Elsevier

Environmental Pollution

Volume 220, Part B, January 2017, Pages 1068-1078
Environmental Pollution

Impact of bio-palladium nanoparticles (bio-Pd NPs) on the activity and structure of a marine microbial community

https://doi.org/10.1016/j.envpol.2016.11.036Get rights and content

Highlights

  • Bio-Pd NPs are deemed not toxic in standard V. fischeri ecotoxicity test.

  • Impact of Bio-Pd NPs tested on microbial community in its native sediment and water.

  • Bio-Pd NPs impact is limited to few respiratory activities.

  • Microbial community is resilient to bio-Pd NPs.

Abstract

Biogenic palladium nanoparticles (bio-Pd NPs) represent a promising catalyst for organohalide remediation in water and sediments. However, the available information regarding their possible impact in case of release into the environment, particularly on the environmental microbiota, is limited. In this study the toxicity of bio-Pd NPs on the model marine bacterium V. fischeri was assessed. The impacts of different concentrations of bio-Pd NPs on the respiratory metabolisms (i.e. organohalide respiration, sulfate reduction and methanogenesis) and the structure of a PCB-dechlorinating microbial community enriched form a marine sediment were also investigated in microcosms mimicking the actual sampling site conditions. Bio-Pd NPs had no toxic effect on V. fischeri. In addition, they had no significant effects on PCB-dehalogenating activity, while showing a partial, dose-dependent inhibitory effect on sulfate reduction as well as on methanogenesis. No toxic effects by bio-Pd NPs could be also observed on the total bacterial community structure, as its biodiversity was increased compared to the not exposed community. In addition, resilience of the microbial community to bio-Pd NPs exposure was observed, being the final community organization (Gini coefficient) of samples exposed to bio-Pd NPs similar to that of the not exposed one. Considering all the factors evaluated, bio-Pd NPs could be deemed as non-toxic to the marine microbiota in the conditions tested. This is the first study in which the impact of bio-Pd NPs is extensively evaluated over a microbial community in relevant environmental conditions, providing important information for the assessment of their environmental safety.

Introduction

Nanoremediation is the application of reactive nanoparticles (NPs), such as nanoscale zero-valent iron (nZVI) (Theron et al., 2008, Zhang, 2003), Pd/Fe bimetallic NPs, carbon nanostructures and many more (Theron et al., 2008), for the detoxification of contaminated water and soils (Karn et al., 2009). NPs show very high reactivity and different properties compared to their bulk counterparts, due to their size and/or surface coatings, allowing efficient and controllable degradation activities, especially against recalcitrant pollutants (Macé et al., 2006, Serrano, 2010).

Pd nano-catalysts were efficiently used as catalysts for the reductive dechlorination of several contaminants (Ukisu and Miyadera, 2003), which occurs through the development of radical cathodic hydrogen from molecular hydrogen (Choi et al., 2009, De Windt et al., 2005). Additionally, Pd NPs can be obtained through bioprecipitation in bacterial cultures and they are referred to as biopalladium nanoparticles (bio-Pd NPs) (Baxter-Plant et al., 2003, De Windt et al., 2005). Bio-Pd NPs were effectively used for the degradation/transformation of contaminants such as heavy metals, azo dyes, pesticides and organohalides in groundwater, wastewater, air, soil, sediments (De Corte et al., 2012, Hennebel et al., 2009, Hennebel et al., 2012, Mertens et al., 2007, Hosseinkhani et al., 2014b, Quan et al., 2015).

Polychlorinated biphenyls (PCBs) are hydrophobic halogenated compounds, extremely recalcitrant to biodegradation and exhibiting toxicity on the environment and on all levels of the trophic chain, including humans (Stockholm Convention, 2004). PCB pollution is persistent in the environment, especially in sediments (Fernández and Grimalt, 2003). In these environmental compartments, however, some microorganisms of the phylum Chloroflexi are able to use them as terminal electron acceptor, which leads to the sequential removal of chlorine atoms from the molecule, resulting in usually lower toxicity and easier biodegradation of PCBs in the aerobic layers (Sowers and May, 2013, Zanaroli et al., 2015). This process is known as microbial reductive dechlorination, and was studied in freshwater sediment cultures (Bedard, 2008, Field and Sierra-Alvarez, 2008, Wiegel and Wu, 2000), and to a lesser extent in marine sediments (Fava et al., 2003a, Fava et al., 2003b, Zanaroli et al., 2015, Zanaroli et al., 2006). Despite their higher environmental and economic sustainability compared to traditional remediation technologies (Khan et al., 2004, Perelo, 2010), microbial reductive dechlorination processes are extremely slow (Wiegel and Wu, 2000) and might require complementation with environmental friendly chemical approaches.

Bio-Pd NPs were recently suggested as a promising approach to enhance PCB degradation in marine environments, as they allow complete dechlorination of TCE in synthetic marine water and marine slurries of water and sediments (Hosseinkhani et al., 2014a, Hosseinkhani et al., 2014b) and extensive dechlorination of Aroclor 1254 PCBs to monochlorobiphenyls (Hosseinkhani et al., 2015). However, concerns are rising around the environmental remediation approaches using these NPs, which may pose risk for aquatic environments (Moore, 2006) and toxic effects on humans (Jiang et al., 2009, Schrand et al., 2010). Pd-NPs, in particular, have an inhibiting effect on E. coli and S. aureus growth, resulting in decreasing CFU/ml values when exposed to Pd-NPs concentrations ranging from 10−9 to 10−4 M of Pd-NPs (Adams et al., 2014). Pd-NPs also inhibit kiwifruit pollen development with an EC50 value of 0.12–0.23 mg/l (Speranza et al., 2010) and show alteration in human peripheral blood mononuclear cells already at 10 μg/ml (Petrarca et al., 2014). These concentrations are similar to or lower than the 5–50 mg/l of bio-Pd NPs used in previous remediation approaches (Hennebel et al., 2009, Hosseinkhani et al., 2014b, Hosseinkhani et al., 2015). Conversely, no toxicity of Pd NPs has been observed on other organisms, such as zebrafish and lettuce seeds (Kovrižnych et al., 2013, Shah and Belozerova, 2009). Since toxic effects would eventually invalidate their benefits as coadiuvant in remediation processes (Grieger et al., 2010, Karn et al., 2009, Schrand et al., 2010, Otto et al., 2008), it is necessary to evaluate risk factors of Pd-NPs as well as other metallic NPs before application (Nowack and Bucheli, 2007, Wiesner et al., 2006). Standardized experimental conditions and analytical protocols are however still lacking (Crane et al., 2008, Grieger et al., 2010, USEPA, 2007, USEPA, 2014). The V. fischeri-based ecotoxicity assay been reported among the most sensitive for the evaluation of sediments and metals toxicity (van Beelen, 2003). In particular, it exhibited lower detection limits of toxic units in sediments elutriates when compared to D. magna standard test (Hyötyläinen and Oikari, 1999) and a broader spectrum of sensitivity towards metals than daphnids or green algae (Hsieh et al., 2004). It is also currently referred to as a standard test for NPs toxicity (Sánchez et al., 2011) and could be thus used to assess bio-Pd NPs toxicity. On the other hand, V. fischeri test might fail to give information on bio-Pd NPs impact over the active bioremediating microbial community, especially on selected metabolic activities and community structure (Farré et al., 2008, Sánchez et al., 2011). In addition, the information it provides is unrelated to any possible interplay between the NPs and the environmental matrix, which might affect their catalytic properties and exposure/toxicity to the (micro)organisms (Nowack and Bucheli, 2007, Wang et al., 2016). Therefore, prior actual delivery or accidental leaks into the environment, such impacts need to be assessed differently, i.e. in matrices close to the environmental conditions and for longer incubation time than current standard tests. Microcosms studies are a good compromise between the complexity of environmental matrices and the need to get preliminary data on the impact of NPs over microbial communities (Echavarri-Bravo et al., 2015), which then need to be thoroughly investigated further in mesocosms (Holden et al., 2016).

The aim of this work was to assess the ecological toxicity of bio-Pd NPs in marine environment using a comprehensive novel approach which complements Microtox® standardized acute toxicity test on V. fischeri (Ma et al., 2014) with evaluation of the impact on the whole microbial community in its sediment of origin. Since bio-Pd NPs could be used to complement biological reductive dechlorination activities with catalytic dehalogenation in nanoremediation approaches, a microbial culture enriched in indigenous organohalide respiring members was selected. In particular, the effects on the main respiratory metabolisms of the examined microbial community (i.e., dechlorination, sulfate reduction and methanogenesis), as well as on the total bacterial community structure were assessed.

Section snippets

Preparation of bio-Pd NPs

Preparation of bio-Pd NPs was performed through bioprecipitation by Shewanella oneidensis pure cultures according to De Windt et al. (2005). Briefly, cells were harvested from an over-night LB culture by centrifugation (4420 × g for 10 min) and washed three times with 50 ml M9 medium. Washed cells were resuspended in M9 medium to obtain an optical density at 610 nm of 0.7 ± 0.3. Palladium(II) and formate were added to a final concentration of 50 mg/l and 25 mM, respectively, from anaerobic

Results

The impact of bio-Pd NPs was assessed firstly on a model marine bacterium, V. fischeri, by assessing eventual inhibition of its bioluminescence. Then, tests focused on the eventual impact of bio-Pd NPs on the main respiratory metabolisms and the structure of a PCB dechlorinating marine microbial community. For this purpose, anaerobic sediment sub-cultures were set-up, in the presence and in the absence of spiked PCBs either: i) in absence of any amendments (unamended controls); ii) in presence

Discussion

Bio-Pd NPs have been recently shown to chemically dechlorinate PCBs in water and sediments (De Windt et al., 2005, Hennebel et al., 2012; Hosseinkhani et al., 2015), a process that may complement microbial PCB reductive dechlorination. In this study, their PCB dechlorination capabilities and the effects on the activity and structure of a marine microbial community was investigated in microcosms of a Venice lagoon sediment. A lack of catalytic activity by bio-Pd NPs over PCBs was evidenced in

Conclusions

Different approaches have been used to evaluate the effect of bio-Pd NPs on marine microbes and communities, taking into consideration their main metabolic activities, their biodiversity and community structure. Bio-Pd NPs do not exert toxicity towards the bioluminescent marine bacterium V. fischeri and may have limited inhibitory effects towards some respiratory metabolisms. In addition, an increase of the community biodiversity along with no permanent effects on its community organization

Acknowledgements

This study was supported by the European Commission [grant number 266473] (ULIXES Project).

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    1

    present address: Hasselt University, Biomedical research institute, Martelarenlaan 42, 3500 Hasselt, Belgium.

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