Elsevier

Water Research

Volume 90, 1 March 2016, Pages 294-300
Water Research

Three degradation pathways of 1-octyl-3-methylimidazolium cation by activated sludge from wastewater treatment process

https://doi.org/10.1016/j.watres.2015.11.065Get rights and content

Highlights

  • Ionic liquid (IL) degradation was achieved by using activated sludge.

  • Three major metabolic pathways responsible for IL degradation were identified.

  • Initial oxidation occurred at different positions of alkyl chains.

  • Biodegradation products were identified by using MS/MS fragmentation patterns.

Abstract

The biodegradability and degradation pathways of 1-octyl-3-methylimidazolium cation [OMIM]+ by microbial community of wastewater treatment plant in Jeonju city, Korea were investigated. It was found that [OMIM]+ could be easily degraded by the microbial community. New degradation products and pathways of [OMIM]+ were identified, which are partially different from previous results (Green Chem. 2008, 10, 214–224). For the analysis of the degradation pathways and intermediates, the mass peaks observed in the range m/z of 50–300 were screened by using a tandem mass spectrometer (MS), and their fragmentation patterns were investigated by MS/MS. Surprisingly, we found three different degradation pathways of [OMIM]+, which were separated according to the initially oxidized position i.e. middle of the long alkyl chain, end of the long alkyl chain, and end of the short alkyl chain. The degradation pathways showed that the long and short alkyl chains of [OMIM]+ gradually degraded by repeating oxidation and carbon release. The results presented here shows that [OMIM]+ can be easily biodegraded through three different degradation pathways in wastewater treatment plants.

Introduction

Ionic liquids (ILs) known as green solvent received a great deal of attention in the last two decades (Earle and Seddon, 2000, Plechkova and Seddon, 2008). Actually ILs have industrially applicable properties i.e. material dissolution, thermal stability, catalytic and electrolytic actions, and remarkably safe properties i.e. non-flammability and low volatility. These remarkable features offer a potential possibility for replacement of environmentally unfriendly organic solvents. In addition to these advantageous properties, ILs can be recycled, which is a preferable property for sustainable development (Welton, 1999, Abu-Eishah, 2011). By considering only advantages of ILs, numerous researchers have employed ILs for many applications in various fields, and this leads a dramatic raise in published papers. However the disadvantages of ILs were not completely studied or evaluated. For instance, even though ILs released into environment may not directly affect human beings and animals by inhalation, they may affect persistently the diverse organisms in aqueous environment due to their thermal and chemical stability. In this perspective many researchers have focused to evaluate environmental aspects of ILs in aqueous and soil systems.

During last two decades, several studies were carried to evaluate ILs' environmental aspects such as toxicity and biodegradability. The toxicological effects of ILs in groundwater were studied by using various organisms such as bacteria (Ranke et al., 2004), human cells (Stepnowski et al., 2004), rat cells (Ranke et al., 2007a, Stolte et al., 2007, Torrecilla et al., 2009), and various aquatic organisms including Lemna minor (Larson et al., 2008), algae (Cho et al., 2007, Cho et al., 2008a, Cho et al., 2008b, Latała et al., 2005, Latała et al., 2009a, Latała et al., 2009b, Latała et al., 2010, Matzke et al., 2007, Pham et al., 2008a, Pham et al., 2008b, Wells and Coombe, 2006) the fresh water crustacean Daphnia magna (Bernot et al., 2005a, Bernot et al., 2005b), fresh water snail Physa acuta (Bernot et al., 2005a, Bernot et al., 2005b) and zebra fish Danio rerio (Pretti et al., 2006). In addition to these studies, for more convenient ways, some researchers were also focused to predict the toxicological effects of ILs and reported various methods for this purpose (Torrecilla et al., 2009, Alvarez-Guerra and Irabien, 2011, Cho et al., 2013, Fatemi and Izadiyan, 2011, Luis et al., 2007, Luis et al., 2010, Torrecilla et al., 2010).

Along with the studies related to toxicity of ILs, biodegradation property of ILs is also a crucial issue to understand their whole environmental fate. _ENREF_22The biodegradability of ILs with different head groups, anions, alkyl chains, and functional groups was studied by Gathergood et al., 2004, Gathergood et al., 2006 and Garcia et al. (2005) by using CO2 headspace test. Harjani et al. (2008) also studied on biodegradable pyridinium based ILs using the same closed bottle method and reported that pyridinium bearing an ester positioned at 1 or 3 of alkyl chain has excellent biodegradability. And Wells and Coombe (2006) reported the biodegradability of imidazolium, ammonium, phosphonium, and pyridinium salts with different alkyl chain lengths by measuring the biochemical oxygen demand (BOD) for 28 days. Using the same method, Romero et al. (2008) also performed biodegradation tests of imidazolium-based ILs with the alkyl chain length (C1–C8) with different anions i.e. Cl, [PF6], [CH3SO4] and [C2H5SO4] in the presence or absence of glucose. And they showed that the tested ILs were poorly degradable in presence and absence of other carbon source. Docherty et al., 2007, Docherty et al., 2010 investigated the biodegradation of imidazolium and pyridinium with different alkyl chain lengths and suggested that imidazolium and pyridinium-based ILs with six or more alkyl chains are biodegradable. They also reported that the pyridinium ring was opened by bacterial metabolism, whereas the imidazolium ring was not open (Docherty et al., 2007). Unlike these studies performed in aqueous phase, Modelli et al. (2008) monitored the environmental fate of ILs in soil. Similarly, Markiewicz et al. (2015) examined biodegradability of an imidazolium based IL in soil and soil amended with activated sludge. Moreover, for the rapid degradation of ILs, Siedlecka et al. (2008) used a Fenton-like system that induces the catalytic decomposition of dilute hydrogen peroxide by iron (II), generating hydroxyl radicals. Furthermore, for the same purpose, Zhou et al., 2013a, Zhou et al., 2013b, treated some ILs in an ultrasound assisted zero-valent iron activated carbon microelectrolysis. For the treatment of non-biodegradable IL such as 1-butyl-3-methylimidazolium chloride, Stolte et al. (2008) performed an electrochemical degradation experiment in an electrolysis cell equipped with two electrodes made of iridium oxide (anode) and stainless steel (cathode). For further information about the environmental risk assessments of ILs e.g. toxicity and/or biodegradation, authors suggest review papers by Ranke et al., 2007b, Pham et al., 2010, Coleman and Gathergood, 2010, Stolte et al., 2011, Petkovic et al., 2011, and Cvjetko Bubalo et al. (2014).

During biodegradation of ILs, identification of the degradation products is an important step because the original compound could be transformed into more toxic chemical structures by microbial activities as Deng et al. (2015) mentioned. And from that kind of study, we can have better understanding on the whole environmental aspects by providing chemical structures of intermediates which are required for detailed studies – e.g. toxicity, adsorption, and mobility etc. – of the intermediates. For the purpose, over the last decade, the studies on the degradation pathway of ILs have been investigated. Preliminary study on degradation pathway of IL was reported by Jastorff et al. (2003). They considered the degradation pathways of 1-butyl-3-methylimidazolium cation within their systematic algorithm. In a practical test, the degradation products of the same target compound were identified by Kumar et al. (2006) by gas chromatography mass spectrometry (GC–MS). Moreover, our research group (Pham et al., 2008) reported the degradation pathways of 1-butyl-3-methylpyridinium cation [BMPy]+ by the oxidation on the butyl chain. In contrast, Docherty et al. (2010) indicated that the degradation pathways of pyridinium-based cations depend on the alkyl chain length, i.e., the biodegradation of [BMPy]+ involved the unsaturation of butyl side chain and hydroxylation of aromatic ring, whereas the biodegradation of 1-octyl- and 1-hexyl-3-butylpyridinium cations involved the unsaturation and hydroxylation of the long side chain. Zhang et al., 2010, Zhang et al., 2011 reported that 2-ethylpyridinium cation [Py2]+ has different degradation pathways according to types of bacteria such as Corynebacterium sp(Zhang et al., 2010) and Pseudomonas fluorescens (Zhang et al., 2011), which are ubiquitous in soil. Stolte et al. (2008) identified the biodegradation pathway of 1-octyl-3-methylimidazolium cation [OMIM]+ by LC-MS. The degradation pathway shows that the oxidation for the carbon fragment started from the end of long alkyl chain until forming 3-carboxymethyl-1-methylimidazolium cation. Very recently, Deng et al. (2015) reported biodegradability and the metabolites of pyridinium, pyrrolidinium, and ammonium based ILs with an isolated strain of Rhodococcus rhodochrous ATCC 29672 or activated sludge. Nevertheless the biodegradability and degradation pathways should be further studied especially with microbial communities from real activated sludge processes because they are dependent on spatial and temporal constraints. In the present study we therefore investigated if [OMIM]+ is degradable and how [OMIM]+ is degraded by microbial community taken from wastewater treatment factory located in Jeonju, South Korea. [OMIM]+ was chosen because in general [OMIM]+ based ILs have many possibilities to be used as catalysis (Maruyama et al., 2002, Maleki et al., 2007), metal extracting system (Chun et al., 2001) and lubricant additives (Yang et al. 2014) in industrial areas.

Section snippets

Chemicals

[OMIM]+ bromide was purchased from C-tri co. (99% purity, Su-Won, Korea). [OMIM]+ bromide was used as received without any pretreatment. Acetonitrile and formic acid used as mobile phase in high-performance liquid chromatography system (HPLC) were purchased from J. T. Baker and Acros (USA), respectively.

Preparation of activated sludge

The activated sludge used to [OMIM]+ biodegradation was obtained from aeration tank of a municipal wastewater treatment plant (WWTP) in Jeonju, Korea. According to the modified OECD screening

Identification of biodegradation pathways

At first, to obtain the information about [OMIM]+ biodegradation by the activated sludge, the reduction of [OMIM]+ concentration with time period (days) was studied and the results are depicted in Fig. 1. The [OMIM]+ in an aerobic condition was completely degraded within 24 days, these results are similar with the previous results reported by Stolte et al. (2008). In contrast, Neumann et al. (2010) estimated that [OMIM]+ was not degradable in an anaerobic condition for 318 days, because of

Discussion

The proposed degradation pathways of [OMIM]+ in present study shows more complex degradation pathways compared to previously reported results (Stolte et al., 2008). However the degradation pathway 2 of Fig. 4 seems a similar pattern with previous results, which shows a regular breakdown of carbon source of the long alkyl chain from its end near to the core. However the remarkable differences of the present work from the past work (Stolte et al., 2008) are to show oxidation-starting positions,

Conclusion

We showed degradation intermediates and three pathways from the biodegradation of [OMIM]+ by microbial community of sewage treatment plant of Jeonju (Korea). The initial biodegradation products can be generated by single oxidation at three points of alkyl chains i.e. end of short alkyl chain, end and middle of long alkyl chains. Accordingly, the oxidized structures became starting points of three degradation pathways, and they were degraded continuously to the small molecule with m/z 99.

Since

Acknowledgment

This research was supported by the Korean Government through NRF (2014R1A2A1A09007378, 2014R1A1A2008337) grant.

References (62)

  • J. Ranke et al.

    Lipophilicity parameters for ionic liquid cations and their correlation to in vitro cytotoxicity

    Ecotoxicol. Environ. Saf.

    (2007)
  • A. Romero et al.

    Toxicity and biodegradability of imidazolium ionic liquids

    J. Hazard. Mat.

    (2008)
  • E. Siedlecka et al.

    Degradation of 1-butyl-3-methylimidazolium chloride ionic liquid in a fenton-like system

    J. Hazard. Mat.

    (2008)
  • J.S. Torrecilla et al.

    Estimation of toxicity of ionic liquids in leukemia rat cell line and Acetylcholinesterase enzyme by principal component analysis, neural networks and multiple lineal regressions

    J. Hazard. Mat.

    (2009)
  • C. Zhang et al.

    Toxicity of imidazolium-and pyridinium-based ionic liquids and the co-metabolic degradation of N-ethylpyridinium tetrafluoroborate

    Chemosphere

    (2011)
  • H. Zhou et al.

    Identification of degradation products of ionic liquids in an ultrasound assisted zero-valent iron activated carbon micro-electrolysis system and their degradation mechanism

    Water Res.

    (2013)
  • H. Zhou et al.

    Degradation of 1-butyl-3-methylimidazolium chloride ionic liquid by ultrasound and zero-valent iron/activated carbon

    Sep. Purif. Technol.

    (2013)
  • S.I. Abu-Eishah

    Ionic liquids recycling for reuse, ionic liquids – classes and properties

  • M. Alvarez-Guerra et al.

    Design of ionic liquids: an ecotoxicity (Vibrio fischeri) discrimination approach

    Green Chem.

    (2011)
  • R.J. Bernot et al.

    Acute and chronic toxicity of imidazolium-based ionic liquids on Daphnia magna

    Environ. Toxicol. Chem.

    (2005)
  • R.J. Bernot et al.

    Effects of ionic liquids on the survival, movement, and feeding behavior of the freshwater snail, Physa acuta

    Environ. Toxicol. Chem.

    (2005)
  • C.-W. Cho et al.

    Influence of anions on the toxic effects of ionic liquids to a phytoplankton Selenastrum capricornutum

    Green Chem.

    (2008)
  • C.-W. Cho et al.

    In silico modelling for predicting the cationic hydrophobicity and cytotoxicity of ionic liquids towards the leukemia rat cell line, Vibrio fischeri and Scenedesmus vacuolatus based on molecular interaction potentials of ions

    SAR QSAR Environ. Res.

    (2013)
  • S. Chun et al.

    Influence of structural variation in room-temperature ionic liquids on the selectivity and efficiency of competitive alkali metal salt extraction by a crown ether

    Anal. Chem.

    (2001)
  • D. Coleman et al.

    Biodegradation studies of ionic liquids

    Chem. Soc. Rev.

    (2010)
  • Y. Deng et al.

    When can ionic liquids be considered readily biodegradable? Biodegradation pathways of pyridinium, pyrrolidinium and ammonium-based ionic liquids

    Green Chem.

    (2015)
  • K.M. Docherty et al.

    Biodegradability of imidazolium and pyridinium ionic liquids by an activated sludge microbial community

    Biodegradation

    (2007)
  • K.M. Docherty et al.

    Microbial biodegradation and metabolite toxicity of three pyridinium-based cation ionic liquids

    Green Chem.

    (2010)
  • M.J. Earle et al.

    Ionic liquids. Green solvents for the future

    Pure Appl. Chem.

    (2000)
  • W.R. Finnerty et al.

    Origin of palmitic acid carbon in palmitates formed from hexadecane-1-C14 and tetradecane-1-C14 by Micrococcus cerificans

    J. Bacteriol.

    (1964)
  • M.T. Garcia et al.

    Biodegradable ionic liquids Part II. Effect of the anion and toxicology

    Green Chem.

    (2005)
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