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Degradation of 1,2-Dichloroethane by Microbial Communities from River Sediment at Various Redox Conditions

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Degradation of 1,2-Dichloroethane by Microbial Communities from River Sediment at Various Redox Conditions water research 43 (2009) 3207–3216 Available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/watres Degradation of 1,2-dichloroethane by microbial communities from river sediment at various redox conditions Bas van der Zaana,b,*, Jasperien de Weertc,d, Huub Rijnaartsc,d, Willem M. de Vosb, Hauke Smidtb, Jan Gerritsec aSoil and Ground Water Systems, TNO Built Environment and Geosciences, Princetonlaan 6, 3584 CB Utrecht, the Netherlands bLaboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, the Netherlands cDeltares, Princetonlaan 6, 3584 CB Utrecht, the Netherlands dSection of Environmental Technology, Wageningen University, Bomenweg 2, 6703 HD Wageningen, the Netherlands article info abstract Article history: Insight into the pathways of biodegradation and external factors controlling their activity is Received 10 March 2009 essential in adequate environmental risk assessment of chlorinated aliphatic hydrocarbon Received in revised form pollution. This study focuses on biodegradation of 1,2-dichloroethane (1,2-DCA) in micro- 20 April 2009 cosms containing sediment sourced from the European rivers Ebro, Elbe and Danube. Accepted 22 April 2009 Biodegradation was studied under different redox conditions. Reductive dechlorination of Published online 5 May 2009 1,2-DCA was observed with Ebro and Danube sediment with chloroethane, or ethene, respectively, as the major dechlorination products. Different reductively dehalogenating Keywords: micro-organisms (Dehalococcoides spp., Dehalobacter spp., Desulfitobacterium spp. and 1,2-Dichloroethane (1,2-DCA) Sulfurospirillum spp.) were detected by 16S ribosomal RNA gene-targeted PCR and sequence Reductive dechlorination analyses of 16S rRNA gene clone libraries showed that only 2–5 bacterial orders were Anaerobic oxidation represented in the microcosms. With Ebro and Danube sediment, indications for anaerobic River sediment oxidation of 1,2-DCA were obtained under denitrifying or iron-reducing conditions. No biodegradation of 1,2-DCA was observed in microcosms with Ebro sediment under the different tested redox conditions. This research shows that 1,2-DCA biodegradation capacity was present in different river sediments, but not in the water phase of the river systems and that biodegradation potential with associated microbial communities in river sediments varies with the geochemical properties of the sediments. ª 2009 Elsevier Ltd. All rights reserved. 1. Introduction lasting danger to humans and the environment because of high water solubility, a long environmental half-life and Chlorinated aliphatic hydrocarbons (CAHs) like tetra- carcinogenic effects (Vogel et al., 1987). chloroethene (PCE), 1,2-dichloroethane (1,2-DCA) and Transformation of CAHs has been studied extensively, vinyl chloride (VC), are widely used in industries as solvents or with specific attention for the microbiology (Mohn and Tiedje, as intermediates in chemical processes. Due to leakage and 1992; Smidt and de Vos, 2004), in situ biodegradation in soil improper disposal, CAHs have often been detected in the systems (Maes et al., 2006; Suchomel et al., 2007; Takeuchi environment (Westrick et al., 1984). Here, they form a long- et al., 2005) and enzymology (Bunge et al., 2007). However, * Corresponding author. Soil and Ground Water Systems, TNO Built Environment and Geosciences, Princetonlaan 6, 3584 CB Utrecht, the Netherlands. Tel.: þ31 6 2349 9738; fax: þ31 8 8866 2042. E-mail address: [email protected] (B. van der Zaan). 0043-1354/$ – see front matter ª 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2009.04.042 3208 water research 43 (2009) 3207–3216 little information is available with respect to the variation of that fermentative as well as anaerobic oxidative pathways can the microbial degradation potential and activity in river sedi- be involved in natural attenuation of 1,2-DCA (Gerritse et al., ment systems (Bradley and Chapelle, 1998). This is in sharp 1999). However, an investigation of the local biogeochemical contrast to the demands of regulatory bodies that require conditions is required before it can be assessed to what extent specific guidelines based on fundamental knowledge of the and via which pathways 1,2-DCA is likely to be degraded in biodegradation of pollutants in river systems for adequate a specific sediment or groundwater system. river management (Barth et al., 2007; Gerzabek et al., 2007). The aim of the present study was to asses the potential for Much attention has been given to 1,2-DCA as a model biodegradation of 1,2-DCA by microbial communities of compound (de Wildeman et al., 2003b; Falta et al., 2005; sediments originating from the rivers Ebro, Danube and Elbe Fishbein, 1979; Janssen et al., 1994), since it can biologically be at different redox conditions, and to identify biodegradation degraded under different geochemical conditions. Moreover, mechanisms and micro-organisms involved. To this end, it has been produced in larger quantities than any other CAH microcosm and cultivation-independent approaches were (Pankow and Cherry, 1996). Currently, more than 17.5 million combined to obtain insight to what extent the mechanisms tons are produced annually in the United States, Western and micro-organisms can be related to prevailing redox Europe and Japan (Field and Sierra-Alvarez, 2004). 1,2-DCA is conditions and characteristics of the tested river inoculum frequently detected in river systems at several tens of micro- material. molars (ATSDR, 1999; Gotz et al., 1998; ICPS, 1995; Yamamoto et al., 1997), which is above the natural background level of 5 mmol in non-industrialized areas (de Rooij et al., 1998). In 2. Material and methods Europe, the Water Framework Directive (WFD, Directive 2000/ 60/EC) classified 1,2-DCA as one of the 33 priority pollutants 2.1. Sampling of river sediments and river water and it has been identified similarly by the U.S. Environmental Protection Agency. The 1,2-DCA pollution in rivers and Sediments were sampled from the rivers Ebro, Elbe and estuaries is generally considered to be caused to a large extent Danube. Ebro sediment was sampled from a rice field in the by anthropogenic sources; however, 1,2-DCA can in low southern part of the river delta (N: 4041011.800;E:00370 31.500) concentrations originate from natural sources (de Rooij et al., in July 2004 and had a clay-like structure. The rice field is 1998). flooded with water from the river, every year from April to Previous studies have focused on the fate of 1,2-DCA in the September and has been formed by sedimentation. environment and showed that it can be transformed through Elbe sediment was sampled near Scho¨ nberg (N: 5290073.200; abiotic as well as biotic reactions. Abiotically, 1,2-DCA is E: 1187021.900) at the west bank of the river in October 2004. transformed to ethylene glycol or VC. However, this is a very The sediment was clear and sandy. Artificial reconstruction slow process (half life >72 years) (Jeffers et al., 1989), and the activities of the river bank were carried out about a year before resulting products may even be more toxic than 1,2-DCA itself sampling. (Gallegos et al., 2007). In contrast, micro-organisms can Danube River sediment was sampled at the East bank near transform 1,2-DCA rapidly to non-toxic end products via Budapest (4727025.800;E:1903046.800) in April 2005. This sedi- different pathways. In the presence of oxygen, 1,2-DCA can ment had a clayey structure. À completely be oxidized to CO2,H2O and Cl by different Sediment samples were taken as 20 cm long vertical cores, bacterial species, including Xanthobacter autotrophicus (Janssen using sterilized PVC tubes (30 cm  3.2 cm inner diameter). et al., 1985) and Ancylobacter aquaticus (van den Wijngaard The PVC tube was completely pushed into the sediment and et al., 1992). However, in aquifers and sediments, oxygen is closed with butyl rubber stoppers on both sides when the tube often not available. The oxidation of 1,2-DCA in the absence of was drawn back. The tubes were stored at 4 C for maximally oxygen has also been observed with nitrate as alternative 1 month until microcosms were set up. electron acceptor (Gerritse et al., 1999). Recently, this process Water sampling was done using a 1-liter sterile glass jar, has been described in more detail by Dinglasan-Panlilio and which was completely filled under water, closed with a Viton co-workers (Dinglasan-Panlilio et al., 2006). stopper, and stored at 4 C. Under methanogenic conditions, ethene is usually the main Sediments and river water were characterized by partners end product of 1,2-DCA dechlorination (Egli et al., 1987) and is in the Aquaterra project: Consejo Superior de Investigaciones formed via either a cometabolic or halorespiration process. Cient A˜ ficas (CSIC), Barcelona, Spain, for Ebro samples; Dehalococcoides ethenogenes strain 195 (Maymo-Gatell et al., Helmholtz-Zentrum fu¨ r Umweltforschung (UFZ), Magdeburg, 1999) and Desulfitobacterium dichloroeliminans strain DCA1 (de Germany, for Elbe samples; International Commission for the Wildeman et al., 2003a) are bacterial isolates that can convert Protection of the Danube River (ICPDR) for Danube samples; 1,2-DCA anaerobically into ethene by reductive dechlorina- and additional analyses on the sediments were performed tion. Chloroethane and ethane can also be formed via reduc- by Al-West B.V. (Deventer, The Netherlands) (Table 1). The tive dechlorination of 1,2-DCA. However, this has scarcely concentration of most CAHs (vinyl chloride,
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