TiO₂ nanoparticles in a biosolid-amended soil and their implication in soil nutrients, microorganisms and Pisum sativum nutrition

Highlights

• TiO₂ treatments in Bs-amended soils depleted mineral nutrients availability.

• A dose-dependent reduction of bacterial biodiversity was observed in treated soils.

• A general imbalance of pea mineral nutrition was observed in TiO₂ treated soils.

• No evident effect attributed to a particular crystalline phase was observed.

• The mix of anatase and rutile seems to be more deleterious in the soil-plant system.

Abstract

The wide use of nanoparticles (NPs), gives concern about their possible negative implications in the environment and living organisms. In particular, titanium dioxide (TiO₂) NPs are accumulated in biosolids (Bs) coming from wastewater treatment plants, which in turn are used as farm soil amendments and are becoming an important way of NPs entrance in the terrestrial ecosystems. In this study, to simulate a low and cumulative load of TiO₂ NPs, 80 and 800 mg TiO₂ per Kg of soil were spiked in the Bs prior to its addition to soil. The effects of different crystal phases of TiO₂ NPs (pure anatase and pure rutile or their mixture) and their non-coated bulk counterparts (larger particles) on the availability of mineral nutrients and on the status of the bacterial communities together with the nutritional status of Pisum sativum L. plants were evaluated. Results showed the reduction, to different extents, on the availability of important soil mineral nutrients (e.g. Mn 65%, Fe 20%, P 27%, averagely), in some cases size- (e.g. P) and dose-dependent. Bacterial biodiversity was also affected by the presence of high TiO₂ dose in soil. The mineral nutrition of pea plants was also altered, showing the main reduction in Mn (80% in the roots and 50% in the shoots), K, Zn, P (respectively, 80, 40, and 35% in the roots), and an increase of N in the shoots, with possible consequences on the quality of the crop. The present study gives new integrated data on the effects of TiO₂ NPs in the soil-plant system, on the soil health and on the nutritional quality of crops, rising new implications for future policies and human health.

Introduction

Engineered nanoparticles (ENPs) find numerous growing applications to a broad range of industrial sectors such as cosmetics, coatings and paints, plastics, foods and beverages, pharmaceutics, textiles, environment, electronics, transports, etc. However, the ambiguous behavior of ENPs, i.e., benefits vs. negative implications for the society, environment and economy systems, gives concern about their increasing release and effects on the environment (Tolaymat et al., 2017).

A survey from companies producing or using ENPs revealed TiO₂ as the most produced ENP with up to 50,000 t/year of worldwide production (Kunhikrishnan et al., 2015). Modeling studies providing predictions for the TiO₂ nanoparticles (NPs) production, application and release, indicated them among the most used NPs and the ones with far higher concentrations in all environmental systems (Sun et al., 2014). Significant flows of TiO₂ NPs from wastewater treatment plants (WWTP) were predicted to be discharged to sewers, accumulated in biosolids (Bs) and wastewater effluents, which will end up in farm soils (8900 t/year), landfills (7600 t/year) or in the water systems (3600 t/year) (Garner et al., 2017; Song et al., 2017). Soil ecosystems (natural, farm, urban, industrial and landfill soils) are considered important sinks for the ENPs. In particular, farm soils were subjected to the application of Bs and sewage sludge as fertilizers, becoming a significant route of entry in the terrestrial environment (Judy and Bertsch, 2014). Moreover, the uptake of NPs by edible plants could represent a way of transfer into the food chain (Pošćić et al., 2016; Tan et al., 2018).

The production of wastewater sludge and Bs in the EU was estimated at 10 million t (dry solids) in 2008, 44% of which recycled to land; by 2020, it is expected to reach a total production of 13 million t (EC Overview Report, 2008). The use of Bs in agricultural soils is currently identified as one of the best environmental management practice, due to the supply of organic matter and nutrients to the soil-plant system. The EU Directive 86/278/EEC seeks to boost its use in agriculture and its quality control to prevent harmful effects to humans and environment. Accordingly, Bs and sewage sludge designated to farm soils are subject to concentration limits for potential toxic metals. Some countries have more updated legislation, which also considers organic contaminants and pathogenic indicator microorganisms. However, no restrictions are defined for the presence of ENPs, although increasing concern regarding their accumulation and ecotoxicity in long-term land application has been found (Chen et al., 2017; Yang et al., 2014).

The effects of ENPs on plants depend on a series of factors (NPs type, plant species, soil properties, etc.). In particular, the soil organic matter could influence the mobility and the bioavailability of ENPs by changing their original properties such as aggregation state, surface charge affinity, Van der Waals force and zeta potential (Pošćić et al., 2016; Tan et al., 2018; Tassi et al., 2012). Although several studies investigated the accumulation and effects of TiO₂ NPs on different plant species (Ruffini Castiglione et al., 2014, 2016; Wang et al., 2019), the ones conducted in real farm soils (Giorgetti et al., 2019; Pošćić et al., 2016; Tassi et al., 2016) are yet not conclusive. The evaluation of NPs’ impact on soil microbial communities (Chen et al., 2017; Dimpka et al., 2015; Simonin et al., 2015) or on crop nutritional quality (Dimpka et al., 2015; Pošćić et al., 2016; Rui et al., 2018; Wang et al., 2019) are gaining increasing interest in view of the possible uses of NPs of micronutrients (e.g. CuO, ZnO NPs) as fertilizers or the use of TiO₂ NPs to face up with problems of adverse environmental conditions (Ji et al., 2017). Moreover, recent studies sustain that TiO₂ crystalline phases, anatase and rutile, distinctly affect physiological, biochemical and genotoxic plant parameters (Tan et al., 2018). Literature data reported that anatase in plants was more toxic than rutile: Silva et al. (2016) revealed anatase toxicity higher than the mixture of anatase and rutile on wheat seed germination and membrane permeability; Giorgetti et al. (2019) showed that anatase on its own or mixed with rutile induced higher oxidative stress and ultrastructural damages in the roots of pea plants than pure rutile; Cai et al. (2017) showed a preferential translocation of anatase from the roots to the upper part of rice plants in the presence of a mixture of anatase and rutile, while a preferential uptake of rutile was demonstrated in cucumber plants (Servin et al., 2012). Therefore, more information about the toxicity of the different crystalline phases and their entry into food crops are important and necessary, in particular, for NPs coming from Bs amended farm soil.

In this study, it was hypothesized that different crystalline forms and dimension of TiO₂ particles may have different and specific influence on the soil-plant system in terms of mineral nutrients availability and soil microbial community, as well as on the nutritional status of plants. To assess these hypotheses, this work evaluated the effects of TiO₂ as anatase and rutile NPs (separately and mixed together) and as bulk particles on the availability of mineral nutrients in a Bs-amended farm soil, on the disturbance of associated soil bacterial community and on the mineral nutrition of the crop plant Pisum sativum L. Two concentrations (80 and 800 mg TiO₂ particles per Kg of soil) were chosen to represent, respectively, a low and a cumulative load of TiO₂ NPs through Bs amendment in farm soils, in accordance to Sun et al. (2014).