Elsevier

Chemosphere

Volume 147, March 2016, Pages 195-202
Chemosphere

Different responses of soil microbial metabolic activity to silver and iron oxide nanoparticles

https://doi.org/10.1016/j.chemosphere.2015.12.055Get rights and content

Highlights

  • AgNPs decrease soil microbial metabolic activity and metabolic efficiency.

  • FeONPs increase soil microbial metabolic activity and metabolic efficiency.

  • AgNPs and FeONPs have the contrast effects on soil nitrification process.

  • Nanoparticles invasion would influence the health and fertility of arable soil.

Abstract

The knowledge regarding the effects of metal or metal oxide nanoparticles on soil microbial metabolic activity and key ecological functions is limited, relative to the information about their species diversity. For this reason, the responses of soil microbial metabolic activity to silver (AgNPs) and iron oxide (FeONPs) nanoparticles, along concentration gradients of each, were evaluated by microcalorimetry and soil nitrification potential. The changes in abundances of bacteria, eukaryotes and ammonia-oxidizing bacteria were measured by real time quantitative PCR. It was found that AgNP (at 0.1, 1 and 10 mg kg−1 soil) amendments decreased soil microbial metabolic activity, nitrification potential and the abundances of bacteria and ammonia-oxidizing bacteria; on the contrary, FeONPs had the positive effects on soil microbial metabolic activity (at 1 and 10 mg kg−1 soil) and soil nitrification potential (at 0.1 and 1 mg kg−1 soil). Specific microbial metabolic activity and specific nitrification potential further revealed that metal or metal oxide nanoparticles could change the C and N cycles of the agricultural soil through influencing soil microbial metabolism. These findings could deepen the understanding of the influence of NPs on soil microorganisms and their driven soil ecology process.

Introduction

Soil microorganisms, the indispensable agents of soil ecosystem, are responsible for decomposition of organic residues and are the key players in driving nutrient cycling in arable soils, such as cycling of nitrogen, phosphorus and potassium (Kaye et al., 2005). Thereby soil microorganisms affect C and nutrient cycling of arable soil. Meantime, soil microorganisms sensitively respond to environmental changes and/or exotic stress. Furthermore, in some instances, the changes in microbial community structure or activity can even mirror the variations in soil physical and chemical properties in response to different exotic disturbances (Lin et al., 2012). For such reason, the influences of exotic stresses on the community composition and functional aspects of soil microorganisms are frequently reported. For example, the environmental stresses caused by heavy metals generally decrease the species diversity of the soil microbial community (Chen et al., 2014b, Wang et al., 2010).

The extensive use of manufactured nanoparticles (NPs) for a variety of industrial, commercial, medical and agricultural products leads to their inevitable release into the environment, where they may potentially become environmental contaminants (Nowack, 2009, Paschoalino et al., 2010). Concomitantly, the impact of NP release on crop and agroecosystem has been focused and reported. Silver nanoparticles (AgNPs) and multi-walled carbon nanotubes (MWCNTs) are documented to decrease plant biomasses by 60% and 75%, respectively (Stampoulis et al., 2009). Our previous investigation found that iron oxide nanoparticles (FeONPs) can stimulate the growth of the mung bean (Vigna radiata) by enhancing its physiological activities (Ren et al., 2011). Soil microorganisms play important roles in plant growth and agroecosystem. Therefore, in order to comprehensively unravel the ecotoxicity of NPs, the soil microbial responses to NP pollution have also been extensively and intensively recorded. Some metal or metal oxide NPs have been found to be toxic to soil microorganisms and influence soil microbial species diversity. Kumar et al. (2012) reported that AgNPs are highly toxic to the soil microbial community, especially to the plant-associated bacteria Bradyrhizobium canariense. Our previous study indicates that FeONPs can potentially stimulate some bacterial growth and change the soil bacterial community structure (He et al., 2011b).

NPs bring changes not only in soil microbial species diversity but also in their ecological functions. AgNPs have been shown to inhibit the activities of soil dehydrogenase activity (Murata et al., 2005), phosphomonoesterase, arylsulfatase, β-d-glucosidase and leucine-aminopeptidase (Peyrot et al., 2014). FeONPs can stimulate soil enzyme activities (He et al., 2011b). Soil enzyme activities and/or ecological functions are concomitant with soil microbial metabolism. Thus, the abovementioned phenomena imply the possible influences of nanomaterials on soil microbial metabolism. Soil respiration has been conducted to evaluate the responses of soil microbial metabolism to NPs (Ge et al., 2013, Kumar et al., 2014, Yang et al., 2014a). In contrast, microcalorimetric technique can provide more detailed information on soil microbial metabolic property than soil respiration does. Indeed, microcalorimetry has been used to evaluate the effects of different pollutants on soil microbial metabolism (Herrmann et al., 2014). However, to the best of our knowledge, there is almost no microcalorimetric report regarding the effect of nanoparticles on soil microbes to date. This type of information would be of great help towards a comprehensive understanding of the effect of NPs on soil microbial ecological functions and their ecological processes. For example, soil microbial metabolic efficiency is closely connected to soil carbon conversion efficiency and soil C cycling (Barros et al., 2003).

Soil microorganisms assimilate or dissimilate soil C to drive nutrient cycles. The changes in soil microbial metabolic activity, therefore, can also imply the influence of NPs on, for instance, the soil N cycle. The rate-limiting step in microbial nitrification is the oxidation of ammonia to nitrite. Ammonia oxidation is mainly carried out by autotrophic ammonia-oxidizing microbes. However, the investigation on the influence of NPs on ammonia oxidation and its drivers in arable soil is at the infant stage. At strain level, Anjum et al. (2013) summarized the inhibitive effects of AgNPs on nitrifying bacterial growth and their activity. The condition of pure culture is quite different from that of soil matrix; only one strain rather than AOB (ammonia-oxidizing bacteria) community is focused. The information on the responses of soil ammonia-oxidizing microbial community to NPs was limited.

In view of the abovementioned information gaps, in this study, AgNPs and FeONPs (iron oxide NPs) are focused, because they are the widely used NPs in a wide range of technical applications and consumer products (Ramimoghadam et al., 2014, Yang et al., 2014b); as a consequence, they are also the NP pollutants (Nair et al., 2010). The changes of soil microbial metabolic activity in a microcosm amended with FeONPs or AgNPs were monitored by microcalorimetry. The responses of the soil nitrification process to two metal (oxide) NPs were also analyzed to evaluate the potential effect of NPs on the N cycle of arable soil. In addition, the shifts in population size of soil bacteria, eukaryotes and AOB were determined by real-time quantitative PCR (qPCR). Collectively, these findings will greatly contribute to the information regarding the assessment of NP ecotoxicity in agroecosystems.

Section snippets

Preparation and characterization of nanoparticles

The standard procedure (Feng et al., 2013) was followed to prepare two types of NPs solutions. Briefly, FeONPs were synthesized by chemical co-precipitation of Molday. Colloidal AgNPs were synthesized by reducing AgNO3 in a polyvinylpyrrolidone (PVP) solution using glucose as reducer and NaOH to accelerate the reaction.

For TEM analysis, 5 μl of each sample solution was placed onto a carbon coated copper grid. Once the solvent evaporated, TEM images were collected with JEM-2000EX (accelerating

The characteristics of two types of nanoparticles

TEM images for FeONPs and AgNPs, have been collected to characterize their physical dimensions. Very distinctive differences have been observed between them. From the inset A of Fig. 1, we can see that majority of the FeONPs were quasi-spherical, with an average diameter of 10.0 ± 2.5 nm. Comparatively, AgNPs were more spherical in shape and larger (average diameter = 20.4 ± 3.2 nm) in size (the inset B of Fig. 1). Besides their differences in physical dimensions, these two types of NPs have

Effects of two nanoparticles on soil microbial metabolic activity and efficiency

All living organisms produce heat during metabolism, which can be quantitatively and qualitatively recorded by isothermal calorimetry (Wadso, 2009). Microcalorimetry has precise control of the isothermal conditions in the thermostated bath and of the detection of thermal events in the system, without disturbance (Barros et al., 2000). Due to these advantages, microcalorimetry has recently become a powerful technique to assess exotic stress on soil microorganisms, such as heavy metals (Zhou

Acknowledgments

This work was supported by National Natural Science Foundation of China (41301267, 41371255 and 41271256), National Basic Research Program (973 Program) (2014CB954500), Foundation of the State Key Laboratory of Soil and Sustainable Agriculture (Grant No. 212000009), Jiangsu Agriculture Science and Technology Innovation Fund (cx(14)5048) and Natural Science Foundation of Jiangsu Province, China (BK20140991).

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