Effects of iron-carbon materials on microbial-catalyzed reductive dechlorination of polychlorinated biphenyls in Taihu Lake sediment microcosms: Enhanced chlorine removal, detoxification and shifts of microbial community

Highlights

• Low dose of ZVI could apprently favor microbial PCB dechlorination.

• nZVI triggered dechlorination faster than mZVI in the short term.

• GAC, nZVI/GAC and nZVI&GAC also could facilitate dechlorination.

• Dechlorination enhancement was primarily via meta dechlorination pathways.

• Bacterial community greatly shifted under different amendment conditions.

Abstract

Nano zero-valent iron particles (nZVI, 0.09 wt%), micro zero-valent iron particles (mZVI, 0.09 wt%), granular activated carbon (GAC, 3.03 wt%), GAC supported nZVI (nZVI/GAC, 3.12 wt%) and nZVI&GAC (nZVI 0.09 wt%, GAC 3.03 wt%) were evaluated for their effects on polychlorinated biphenyls (PCBs) anaerobic reductive dechlorination, detoxification, as well as microbial community structure in Taihu Lake (China) sediment microcosms. The results showed that all of these five materials could stimulate PCBs reductive dechlorination, especially for dioxin-like PCB congeners, and nZVI&GAC had the best removal effect on PCBs. The reduction of total PCBs increased from 13.5% to 33.2%. H₂ generated by zero-valent iron corrosion was utilized by organohalide-respiring bacteria (OHRB) to enhance the dechlorination of PCBs predominantly via meta chlorine removal in the short term. The addition of ZVI had little impact on the total bacterial abundance and the microbial community structure. The adsorption of GAC and potential bioremediation properties of attached biofilm could promote the long-term removal of PCBs. GAC, nZVI/GAC, nZVI&GAC had different influences on the microbial structure. These findings provide insights into the biostimulation technique for in situ remediations of PCBs contaminated sediments.

Introduction

Polychlorinated Biphenyls (PCBs) are a class of chlorinated aromatic compounds, including 209 molecules known as congeners. They are composed of biphenyl with 1 to 10 chlorine atoms substituted at the ten available positions (Bedard, 2008). From 1929 to 1970S, PCBs were widely used for various industrial applications as fluid-filled capacitors and transformers, hydraulic fluids, heat transfer fluids, and dielectric fluids due to their excellent chemical stability, heat resistance, non-flammability, and low water solubility (Brown et al., 1987b; Quensen et al., 1988). PCBs released into the environment could cause a series of environmental issues and be bioaccumulated and biomagnified through the food chain (Schantz et al., 2003). They were also suspected of associating with many health problems (Lyall et al., 2017; Simhadri et al., 2020). In 2001, PCBs were listed as Persistent Organic Pollutants by the Stockholm Convention (Simhadri et al., 2020). Although commercial PCBs production and use had been banned, the persistence of PCBs led to their long-term presence in the environment (Sinkkonen and Paasivirta, 2000). Hydrophobic PCBs can be easily sorbed by natural organic matters (NOMs). Therefore, soil and sediment had become the primary sink of PCBs (Lu et al., 2021; Nakata et al., 2006). Most traditional techniques like dredging, solvent extraction, or thermal desorption used for PCB-impacted sediments are costly and may cause secondary pollution (Passatore et al., 2014). Therefore, PCB bioremediation attracts an increasing amount of attention because of its low cost and environmental friendliness. As an effective dechlorination and detoxification route, microbial-catalyzed anaerobic reductive dechlorination of PCBs had been commonly observed in many sediment systems globally since the 1980s (Alder et al., 1993; Brown et al., 1987a; Kjellerup et al., 2008; Park et al., 2011; Payne et al., 2011; Qiu et al., 2020; Quensen et al., 1990; Rhee et al., 1993; Sokol et al., 1998). Anaerobic reductive dechlorination converts high chlorinated PCBs into low chlorinated clusters, reduces their toxicity and bioaccumulation potential, and makes PCBs more easily degraded, even completely mineralized by the aerobic microorganisms (Passatore et al., 2014; Praveckova et al., 2016; Zanaroli et al., 2012). Taihu Lake, the third-largest freshwater lake and important drinking water source in China, had been suffering from extensive eutrophication and cyanobacteria blooms occur frequently (Qin et al., 2007; Xu et al., 2010). It was reported that NO₃⁻-N concentrations were as high as 12.06 mg/kg and 3.18 mg/L in the north of Taihu lake sediments and water, respectively (Gao et al., 2019). Nitrate was added in this study to simulated the environment of Taihu Lake. Moreover, a variety organohalogen pollutants including PCBs, PBDD/PBDFs, and PCDD/PCDFs, had been found in Taihu Lake sediments with high measured Toxic equivalencies (TEQs) 0.7–1.6 pg/g dry weight, 0.16–1.6 pg/g, and 2.7–6.9 pg/g, respectively, indicating that existed high dioxin-like activity (Li et al., 2019; Xu et al., 2015; Zhou et al., 2012). As a natural attenuation process, PCB dechlorination in Taihu Lake sediments remain unclear yet.

To date, limited numbers of organohalide-respiring bacteria (OHRB) have been identified as PCB dechlorinators. Most of them belong to the phylum Chloroflexi like Dehalococcoides mccartyi strain CBCD1 (Adrian et al., 2009), 195 (Fennell et al., 2004), CG1, CG4, CG5 (Wang et al., 2014; Wang and He, 2013), SG1, CG3 (Wang et al., 2019a), JNA (Laroe et al., 2014), Dehalobium chlorocoercia strain DF-1 (May et al., 2008), Bacterium ortho-17 (Cutter et al., 1998) and two different phylotypes DEH10 and SF-1 (Fagervold et al., 2005). These microorganisms play a crucial role in the anaerobic dechlorination of PCBs (Fagervold et al., 2005; Field and Sierra-Alvarez, 2008; Quensen et al., 1988; Rysavy et al., 2005). To our best knowledge, the identified PCB dechlorinators are strictly anaerobic and grow slowly with carbon sources (acetate, lactate et al.), electron donors (mainly hydrogen) (Sowers and May, 2013; Xiao et al., 2020). The difficulties in dechlorinator isolation and enrichment limit their bioremediation applications (Qiu et al., 2020; Zanaroli et al., 2012). The supplementation of electron donors is regarded as an effective biostimulation approach that promotes PCB dechlorination by boosting the growth of OHRB (Varadhan et al., 2011). Hydrogen (H₂), an ideal electron donor, can be directly utilized by OHRB but not practical to use in contaminated sediments directly (Zanaroli et al., 2012). For in situ bioremediation, zero-valent iron (ZVI) is a potential substitute because H₂ produced by iron corrosion could continuously provide electron donors for OHRB (Rysavy et al., 2005; Wang et al., 2016; Zanaroli et al., 2012). A previous study reported that the lag time of PCB dechlorination in Baltimore Harbor sediments could be reduced with ZVI supplementation (0.1 g/g dry sediment) by creating a niche for OHRB via H₂ production (Rysavy et al., 2005). This perspective was confirmed by other researchers, and even lower doses of iron (0.01 g/g dry sediment or 6.7 g/kg dry sediment) could still promote PCBs dechlorination (Varadhan et al., 2011; Zanaroli et al., 2012). However, the effectiveness of biostimulation largely depended on indigenous microbial population (Winchell and Novak, 2008) and a significant amount of soluble Fe²⁺ ion produced by corrosion of ZVI might harm microorganisms (Dunning et al., 1998; Rysavy et al., 2005). Activated carbon (AC) could remove PCBs from the water phase and reduce the toxicity and bioavailability of PCBs by adsorption in laboratory and field studies (Kjellerup et al., 2014). AC also affected the biodegradation process because AC could facilitate the attachment of microorganisms to form a biofilm and enrich some specific microorganisms (Mercier et al., 2014). Besides, AC could serve as an electron shuttle in the anaerobic biological reduction (Pereira et al., 2016), presumably promoting biodegradation. Therefore, it is worthy of research on ZVI-AC material for the biodegradation of PCB in Taihu Lake sediments and their effect on microorganisms.

Nano zero-valent iron(nZVI) is more reactive than conventional ZVI powders because of the greater surface area (Li et al., 2006). However, nZVI is easy to agglomerate and react with environmental media to lose its reactivity (Zhao et al., 2016). AC as great support could prevent nZVI particles from agglomeration, prolong the reactivity of the particles, and adsorb and stabilize hydrophobic contaminants on the particle surface (Beckingham and Ghosh, 2011; Schrick et al., 2004). A study had successfully applied carbon-supported nZVI for abiotic PCB dechlorination (Liu et al., 2016). However, the amount of carbon-supported nZVI was close to 80 g/L. The high costs prohibited its application in in situ remediation. So far, there were few studies focused on the use of nZVI/AC for microbial-catalyzed PCB dechlorination.

In this study, low levels nZVI, micro ZVI (mZVI), GAC, nZVI/GAC, nZVI and GAC (nZVI&GAC) were investigated for their effects on PCB dechlorination in Taihu Lake sediment microcosms. Dechlorination extent, pathway preferences, and microbial community structure were comprehensively examined and analyzed to better elucidate the mechanisms of enhanced microbial-catalyzed PCB reductive dechlorination. Therefore, the findings of the present study may provide a promising approach for in situ bioremediation of PCB-impact sediments and have practical significance.