Arsenic in rice straw phytoliths: Encapsulation and release properties
Introduction
The world rice production currently produces approximately 500 million tonnes of rice per annum that feeds half of the world population (Earth Security Group, 2019), but it also creates at least the same amount of straw. Recycling the soil through incorporation or on-site open burning is still the most common practice because it is the easiest way to handle straw after harvesting. However, rice straw is also encouraged to be utilized for various purposes, e.g., fodder (Aquino et al., 2020), construction materials (Ghaffar, 2017), composting (Mahmoud et al., 2009), growing media (Feng et al., 2020) or biofuels (Satlewal et al., 2018). The development of new rice straw applications is important to create other additional value for the rice production sector, but it requires more in-depth insights into the nature and traits of straw, particularly composition or structure at the microscale. Generally, rice straw is composed of lignocellulose, silica, nutrients and other “impurities”, e.g., heavy metals (Nguyen et al., 2019), radioactive (Ohmori et al., 2016) and persistent organic matter (Zhang et al., 2016). However, much less effort has been focused on discovering impurities in straw, and this fact could be one of the challenges to broadening the utilization of straw.
Heavy metals or metalloids, particularly arsenic (As), are present in the soil as they are a part of soil materials (Igarashi et al., 2008) or can be supplemented through various anthropogenic activities, e.g., irrigation (Farooq et al., 2019), fertilization (Campos, 2002) or application of pesticides and herbicides (Saxe et al., 1964; Quazi et al., 2011), and their availability leads to possible uptake by plants via various active or passive mechanisms (Awasthi et al., 2017; Chen et al., 2017). To date, the assimilation of As in rice has been intensively studied, as it causes potential risks to human health (Ng et al., 2003; Meharg, 2004; Biswas et al., 2020). Several transporters that are responsible for phosphorus (P) and silicon (Si) uptake, such as Pht, Lsi1, Lsi2, and Lsi6, are involved in transporting As from soil to roots and shoots (Chen et al., 2017). This implies that As is likely assimilated passively, and its occurrence in rice plant organs is a consequence of unintended deposition/localization. Using the same transporters, Si, P, and As share the transport route in plant organs. However, little is known about the interaction of As with P, particularly with Si, which is ubiquitous and comprises up to 15% of rice plants (Epstein, 2001; Guntzer et al., 2012).
The siliceous structure is commonly found within plant tissues or organs in many Si hyperaccumulators, e.g., rice (Nguyen et al., 2014), wheat (Meunier et al., 2017), sugarcane (Parr et al., 2009), grass (Bremond et al., 2008), and bamboo (Parr et al., 2010). This structure is also named the ‘phytolith’ and is formed through the precipitation of Si on the cell wall or in inter- and intracellular space when the Si concentration in the transport sap or cytoplasm is oversaturated. As a traditional research material of phytology or archaeology (Ryan, 2014), however, phytoliths have been more intensively studied because of their agronomical or environmental benefits (Song et al., 2016). The structure of phytoliths has been more clearly revealed as a platform to encapsulate organic matter (Parr and Sullivan, 2005; Li et al., 2013; Huang et al., 2014), nutrients (Nguyen et al., 2015; Trinh et al., 2017) and other toxic components (Nguyen et al., 2019; Tran et al., 2019; Delplace et al., 2020). As described in these studies, it is likely that the matter is physically held within the porous system of the phytolith structure, while the role of the chemical association is poorly understood. Because As is a chemical analogue of Si, it is hypothesized that As can chemically associate with Si in the phytolith structure. If so, the fate of As could in turn depend on both the dissolution properties of the phytolith (at the molecular scale) and the cycle of straw-derived phytoliths (at the field scale).
The recycling of phytolith silica provides a fast-reacting Si source for soil, and this has been highlighted as a “silver bullet” for maintaining crop productivity (Meena et al., 2014) or mitigating As uptake (Meharg and Meharg, 2015; Tran et al., 2020). This means that phytolith-associated substances such as As can also be recycled to the soil. To warrant that this practice will not result in an enrichment of the “fast-reacting” As pool in paddy soils or an increase in the exposure of As to human health, the phytolith and its encapsulated As need additional considerations. In this study, we performed a survey on the accumulation level of As in straw in the Red River Delta (Vietnam). Tainted-As straw was used to evaluate the possible encapsulation of As in straw phytoliths. Despite many efforts to enforce worldwide bans, on-site burning still takes place in many cultivation regions, as this is an “easy-to-go” practice, and rice growers have little incentive to stop. Furthermore, worldwide bans of on-site open burning of rice straw waste during rice production have forced rice growers to find alternative straw-disposal strategies, including straw removal from paddy ecosystems. This could inadvertently lead to increased As levels in rice due to the loss of a fast-reacting source of silicon in straw, which is vital to combat As accumulation in rice (Nguyen, 2020). However, burning has also been known as a route to spread out As into the environment (Wang et al., 2020). Hence, addressing the on-site open burning issue needs more insights into the burning process and the resulting fate of As in straw. On the one hand, burning decomposes straw's organic phases and, on the other hand, transforms silica phytoliths (Trinh et al., 2017; Mai et al., 2019). Here, we examined the micromorphology and release rate of As for phytolith samples obtained from controlled pyrolysis in a temperature range from 300 to 900 °C. These thermal treatments reflect possible exothermic changes in which the fate of As in relation to silica transformation can be elucidated. Underlying mechanisms for encapsulating or releasing As from phytoliths are the premise of developing mitigation strategies to reduce As exposure and its potential risks.
Section snippets
Study area and sampling
The Red River Delta (RRD) is a lowland area of the Red River basin formed from fluvial deposits of the Red River and Thai Binh River systems in northern Vietnam. Contamination of soil and groundwater by As has been identified as one of the threats to rice cultivation in this region (van Geen et al., 2013; Tran et al., 2020). With an area of 15,000 km2, the RRD is the third largest delta in Southeast Asia and produces up to 10 million tonnes of rice per annum and creates approximately the same
Rice straw as sink and source of arsenic
Rice is an As-philic species; thus, rice straw can be a sink of As. This sink is built up seasonally or annually and becomes a new and mobile source of As when the straw is upcycled or utilized for other purposes. While enrichment of As in soil resulting in increased availability of As has been reported in many rice-growing deltas worldwide, it should be warned that this sink continues to grow up. The RRD can likely exemplify deltas that suffer from the enrichment of As. The concentrations of
Discussion
The gradual release of As accompanying the dissolution of phytoliths, as revealed in Fig. 4, Fig. 5, could be an initial clue of the encapsulation process of As mediated by the precipitation of Si to form phytoliths during rice growth or the transformation of phytoliths under thermal treatment (e.g., on-site open burning). It can be hypothesized that the encapsulation of As into phytolith structure during the growth of plants involves both physical encapsulation and chemical association.
Conclusion
Rice straw in the RRD contains up to ~12 mg kg−1 As. Although the concentrations of straw As are relatively low, it is still worthwhile to highlight rice straw as a sink and source of As that needs to be taken into account, especially in the context that we need to expand rice cultivation to meet the future demand and straw is utilized for various purposes. Straw As can be readily released and the extent to which it contaminates the environment or affects human health is largely dependent on
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
X-ray tomographic microscopy was performed by Julie Fife at the TOMCAT beamline of the synchrotron facility of the Paul Scherrer Institute, Villigen, Switzerland. Great help of Sarah B. Cichy for morphological characterization of phytoliths from the tomographic dataset is acknowledged. X-ray photoelectron spectroscopy was performed at the Kyushu Institute of Technology, Japan and we gratefully acknowledge Dr. Toshiki Tsubota for his support.
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