 600 nm was measured. On the other hand, the remaining 180 mL was vacuum filtered through a PTFE membrane (0.45 μm), washed with distilled water and dried for 24 h at 120 °C until constant weight was achieved. With this weight, the cell concentration of the culture and the dilutions is represented against the absorbance values and fitted to a linear equation. Dyes Decolorization. Dyes concentrations (both independently and mixed) in the culture media were analyzed by UV−vis spectrophotometry taking into account the maxima obtained for each dye (597 nm for RB5, 663 nm for AB48 and from 547 to 713 nm for mixture of dyes, calculated by measuring the area under the plot). Decolorization (D) was expressed in terms of percentage units by using the following expression:

In this work, we have hypothesized the suitability of an adapted P. stutzeri to enhance its bioremediation capacity when applied to aqueous effluents polluted with two model anthraquinone and azo dyes (AB48 and RB5). The dyes remediation strategy followed a bottom-up methodology, both from the contaminant and operation point of view: after demonstrating the viability of the process at small scale (shaken flasks) and with individual dyes, the operation was performed at bench scale bioreactor and with a mixture of dyes.

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EXPERIMENTAL SECTION

Chemicals. The structure and main characteristics of dyes RB5 and AB48 are shown in Table 1, purchased from Sigma-Aldrich. Glucose (>99%) was obtained from Scharlau.

Table 1. Characteristics of the Dyes and Ionic Liquid Used

D (%removal) = (Ii − If )· 100/Ii

(1)

where Ii and If are initial and final concentration of the dye solution, respectively. Each decolorization value was the mean of two parallel experiments. Abiotic controls (without microorganisms) were always included. The assays were done in duplicate, and the experimental error was less than 3%.

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RESULTS AND DISCUSSION The outstanding capacity of P. stutzeri to be used as a remediation agent for different kinds of recalcitrant contaminants, ranging from pure organic compounds like PAHs to hybrid chemicals like organophosphate pesticides, has been stressed in previous research works.18,19 Moreover, it was demonstrated that this bacterium possesses a remarkable adaptation capacity, because the presence of organic contaminants could trigger a permanent alteration at the gene level, by acquiring a nahH gene (responsible for encoding catechol 2,3-dioxygenase).24 Therefore, in a previous research work of our group23 we made use of these features to analyze the response of the bacterium when a novel class of neoteric contaminants like an imidazolium-based ionic liquid was present, and the biosynthesis of a polymer was recorded. Different research works have stressed the importance of microbial adaptation to several contaminants to increase the bioremediation efficiency,25 and the suitability of imidazoliumbased ionic liquids such as C8C1imCl to further the adaptation of microorganisms from municipal sewage sludge has already been demonstrated.26 In this sense, the ESI-MS analysis confirmed the presence of several metabolites that resulted from an initial hydroxylation of the ionic liquid followed by a degradation of the alkyl side chain via oxidation.26 Taking into account these facts, a scenario where the adapted bacterium is able to remediate another kind of pollutants such as anthraquinone and azo dyes is envisaged. Dyes Biotreatment by C2C1imC2SO4-Adapted P. stutzeri at Small Scale. The appropriateness of P. stutzeri for the biological decolorization of an aqueous stream containing two reactive dyes such as RB5 and AB 48 was first checked at small scale (shaken flasks). One of the decisive challenges to be faced when designing a point-source treatment technology is the existence of sudden changes in the dye concentration profiles released by industries.27,28 Actually, these

Microorganism. Bacterium Pseudomonas stutzeri CECT 930 was obtained from the Spanish Type Culture Collection (ATCC 17588). This bacterium was acclimatized for 2 months in a lab-scale bioreactor in the presence of 0.2 mM C2C1imC2SO4 (>99%, IoLiTec) under controlled agitation, aeration and temperature as previously reported.23 Bioremediation Medium. Minimal medium (MM) was used, composed of (g L−1 in distilled water): Na2HPO4·2H2O 8.5 (>99%), KH2PO4 3.0 (>98%), NaCl 0.5 (>99%), NH4Cl 1.0 (>99%), MgSO4· 7H2O 0.5 (>98%), CaCl2 0.0147 (>97%). MM also contained trace elements as follows (mg L−1 in distilled water): CuSO4 0.4 (>99%), KI 1.0 (>99%), MnSO4·H2O (>99%) 4.0, ZnSO4·7H2O 4.0 (>99%), H3BO3 5.0 (>99%), FeCl3·6H2O (>99%). All these salts were purchased from Sigma-Aldrich. 2.0. 10 g L−1 of glucose was also included in the culture medium as carbon source. Operation at Small Scale. The biotreatment at small scale was carried out in 250 mL Erlenmeyer flasks with 50 mL of MM. The pH was initially adjusted to 7.2 and the MM without dyes was autoclaved at 120 °C for 20 min. The dyes were sterilized by filtration through a 20 μm filter prior to the addition to the autoclaved medium in order to avoid any possible alteration of their chemical structure. The flasks were inoculated (3% v/v) with previously obtained cell pellets, which were them incubated in an orbital shaker (Thermo Fisher Scientific 496) at 37 °C and 150 rpm. Operation at Bioreactor Scale. A 2 L stirred tank bioreactor (BIOSTATB-MO) was used for the scaling up of the process. Temperature was maintained at 37 °C by circulation of thermostated water, and the agitation rate was set at 200 rpm. The initial pH was adjusted to 7.2. First, cells were grown for 12 h in flask cultures (3% v/ v) and subsequently used for bioreactor inoculation. Air was supplied continuously at 0.17 vvm. 1638


Research Article

ACS Sustainable Chemistry & Engineering variations may drastically alter the outcomes of the biological treatment, by inhibiting the microbial activity. Therefore, as dye concentrations detected in aqueous effluents from textile industry usually range from 0.01 to 0.2 g/L,29 the influence of this parameter in the biological decolorization was checked for both model dyes independently, and the results obtained are presented in Figure 1.

Figure 1. Decolorization of AB48 (○) and RB5 (□) by ionic liquidadapted P. stutzeri for different dyes concentration.

The results obtained evidence a great decolorization efficiency for both dyes (>50%) no matter the concentration used, which is very encouraging because the strain non adapted to C2C1imC2SO4 did not show any remediation capacity. In this sense, it becomes patent that the operation at concentration values between 0.03 and 0.06 g L−1 entails very high levels of dye remediation, up to 90%. Therefore, the operation at industrial scale should consider the dilution of the effluent to yield maximum values of dye biotreatment. Additionally, the monitoring of biomass production and decolorization levels (Figure 2) during bioremediation experiments at the concentration leading to maximum decolorization levels (0.04 g L−1) for AB48, RB 5 and the mixture reveals that the stationary phase of growth is reached in less than 1 day of treatment both for individual dyes and the mixture. On the other hand, it becomes patent that the C2C1imC2SO4-adapted P. stutzeri displays the highest decolorization potential within 48 h, reaching levels over 75%, which points out the interest of ionic liquid adaptation as a strategy to get more versatile microbial remediation agents. In this vein, the comparison with literature data allows concluding the suitability of this modified strain, since the remediation medium used is a synthetic one (with salts and glucose), contrarily to the fact reported by Deive et al. (2010) and Barragan et al. (2007).30,31 They established the necessity of adding complex organic sources such as peptone or yeast extract to treat a dye-polluted effluent to yield similar decolorization values, which is disadvantageous to ease process modeling and simulation or to carry out fundamental kinetic studies. Dyes Biotreatment by C 2C1imC2SO4-Adapted P. stutzeri at Bench Scale Bioreactor. Once the suitability of this adapted bacterium was demonstrated at flask scale, it is necessary to check its viability when operating at higher scale. In this sense, the feasibility of the operation at bioreactor entails many considerations like a suitable mass transfer or optimum

Figure 2. Cell growth (○) and decolorization (Δ) by ionic liquidadapted P. stutzeri in aqueous effluents polluted with (A) AB48, (B) RB5 and (C) mixture of dyes, at flask scale. Experimental data are represented by symbols and solid lines are used for the proposed theoretical models.

operating conditions allowing an efficient removal of the dye mixture. The viability of this scale-up was assessed by monitoring the biomass and decolorization capacity of the dye mixture (initial concentration of 0.04 g L−1 of each dye) in a stirred tank bioreactor, and the results obtained are shown in Figure 3. A visual inspection of the experimental data allows detecting an improvement both in the remediation values and in the times required to reach the maximum, which is an important advantage when implementing this biotreatment at industrial scale. In this sense, it is outstanding that about 80% of decolorization is recorded after less than 1 day. Although this kind of bioreactor configuration entails advantages like an efficient control of aeration and agitation, separately, sometimes some degree of mechanic stress could be inflicted by the impeller. However, it seems evident that no important cell damage is recorded, since a very slight decrease in the biomass concentration values is observed. 1639


Research Article


Figure 3. Cell growth (○) and decolorization (Δ) by ionic liquidadapted P. stutzeri in aqueous effluents polluted with a mixture of dyes RB5 and AB48 at bench scale bioreactor (37 °C, 200 rpm, 0.17 vvm). Experimental data are represented by symbols and solid lines are used for the proposed theoretical models.

Figure 4. UV visible spectra of untreated (solid line) and biotreated (dashed line) effluents polluted with a mixture of AB.

D=

Dmax [ln((Dmax / D0) − 1) − μDt ]

(3)

1+e

−1

where X and D are the biomass (g L ) and dye decolorization (%), X0 and D0 are the initial biomass and decolorization, Xmax (g L−1) and Dmax are the maximum biomass and decolorization, μm and μD are the maximum specific growth rate and maximum specific remediation rate (h−1) and t is the time where each sample was taken out. The fitting of experimental data to the proposed model was carried out by using the SOLVER function in Microsoft EXCEL, by minimizing the standard deviation, calculated as follows:

After the suitability of the operation at bioreactor scale was demonstrated, the elucidation of the characteristics of the remediation process was approached. The reason for the elevated percentages of decolorization can be linked with the nature of the remediation process. In this sense, the production of a biopolymer by this strain once adapted to the presence of C2C1imC2SO4, as reported recently,23 promoted dye biosorption on the biomass. Additionally, a drastic decrease in pH values was recorded (from 7.2 to 4.5), which can also help to increase the dye removal. Thus, the improvement in dyes biosorption may be explained in terms of the electrostatic interactions between the biomass and the dye structure.32 More specifically, the nitrogen-containing functional groups in proteins and biomass will be easily protonated under acidic conditions, thus leading to a net positive charge and consequently furthering an electrostatic attraction with the negatively charged dye anions. This electrostatic behavior has been considered to be the primary mechanism concluded for the biosorption of different dyes.33,34 Additionally, given the biosorptive nature of dye decolorization, the monitoring of the UV−visible spectra must be tackled in order to demonstrate the absence of dye in the biotreated effluent. The results shown in Figure 4 indicate the suitability of the proposed adapted P. stutzeri, because the absence of the characteristic band for the dye mixture is detected once the stationary phase of the decolorization process is reached. The technical implementation of the proposed process at industrial scale requires a deeper knowledge of the biotreatment kinetics. One of the useful means to get a better insight into the biological process is the description of the quantitative relationship between the biomass and the dye decolorization at a specific moment of the culture time t (h). A logistic model has been proposed for the bioremediation of different contaminants.19,20,30 In this way, the biomass and the decolorization percentage can be defined on the basis of the initial and maximum biomass and decolorization rate as follows: X=

⎛ n DAT ⎞1/2 2 ⎜ Σ (zexp − z theor) ⎟ ⎟ σ=⎜ i nDAT ⎜⎜ ⎟⎟ ⎝ ⎠

being zexp and ztheor the experimental and theoretical data, respectively and nDAT is the number of experimental data. The model suitably fitted to the experimental data, as can be concluded from the regression coefficients listed in Table 2, because all of them are higher than 0.98. This suitability can also be visually inspected in Figures 2 and 3, where the theoretical data are presented as solid lines. The analysis of the parameters confirms previous conclusions, because slightly lower maximum biomass levels are obtained at bioreactor scale, and the maximum decolorization percentages are 10% higher at greater scale for the dyes mixture. Additionally, it can be remarked that the maximum specific growth rate obtained at bioreactor scale is 25% higher than that existing in shaken flasks, probably due the increased mass transfer provided by the mechanic agitation. The same trend is concluded when comparing the maximum specific decolorization rate, as it increases by 11% when operating in stirred tank bioreactor. It is outstanding that the values obtained are in the same order of magnitude than those reported for other microbial agents.30

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CONCLUSION This study allowed checking the viability of ionic liquid acclimation as a strategy for improving microbial versatility to

X max 1 + e[ln((X max / X 0) − 1) − μm t ]

(4)

(2) 1640


Research Article


(6) Puvaneswari, N.; Muthukrishnan, J.; Gunasekaran, P. Toxicity assessment and microbial degradation of azo dyes. Indian J. Exp. Biol. 2006, 44, 618−626. (7) Sancar, B.; Balci, O. Decolorization of different reactive dye wastewaters by O3 and O3/ultrasound alternatives depending on different working parameters. Text. Res. J. 2013, 83, 574−590. (8) Vecino, X.; Devesa-Rey, R.; Cruz, J. M.; Moldes, A. B. Entrapped Peat in Alginate Beads as Green Adsorbent for the Elimination of Dye Compounds from Vinasses. Water, Air, Soil Pollut. 2013, 224, 1448− 1458. (9) Iglesias, O.; de Dios, M. A.; Rosales, E.; Pazos, M.; Sanromán, M. A. Optimisation of decolourisation and degradation of reactive black 5 dye under electro-Fenton process using Fe alginate gel beads. Environ. Sci. Pollut. Res. 2013, 20, 2172−2183. (10) Kang, Q. Residual color profiles of simulated reactive dyes wastewater in flocculation processes by polydiallyldimethylammoniumchloride. Sep. Purif. Technol. 2007, 57, 356−365. (11) Zarei, M.; Niaei, A.; Salari, D.; Khataee, A. R. Removal of four dyes from aqueous medium by the peroxi-coagulation method using carbon nanotube-PTFE cathode and neural network modeling. J. Electroanal. Chem. 2010, 639, 167−174. (12) Banat, I. M.; Nigam, P.; Singh, D.; Marchant, R. Microbial decolorization of textile-dye containing effluents: A review. Bioresour. Technol. 1996, 58, 217−227. (13) Liu, G.; Zhou, J.; Meng, X.; Fu, S. Q.; Wang, J.; Jin, R.; Lv, H. Decolorization of azo dyes by marine Shewanella strains under saline conditions. Appl. Microbiol. Biotechnol. 2013, 97, 4187−4197. (14) Chojnacka, K. Biosorption and bioaccumulation - the prospects for practical applications. Environ. Int. 2010, 36, 299−307. (15) Aksu, Z. Reactive dye bioaccumulation by Saccharomyces cerevisiae. Process Biochem. 2003, 38, 1437−1444. (16) El-Sheekh, M. M.; Gharieb, M. M.; Abou-El-Souod, G. W. Biodegradation of dyes by some green algae and cyanobacteria. Int. Biodeterior. Biodegrad. 2009, 63, 699−704. (17) Wasi, S.; Tabrez, S.; Ahmad, M. Use of Pseudomonas spp. for the bioremediation of environmental pollutants: a review. Environ. Monit. Assess. 2013, 185, 8147−8155. (18) Moscoso, F.; Deive, F. J.; Longo, M. A.; Sanromán, M. A. Technoeconomic assessment of phenanthrene degradation by Pseudomonas stutzeri CECT 930 in a batch bioreactor. Bioresour. Technol. 2012, 104, 81−89. (19) Moscoso, F.; Teijiz, I.; Deive, F. J.; Sanromán, M. A. Approaching chlorpyrifos bioelimination at bench scale bioreactor. Bioprocess Biosyst. Eng. 2013, 36, 1303−1309. (20) Moscoso, F.; Deive, F. J.; Villar, P.; Pena, R.; Herrero, L.; Longo, M. A.; Sanromán, M. A. Assessment of a process to degrade metal working fluids using Pseudomonas stutzeri CECT 930 and indigenous microbial consortia. Chemosphere 2012, 86, 420−426. (21) Herzog, B.; Yuan, H. Y.; Lemmer, H.; Horn, H.; Muller, E. Effect of acclimation and nutrient supply on 5-tolyltriazole biodegradation with activated sludge communities. Bioresour. Technol. 2014, 163, 381−385. (22) Romero, A.; Santos, A.; Tojo, J.; Rodriguez, A. Toxicity and biodegradability of imidazolium ionic liquids. J. Hazard. Mater. 2008, 151, 268−273. (23) Á lvarez, M. S.; Rodríguez, A.; Sanromán, M. A.; Deive, F. J. Microbial adaptation to ionic liquids. RSC Adv. 2015, 5, 17379−17382. (24) Lalucat, J.; Bennasar, A.; Bosch, R.; García-Valdés, E.; Palleroni, N. J. Biology of Pseudomonas stutzeri. Microbiol. Mol. Biol. Rev. 2006, 70, 510−547. (25) Puglisi, E.; Hamon, R.; Vasileiadis, S.; Coppolecchia, D.; Trevisan, M. Adaptation of soil microorganisms to trace element contamination: A review of mechanisms, methodologies, and consequences for risk assessment and remediation. Crit. Rev. Environ. Sci. Technol. 2012, 42, 2435−2470. (26) Markiewicz, M.; Stolte, S.; Lustig, Z.; Łuczak, J.; Skup, M.; Hupka, J.; Jungnickel, C. Influence of microbial adaption and supplementation of nutrients on the biodegradation of ionic liquids

Table 2. Parameters of the Logistic Model To Characterize the Kinetic Growth and Dye Decolorization of Ionic Liquids-Adapted P. stutzeri at Flask and Bioreactor Scale dye

X0

RB5 AB48 RB5+AB48

0.09 0.14 0.06

RB5+AB48

0.31 D0(%)

RB5 AB48 RB5+AB48

0.11 0.17 0.06

RB5+AB48

0.78

Xmax flask scale 6.40 6.29 6.76 bioreactor scale 5.48 Dmax(%) flask scale 72.43 92.71 77.05 bioreactor scale 86.62

μmax

R2

σ

0.39 0.41 0.44

0.98 0.99 0.98

0.35 0.23 0.40

0.55 μD

0.99 R2

0.26 σ

0.31 0.29 0.28

0.98 0.99 0.99

5.05 2.82 2.67

0.31

0.99

2.43

treat azo and anthraquinone dyes. An adapted potential of the P. stutzeri was confirmed for the typical dye concentration range detected in waste waters released from textile factories. Additionally, biopolymer synthesis observed in the adapted bacterial strain, together with the low pH values furthered dye biosorption on the biomass. The biological process was carried out at small and bioreactor scale, obtaining promising decolorization levels both for each dye individually and mixed. All the experimental data were suitably modeled with logistic equations, allowing characterizing the kinetics of the biological reaction in order to ease process implementation at higher scale.

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AUTHOR INFORMATION

Corresponding Authors

*F. J. Deive. E-mail: [email protected]. Tel.: +34986818723. ́ *A. Rodriguez. E-mail: [email protected]. Tel.: +34986812312. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research has been financially supported by the Spanish Ministry of Economy and Competitiveness, Xunta de Galicia and ERDF Funds (Projects CTM2014-52471-R and GRC 2013/003). The authors are grateful to the Spanish Ministry of Economy and Competitiveness for the financial support of F. J. Deive under the Ramón y Cajal program (RyC-2013-14225).

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REFERENCES

(1) Zaharia, C.; Suteu, D. Coal fly ash as adsorptive material for treatment of a real textile effluent: operating parameters and treatment efficiency. Environ. Sci. Pollut. Res. 2013, 20, 2226−2235. (2) Robinson, T.; McMullan, G.; Marchant, R.; Nigam, P. Remediation of dyes in textile effluent: a critical review on current treatment technologies with a proposed alternative. Bioresour. Technol. 2001, 77, 247−255. (3) Bae, J. S.; Freeman, H. S. Aquatic toxicity evaluation of new direct dyes to the Daphnia magna. Dyes Pigm. 2007, 73, 81−85. (4) Vandevivere, P. C.; Bianchi, R.; Verstraete, W. Treatment and reuse of wastewater from the textile wet-processing industry: Review of emerging technologies. J. Chem. Technol. Biotechnol. 1998, 72, 289− 302. (5) Zollinger, H. Color chemistry-Synthesis, properties and applications of organic dyes and pigments; VCH Publishers: New York, 1987. 1641


Research Article

ACS Sustainable Chemistry & Engineering in sewage sludge treatment processes. J. Hazard. Mater. 2011, 195, 378−382. (27) Koutinas, M.; Martin, J.; Peeva, L. G.; Mantalaris, A.; Livingston, A. G. An Oil-Absorber-Bioscrubber System To Stabilize Biotreatment of Pollutants Present in Waste Gas. Fluctuating Loads of 1,2Dichloroethane. Environ. Sci. Technol. 2006, 40, 595−602. (28) Koutinas, M.; Baptista, I. I. R.; Peeva, L. G.; Ferreira Jorge, R. M.; Livingston, A. G. The use of an oil absorber as a strategy to overcome starvation periods in degrading 1,2-dichloroethane in waste gas. Biotechnol. Bioeng. 2007, 96, 673−686. (29) Pandey, A.; Singh, P.; Iyengar, L. Bacterial decolorization and degradation of azo dyes. Int. Biodeterior. Biodegrad. 2007, 59, 73−84. (30) Deive, F. J.; Domínguez, A.; Barrio, T.; Moscoso, F.; Morán, P.; Longo, M. A.; Sanromán, M. A. Decolorization of dye Reactive Black 5 by newly isolated thermophilic microorganisms from geothermal sites in Galicia (Spain). J. Hazard. Mater. 2010, 182, 735−742. (31) Barragán, B. E.; Costa, C.; Márquez, M. C. Biodegradation of azo dyes by bacteria inoculated on solid media. Dyes Pigm. 2007, 75, 73−81. (32) Savin, I. I.; Butnaru, R. Wastewater characteristics in textile finishing mills. Environ. Eng. Manage. J. 2008, 7, 859−864. (33) O'Mahony, T.; Guibal, E.; Tobin, J. M. Reactive dye biosorption by Rhizopus arrhizus biomass. Enzyme Microb. Technol. 2002, 31, 456− 463. (34) Bidisha, C.; Sreeranjani, R.; Shaik, A.; Chaudhari, S.; Sumathi, S. Bioaccumulation and biosorption of drimarene red dye by Aspergillus foetidus. Int. J. Environ. Pollut. 2006, 28, 517−533.

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Microbial Adaptation to Ionic Liquids Increases the âTalentâ to Treat

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Microbial Adaptation to Ionic Liquids Increases the âTalentâ to Treat