Journal of Hazardous Materials 274 (2014) 399–403

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Response of soil bacterial community to metal nanoparticles in biosolids Vishal Shah ∗ , Jamilee Jones, Jenifer Dickman, Steven Greenman Department of Biology, Dowling College, Oakdale, NY 11769, USA

h i g h l i g h t s • Toxicity of five different metal NPs against soil bacterial community as a function of time has been studied. • ZnO and Cu NPs did not change the structure of soil bacterial community when present in biosolids. • Ag nanoparticles, anatase and rutile TiO2 nanoparticles altered the structure of bacterial community.

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Article history: Received 7 February 2014 Received in revised form 4 April 2014 Accepted 5 April 2014 Available online 13 April 2014 Keywords: Nanoparticles Microbial toxicity Biosolids

a b s t r a c t The increasing use of engineered nanoparticles (NPs) in industrial and household applications will very likely lead to the increased release of such materials into the public sewer systems. During the wastewater treatment process, some fraction of NPs would always be concentrated in the biosolids. When biosolids is applied on the agricultural land, NPs are introduced into the soil matrix. In the current study we investigate the influence of five different metal nanoparticles present in biosolids on soil microbial community as a function of time. Results indicate that ZnO and Zero Valent Cu NPs were not toxic to soil bacterial community. Biosolids mixed with Ag NPs and TiO2 (both anatase and rutile phase) in contrast changed the bacterial richness and composition in wavering pattern as a function of time. Based on the observations made in the study, we suggest caution when interpreting the toxicity of NPs based on single time point study. © 2014 Elsevier B.V. All rights reserved.

1. Introduction With increasing inventions related to the applications of nanoparticles (NPs), more than 15% of all products on the global market today is predicted have some kind of nanotechnology incorporated into their manufacturing process [1]. Increase in production and use of NPs will inextricably lead to an increase in their release into the environment. Numerous studies have shown that NPs may be released into sewer systems by industrial and municipal sources and thus reach wastewater treatment plants [2–7]. In a typical wastewater treatment process, NPs will either deposit in the wastewater sludge and depending on the process conditions can undergo desorption and or complexation/ionization [5]. While the percentage of the NPs removed from the wastewater by the treatment plants depends on numerous process parameters, a fraction of NPs would always be concentrated in the sludge [5,8,9]. The sludge generated from the waste treatment plants is normally

∗ Corresponding author. Tel.: +1 631 244 3339; fax: +1 631 244 1033. E-mail address: [email protected] (V. Shah). http://dx.doi.org/10.1016/j.jhazmat.2014.04.003 0304-3894/© 2014 Elsevier B.V. All rights reserved.

stabilized to reduce its pathogen content and is therein termed as biosolids. In the United States, each year 7 million dry tons of biosolids are generated by the wastewater treatment plants and approximately 60% is disposed of on agricultural land [10]. Traditional disposal on agricultural land provides an economic disposal method for large volumes of biosolids generated every day, reduces the erosion of soil, serves as a cheap substitute for chemical fertilizers, and improves soil properties [11]. Biosolids are also disposed on forests, rangelands, or on disturbed land in need of reclamation [11]. Most researchers agree that the effects of organic compounds, metals, and microorganisms in biosolids are not harmful to humans or the environment if managed carefully [12]. Studies have shown that metals in biosolids are chemically bound in stable compounds and will not easily move into ground and surface waters [12]. However, little information is available on the impact of NPs present in the biosolids on the soil microbial community. In the only study conducted thus far, Colman et al. recently reported the adverse effects of low concentration of silver nanoparticles in biosolids on soil microbial community [13]. The study reported here was undertaken to compare the effects of five different metal NPs (Ag

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V. Shah et al. / Journal of Hazardous Materials 274 (2014) 399–403

NPs, Cu NPs, TiO2 NPs (anatase and rutile phase), and ZnO NPs) on soil microbial community over time, when present in the biosolids. NPs were selected based on the literature showing their reported appearance and/or the high probability of their future occurrence in public wastewater treatment plants as well as the sludge that is recovered from such plants [2–7,9].

2. Experimental 2.1. Materials Upon the removal of plant litter, top soil was collected from Pine Barrens Forest region of NY [14]. The sampling location was away from any roads or human development and no permit was required to collect the soil. Detailed characterization of soil has been reported elsewhere [14]. In brief, the soil is acidic with pH between 4.3 and 4.9, sandy, and rich in iron and aluminum. Total Organic Carbon (TOC) was between 14.9 and 37.1 g/kg and Total Kjeldahl Nitrogen (TKN) was between 1.0 and 4.4 g/kg [14]. The biosolids and wastewater effluent were obtained from the wastewater treatment plant located within Brookhaven National Laboratories, Upton, NY. NPs were purchased from Sun Innovations, USA in powder form and had no surface coating. The properties of the NPs were provided by the manufacturer and the particles were used as received. TiO2 NPs (Anatase phase) were 99.0% pure, with an average size range of 5–10 nm. TiO2 NPs (Rutile phase) were 98% pure with an average size of 55 nm. Zero valent Cu NPs (Co NPs) were 99.8% pure, with an average size of 25 nm and size range of 2–60 nm. Ag NPs were 99.8% pure, with an average size of 35 nm. ZnO NPs were 99.8% pure, with an average size of 35 nm. 2.2. Experimental set up The soil was transported in laboratory in plastic buckets and any visible debris (plant matter, rocks, and wood chips) was removed manually. Before the beginning of experiment, the soil was homogenized by mixing it with hands for 30 min. 2.0 L of waste effluent was filtered through a 0.22 ␮m filter. Individual NPs stock solution were prepared by adding NPs to the filtrate to give final concentration of 10 ppm followed by sonication at 25 ◦ C, 250 W, and 40 kHz for 1 h. 2.5 kg of biosolid was homogenized by hand in trays by kneading and mixing for 10 min. 10 mL of NP stock solution (0.1 mg NPs) was added to 400 g of homogenized biosolids and mixed manually for 30 min. For the control experiment, 10 mL of filtrate was added (without NPs) and mixed for 30 min. 50 g of NP containing biosolids (0.0125 mg NPs) were then added to 150 g of soil, mixed for 15 min, and added to NalGene RapidFlow Sterile Bottles fitted with 0.22 ␮m filters. Four bottles were set up for control and each of the NPs studied. The final concentration of NPs in the soil was 0.0625 mg NPs/kg soil. The bottles were incubated in an environmental chamber set at 25 ◦ C under 16 h light/8 h dark cycle. Distilled water was added periodically to maintain constant moisture content. During each sampling time point, one bottle was removed from the environmental chamber for control and experimental sets. Prior to sampling, the bottles were shaken vigorously for 2 min for homogenization. 2.3. DNA extraction and microbial tag-encoded FLX amplicon pyrosequencing (TEFAP) DNA isolation and bacterial pyrosequencing was carried out using the protocol described earlier [14]. In brief, PowerSoilTM DNA Isolation Kit (MO BIO Laboratories, Inc. CA) was used to extract the DNA. The microbial tag-encoded FLX amplicon pyrosequencing

(TEFAP) was performed using primers Gray28F 5 GAGTTTGATCNTGGCTCAG and Gray519r 5 GTNTTACNGCGGCKGCTG. 2.4. Statistical analysis DNA isolation was performed in duplicate for each sample and two isolated DNA samples were pooled prior to pyrosequencing. To ensure that minor changes in abundance of Genus that are present in lower percentage did not influence the results, only those present at >1% abundance were used in the statistical analysis. Table S1 shows the total bacterial community in each of the soil sample tested. As the assumption that the data being analyzed would be normally distributed may not always hold true, nonparametric statistical analysis were performed. Wilcoxon Matched Pair test was used to compare the pyrosequencing data between untreated control versus treated samples. A value of ≤0.05 indicates a significant difference between compared values. Analysis was performed using Statistica (Release 8.0) software. Bacterial richness was calculated as the sum of number of genus occupying more than 1% of the total community. 3. Results Organisms belonging to Acidobacterium, Pirellua, and Nitrospira are the major contributors in the microbial community of control soil mixed with biosolids on day 0 (Table 1). A significant shift in the community was observed in control within 30 day of incubation, with organisms from Rudaea genus now occupying 50% of the total community. The organisms from this genus are known for cellulose degradation and remain predominant in the bacterial community of control soil throughout the duration of experiment (Table 1) [15]. Statistical comparison of the bacterial community in the control soil to NP exposed soil suggests that zero valent Cu NPs and ZnO NPs do not change the structure of community significantly. p value >0.05 was observed for all the time points tested. Fig. 1 illustrates that the richness in the soil exposed to these NPs also remained fairly consistent as a function of time. Ag NPs significantly altered the bacterial community in soil within 30 days of incubation. However, the observed change cannot be considered toxic since there an increase in the richness as compared to control, and an increase in organisms involved in nitrogen cycle, Nitrosovibrio, Nitrospira and Bradyrhizobium genera (Table 1 and Fig. 1). While no change was observed in the soil exposed to Ag NPs for 60 days, prolonged incubation resulted in sharp decline in the richness. Richness value of 13 was observed for both 90 and 120 days incubated soil sample containing NPs, as opposed to 20 and 19 in the control sample for respective sampling time points (Fig. 1). Organisms from Bacillus and Geobacter genera occupy double the fraction of bacterial community in Ag NPs containing soil sample sampled on 120th day as opposed to control soil. Comparison of the influence of TiO2 NPs in Anatase and Rutile phase suggests that while both the NPs do alter the community structure significantly, TiO2 in Rutile phase has more prolonged influence then Anatase phase NPs. p value 0.05 was observed when the bacterial community in TiO2 Anatase phase NPs exposed soil was compared to control soil. The community structure in both the TiO2 exposed soil became statistically similar to control soil (p > 0.05) after 120 days of incubation. Similar to Ag NPs, sharp increase in the richness was seen in the soil sample incubated for 30 days with TiO2 NPs (Fig. 1). The increase in richness is because of the appearance of organisms from genera that were occupying less than 1% of the bacteria community. Organisms from Rudaea genus seem to be mostly sensitive to TiO2 NPs (Table 1). When incubated for 120 days, while the

Table 1 Percentage of rDNA sequences of bacteria present in the soil treated with biosolids without NP (control) and with NPs. Only genus occupying 1% or more of the total community was included in the statistical analysis. Genus

Soil-BS

Control

Ag

Day 0

TiO2 (A)

TiO2 (R)

ZnO

Control

Day 30 0 10 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 1 1 1 1 0 0 2 0 0 0 1 1 3 1 2 0 0 2 1 0 50 0 0 0 0 1 0 0

1 9 0 0 0 1 3 1 0 0 0 0 2 0 0 0 1 2 1 1 1 1 2 9 0 0 1 1 1 5 2 2 1 0 2 1 1 23 0 1 0 0 0 1 0 0.00

0 1 1 0 0 9 16 12 15 8 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 1 1 1 0 2 3 2 1 1 1 1 1 0 1 0 1 1 1 0 1 1 1 0 1 0 0 1 0 1 0 0 0 0 0 1 3 2 1 1 0 0 0 1 0 0 0 1 0 0 0 1 1 0 0 0 1 1 0 0 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 4 1 1 1 1 1 0 1 2 0 1 2 2 1 0 3 0 1 1 0 0 0 1 1 1 1 1 2 2 0 0 1 1 1 0 1 0 1 0 1 1 4 7 12 3 4 1 2 2 1 1 4 1 1 1 4 1 2 1 0 0 0 1 1 0 0 3 2 3 2 2 1 1 2 2 2 1 1 1 1 1 38 8 13 49 35 0 1 1 0 0 0 1 0 0 1 0 1 1 0 0 1 0 1 0 1 1 0 0 1 0 1 2 1 0 0 0 0 0 0 0 0.19 0.00 0.00 0.36

Ag

Cu

TiO2 (A)

TiO2 (R)

ZnO

Control

Day 60 0 0 0 0 0 2 8 8 3 4 15 3 0 0 0 7 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 3 3 1 0 2 2 1 1 0 0 1 0 1 0 1 1 0 0 0 0 1 1 0 1 0 0 1 1 0 1 0 0 0 0 0 0 2 2 1 1 1 2 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 3 1 1 2 0 1 1 1 1 0 1 0 1 1 1 1 0 1 2 0 6 3 2 1 1 1 1 2 1 1 0 1 0 0 0 1 3 4 0 0 1 0 0 0 0 0 0 0 1 0 0 0 2 0 0 0 0 0 1 0 1 1 1 1 1 1 1 1 0. 0 1 1 5 7 2 1 6 2 1 1 1 1 2 0 5 5 0 0 1 1 0 1 0 0 1 0 0 1 0 0 0 1 4 2 1 1 2 2 2 2 2 2 2 1 1 1 1 0 1 1 33 31 65 60 27 55 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 0 0 1 0 0 0.76 0.85 0.00 0.01 0.24

Ag

Cu

TiO2 (A)

TiO2 (R)

ZnO

Control

Day 90 0 0 1 0 0 0 2 10 7 12 3 2 0 0 0 0 0 1 0 0 0 2 0 0 0 0 0 0 0 3 0 0 0 0 1 0 1 1 1 3 2 1 0 0 1 0 0 1 0 1 0 0 1 0 1 0 1 1 0 1 3 1 1 0 2 3 0 0 0 0 0 0 1 2 2 1 1 20 2 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 1 0 0 0 0 1 1 0 0 1 0 0 0 5 2 0 1 4 5 0 3 2 1 1 1 3 1 0 1 2 2 1 3 0 1 5 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 1 1 0 1 0 1 1 1 1 1 1 11 6 8 1 2 0 1 1 1 1 0 1 0 1 6 1 0 0 1 0 1 0 0 0 0 0 0 1 0 1 1 2 5 1 1 1 1 1 1 1 1 0 1 1 : 0 0 71 40 31 9 46 34 0 1 0 0 0 0 0 0 2 1 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 3 1 0 1 0 1 2 0 0 0 0 0 0 0 0.01 0.76 0.05 0.01 0.42

Ag

Cu

TlO: (A)

TlO: (R)

ZnO

Day 120 1 1 1 0 0 4 4 2 6 5 0 0 0 0 0 0 0 0 0 1 11 5 0 2 5 0 0 0 0 1 0 1 1 1 1 4 3 2 1 4 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 0 0 0 0 0 26 22 25 53 28 0 0 0 0 0 1 1 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 1 1 0 1 2 2 2 1 3 1 1 1 0 0 7 3 4 5 8 0 2 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0 1 0 2 0 0 1 3 3 4 2 3 0 0 0 0 1 0 1 1 0 1 0 0 0 0 0 0 0 0 0 0 1 2 2 1 3 0 1 1 0 1 1 0 0 1 1 15 24 25 11 7 0 0 0 0 0 0 0 1 1 0 0 0 1 0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.43 0.14 0.73 0.21 0.06

V. Shah et al. / Journal of Hazardous Materials 274 (2014) 399–403

Acetivibrio 0 17 Acidobacterium 0 Alicyclobacillus Aquiflexum 3 0 Bacillus Blastochloris 1 2 Bradyrhizobium 0 Burkholderia 1 Caldilinea 0 Caulobacter 1 Chitinophaga 3 Chloroflexus 1 Clostridium 0 Coxiella 0 Cytophaga 1 Denitratisoma 1 Derxia 0 Dyella 0 Edaphobacter 0 Flavisolibacter 1 Flavobacterium 1 Gemmattmonas 0 Geobacter 0 Geothrix Haliscomenobacter 4 1 Hyphomicrobium 2 Metiiylocapsa 0 Mycobacterium 0 Natronocella 1 Nitrosovibrio 5 Nitrospira 0 Opitutus 8 Pirelhla 1 Polyangium 2 Rhizobium 0 Rhodanobacter 1 Rhodoplanes 0 Rudaea 1 Schlegelella 0 Sideroxydans 0 Sphingobacterium 1 Sterolibacterium 0 Terrimonas 1 Thennomicrobium 0 Thiorhodospira p value

Cu

401

402

V. Shah et al. / Journal of Hazardous Materials 274 (2014) 399–403

Fig. 1. Bacterial richness in control and nanoparticles in biosolids exposed soil as a function of time.

community is statistically similar to the control soil, the richness of soil incubated with Rutile phase TiO2 has significantly declined (Fig. 1).

4. Discussion There are only few studies reported on the influence of metal NPs on soil microbial diversity. In all of these studies a similar conclusion has been reached that metal NPs indeed change the composition of soil microbial communities [16–26]. The results obtained in the current study are in line with those obtained in literature. All NPs tested here altered the bacterial community structure in soil to varying degree. Cu and ZnO NPs altered the structure minimally. The observed results can be attributed to higher affinity of biosolids for Cu and Zn and to the biological adaptation of soil microbes to transition metals. Over period of time, Cu and ZnO NPs have been shown to undergo ionization in soil [25]. In the microcosms, NPs and ions could be presumed to be tightly bound to the biosolids preventing direct contact between microorganisms and the metal. Such contact has been shown to be critical for any toxicological observations [27]. The soil of Pine Barrens Forest has iron concentration and the bacteria present in the soil have evolved to live in the presence of such high concentration [14]. Since Cu and Zn belong to same transition metal group as iron, the community could resist the presence of Cu and ZnO NPs. Ag NPs have been shown to undergo oxidation and sulfidation in soil over time [5,28]. The changes in bacterial community over time could be a response to the changing chemical state of Ag. During 30 and 90 day sampling time point, Ag could be presumed to be in a state having higher influence on the soil community as opposed to day 60 and 120. Coleman et al. showed a sharp increase in N2 O production from the soil treated with Ag NPs after 8 days of incubation [13]. They also observed that the N2 O production was similar to control soil samples after 50 days of incubation. The increase in Nitrosovibrio and Nitrospira observed in the current study after 30 days of incubation and subsequent return to control levels supports their observation. Organisms from these genera are known to oxidize ammonia. Increase in ammonia oxidizers and the subsequent increase in N2 O could not only have global environmental consequences as suggested by Coleman et al. but could also have human health effect in the area around the fields where Ag NPs are dispersed through biosolids.

The influence of crystalline state of TiO2 NPs on soil bacterial community is noteworthy. The positive influence of TiO2 on soil richness was striking within 30 days of incubation. It has been long known in the literature that TiO2 in rutile state is more stable as opposed to anatase state [29] and can interact with heavy metals. Kim et al. reported the presence of aggregates of TiO2 NPs with rutile phase crystalline structure in sewage sludge [5]. They showed the property of these NPs to interact with heavy metals. In the current study, we propose that TiO2 NPs interact with the heavy metals present in the environment, decreasing their bioavailability and thereby increasing richness within the soil. Over a period of time, the NPs would undergo transformation resulting in the decreased interaction with the heavy metals. Increased biologically available heavy metals would impact the bacterial diversity, and indeed the richness dropped in the soil sample sampled on 60th day. Differential rate of transformation between anatase and rutile phase TiO2 NPs could be responsible for varied influence on soil microbial diversity. Detailed chemical and physical characterization of NPs in the soil was not possible due to low concentrations of particles used in the study. This prevents any direct correlation between observed changes in the bacterial community and changes in NP chemistry. Nevertheless, the observations made in the current study, including wavering richness and bacterial community structure suggests that further detailed time course studies to better understand the ecological impacts of NPs. We also suggest that the scientific community be extremely cautious when classifying NP as ecologically toxic based on a single time point study.

Acknowledgement The research was supported by the National Science Foundation grant #0966741.

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Response of soil bacterial community to metal nanoparticles in biosolids.

The increasing use of engineered nanoparticles (NPs) in industrial and household applications will very likely lead to the increased release of such m...
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