Chromium biogeochemical behaviour in soil-plant systems and remediation strategies: A critical review

Highlights

• The biogeochemical behaviour of Cr in soil-plant systems and remediation strategies are summarised.

• Soil properties and microorganisms largely control the Cr geochemical behaviour.

• The migration and transformation of Cr in the soil-plant systems are highlighted.

• Plants have evolved well-organised antioxidant mechanisms to cope with Cr toxicity.

• Organic and inorganic reductants can effectively reduce Cr(VI) to the less toxic Cr(III).

Abstract

Chromium (Cr) is a toxic heavy metal that is heavily discharged into the soil environment due to its widespread use and mining. High Cr levels may pose toxic hazards to plants, animals and humans, and thus have attracted global attention. Recently, much progress has been made in elucidating the mechanisms of Cr uptake, transport and accumulation in soil-plant systems, aiming to reduce the toxicity and ecological risk of Cr in soil; however, these topics have not been critically reviewed and summarised to date. Accordingly, based on available data—especially from the last five years (2017–2021)—this review traces a plausible link among Cr sources, levels, chemical forms, and phytoavailability in soil; Cr accumulation and translocation in plants; and Cr phytotoxicity and detoxification in plants. Additionally, given the toxicity and hazard posed by Cr(VI) in soils and the application of reductant materials to reduce Cr(VI) to Cr(III) for the remediation of Cr(VI)-contaminated soils, the reduction and immobilisation mechanisms by organic and inorganic reductants are summarised. Finally, some priority research challenges concerning the biogeochemical behaviour of Cr in soil-plant systems are highlighted, as well as the environmental impacts resulting from the application of reductive materials and potential research prospects.

Introduction

Chromium (Cr) is the 7th most abundant chemical element in the Earth’s crust and has been extensively mined in South Africa, Kazakhstan, and India (USGS, 1996–2021; Shahid et al., 2017). As a serious environmental contaminant, Cr is released into soil through geological processes and anthropogenic activities (Rajapaksha et al., 2013, Coetzee et al., 2018). Approximately 1.29 × 10⁵ t of Cr is released annually in the global environment, most of which has accumulated in soil and thus caused serious Cr pollution (Coetzee et al., 2018). Although Cr(III) is an essential element for humans and has been associated with the metabolism of carbohydrates, lipids and proteins, public health concerns focus on Cr toxicity (Pavesi and Moreira, 2020, Zhao et al., 2020), with excessive exposure and ingestion having negative effects on human organs (e.g., skin, lungs, kidneys and liver). Cr(VI), which is ranked as 100 times more toxic than Cr(III) in terms of its toxicological profile, is classified as the No.1 carcinogen by inhalation in humans (Cheng et al., 2014, EFSA (European Food Safety Authority), 2014, Pavesi and Moreira, 2020, Zhao et al., 2020). However, human exposure to Cr is mainly derived from soil-crop systems because Cr is easily integrated into the food chain (EFSA, 2014; Christou et al., 2021). Considering these potential risks to humans and plants, Cr contamination in soil has attracted worldwide attention (Zhang et al., 2016, Hernandez et al., 2019). Therefore, a detailed understanding of the biogeochemical behaviour of Cr and better environment monitoring are important to assess the potential risk of Cr to ecosystems, particularly soil-plant systems.

As a redox-sensitive metal, Cr does not exist as a pure metal and is easily converted from one oxidation state to another (Wei et al., 2020). Cr is generally present in compounds in several valence states ranging from 0 to VI. Among these, Cr(III) and Cr(VI) are the most stable and common oxidation states in the environment (Silva et al., 2016, Xia et al., 2019a), both of which can be taken up by plants (Singh et al., 2013). Excessive Cr in soil, especially Cr(VI), can inhibit plant growth and even seriously threaten the soil ecosystem (Dazy et al., 2008). Cr(VI) is the most toxic form of Cr to plants, animals, and humans (Medda and Mondal, 2017, Pavesi and Moreira, 2020). In contrast, Cr(III) is an essential trace element for maintaining the metabolic activity of humans and animals and has lower toxicity to organisms. Cr has no identified biological role in plants (Danish et al., 2019). The biogeochemical behaviour of Cr in soil-plant systems is controlled by multiple factors, including the soil properties—such as texture, pH, Eh, OM, Fe and Mn oxides, sulphide ions, soil moisture content and microbial activity, and plant physiology—such as plant type, root surface area, rate of root exudation and rate of transpiration (Banks et al., 2006, Dazy et al., 2008, Dong et al., 2018, Xiao et al., 2021). Given that Cr is a non-essential element for plants, they do not have specific transporters and channels for Cr uptake (Adhikari et al., 2020). Therefore, Cr is accumulated by plants through specific carriers of the essential ions for plant metabolism, such as Fe for Cr(III), and sulphate and phosphate for Cr(VI) (Ding et al., 2019, Xu et al., 2021).

Although Cr has been suggested as being capable of promoting the growth of some plants at lower concentrations (< 10 mg/L) (Saddiqe et al., 2015, Christou et al., 2021), it is extremely toxic at higher concentrations and can inhibit photosynthesis, trigger lipid peroxidation and ROS production in plants, and may lead to considerable damage or even death (Danish et al., 2019, Adhikari et al., 2020). As sessile organisms, plants under Cr stress have evolved elaborate mechanisms for minimising Cr uptake or transportation and for detoxification through compartmentalisation, modification or PCs (Gong et al., 2020). These defensive mechanisms include the scavenging of ROS by some antioxidant enzymes and non-enzymatic scavengers to reduce Cr toxicity (Adrees et al., 2015, Ma et al., 2016, Akyol et al., 2020, Sharma et al., 2020, Usman et al., 2020). Thus, the effects of Cr-induced toxicity on soil-plant systems and related detoxification mechanisms of plants need to be comprehensively analysed.

As the most dangerous form of Cr in the environment, Cr(VI) is not only more easily taken up by plants and affects the crop yield and quality but also has harmful effects on humans and animals due to its carcinogenicity, mutagenicity and genotoxicity (Aharchaou et al., 2017, Hernandez et al., 2019, Pavesi and Moreira, 2020, Zhao et al., 2020). Therefore, the remediation of Cr(VI)-contaminated soil is imperative. Considering the lower toxicity and higher stability of Cr(III), chemical reduction is the most commonly used approach for the remediation of Cr(VI)-contaminated soils (Li et al., 2019, Bashir et al., 2020). Organic or inorganic electron donors reduce Cr(VI) to Cr(III), which then exists as insoluble Cr(III) hydroxides (Li et al., 2020a, Li et al., 2020b, Li et al., 2017, Liu et al., 2018). Although the chemical reduction approach cannot remove or extract Cr from soils, it can significantly reduce the concentration and mobility of Cr(VI) in soils without generating contaminating by-products; this can effectively reduce the risk of Cr(VI) in soil-plant systems (Liu et al., 2018, Guan et al., 2019).

This review summarises current knowledge on Cr in soil-plant systems, particularly on the mechanisms of Cr migration, accumulation, toxicity and detoxification. Considering the harmful effects of Cr(VI) in soil on plants and humans and the advantages of in-situ reduction remediation over other conventional techniques, the mechanisms of reduction and immobilisation of Cr(VI) by organic amendments and inorganic reductants is also reviewed. Finally, research gaps in the biogeochemical behaviour of Cr in soil-plant systems and the challenges in the use of in-situ remediation materials for Cr(VI)-contaminated soils are discussed to determine future research directions and needs.