Arsenic and selenium in the plant-soil-human ecosystem: CREST publications during 2018–2021

Abstract

The biogeochemical transformations and biological effects of metalloids arsenic (As) and selenium (Se) in the environment has been extensively explored during the last decade, mainly owing to their ubiquitous distribution in the environment and their toxicity to biota. Here, we summarized recent research progress regarding As and Se in plant-soil-human ecosystem based on 17 publications in Critical Reviews in Environmental Science and Technology (CREST) during 2018–2021. The topics include: 1) organic As transformation in the environment and inorganic As uptake by plants (4 publications), 2) Se uptake by plants and its interactions with toxic metals in plants (6 publications), 3) As bioaccessibility and remediation of As-contaminated soils (4 publications), and 4) As research across spatial and temporal scale (3 publications). Specifically, the uptake, transformation, toxicity, bioaccessibility of As/Se in the plant-soil-human ecosystem together with pollution control measures are summarized. Future studies should focus on better understanding the cycling and biogeochemistry of As/Se in the environment, further decoding their environmental effects from the One Health perspective.

Keywords:

• Remediation
• uptake
• transformation
• toxicity
• transporters
• bioaccessibility

1. Introduction

Arsenic (As) and selenium (Se) are both metalloids, which are ubiquitous and mainly exist as inorganic oxyanions in soils (Ali et al., 2021). As a carcinogen, As is highly toxic to all biota. Unlike As, Se is an essential micronutrient for humans and animals, and a beneficial element to plants (Li et al., 2021; Rizwan et al., 2021). As such, it is important to understand the biogeochemical processes controlling their transformations in soils and their uptake by plants, which helps to reduce plant As uptake while enhancing plant Se uptake.

The biological functions of As and Se in the environment are determined not only by their concentration, but also by their speciation (Ali et al., 2021; Li et al., 2020). For As, common species in the environment include both inorganic such as arsenite (AsIII) and arsenate (AsV), and organic such as monomethylarsonous acid, dimethylarsinous acid, arsenosugar, arsenolipid, arsenobetaine and methylated thioarsenate (Chen et al., 2020). Similarly, for Se, there are inorganic (selenate-SeVI and selenite-SeIV) and organic (selenocysteine and selenomethionine) species (Kushwaha et al., 2021). In soils, inorganic species are dominant for As (AsV and AsIII) and Se (SeVI and SeIV), which can be taken up by microbes and plants.

Besides natural sources of As and Se in the environment, increased human activities including mining and smelting, coal burning and pesticide application in the past have accelerated their transfer to the environment, causing toxicity to biota (Kumarathilaka et al., 2020; Kushwaha et al., 2021). While trying to understand the toxic effects of As and Se, we also use the beneficial effect of Se. This editorial summarizes recent research progress focusing on As and Se based on CREST publications during 2018–2021. Among the 17 publications, 11 publications focus on As and 5 publications focus on Se, with 1 publication on As-Se interaction (Figure 1). They cover a wide range of subjects, including their uptake, transformation, toxicity, bioaccessibility, and interactions in the plant-soil-human ecosystem.

Figure 1. Graphic description of the topics covered by the 17 publications in CREST.

2. Organic As transformation in the environment and inorganic As uptake by plants

Besides inorganic As species, organoarsenicals are widely distributed in the environment, which are mainly from anthropogenic sources. Two recent reviews focused on their occurrence and fate in the environment, as well as their metabolisms, toxicology and biological functions in microbes, plants and/or humans. Chen et al. (2020) summarized the occurrence, toxicology and biotransformation of two types of organoarsenicals (aliphatic and aromatic) in the environment. Further, it is important to understand the environmental fates and metabolic pathways, develop advanced analytical techniques, and identify exposure biomarkers of organoarsenicals. Xue et al. (2021) adopted a different classification method for organoarsenicals, i.e., water-soluble and lipid-soluble. They discussed their environmental occurrence, biosynthesis, degradation, toxicity and potential biological functions. Given our poor understanding regarding the cycling and biogeochemistry of organoarsenicals in the environment, collaborative research from different disciplines is critical.

Over time, organoarsenicals in soils are eventually converted to inorganic species, which are taken up by plants. However, arsenic shows no physiological function in plants, as such it often causes adverse effects. While AsV is mostly taken up by phosphate transporters in plants, AsIII is taken up by aquaporins. Tang and Zhao (2021) summarized the roles of various transporters in the uptake, transport, accumulation and detoxification of different As species including AsV and AsIII, and their regulation mechanisms in plants including As-hyperaccumulator Pteris vittata. While the review by Tang and Zhao (2021) is broad including different As species in soils, Deng et al. (2020) focuses on aquaporin-mediated AsIII uptake, transport, and accumulation in microbes and plants. Based on the functions and expression patterns, these transporters can be employed to genetically-engineer crops of low-As accumulation to ensure food safety or plants of high-As accumulation for phytoremediation (Deng et al., 2020; Tang & Zhao, 2021).

3. Selenium uptake by plants and its interactions with toxic metals in plants

Unlike As, Se is a beneficial element for plants, so it is important to understand its biogeochemical transformation in soils as well as to develop methods to improve Se nutrition in plants. Dinh et al. (2019) evaluated the biogeochemical transformation of Se in the soil-plant system and discussed potential methods to control Se bioavailability in soils. They suggested that diffusive gradients in thin-films technique can be used to evaluate Se phytoavailability in soils. Further, application of Se, N, P and S fertilizers and Se-enriched organic materials is effective in improving plant Se nutrition. Besides, Chauhan et al. (2019) examined the uptake and metabolism of Se in plants, mostly focusing on the beneficial functions of Se-containing metabolites. Kushwaha et al. (2021) reviewed the roles of Se in soil-microbe-plant systems, mainly focusing on its speciation, bioavailability, toxicity, and detoxification mechanisms. To improve Se nutrition in plants, it is important to select proper plant varieties, fertilizer application strategy, and symbiotic bacteria (Chauhan et al., 2019; Dinh et al., 2019; Kushwaha et al., 2021).

As a beneficial element, Se can counteract stresses from toxic metals including As, Cd, Sb and Hg in plants. Several mechanisms are proposed including inhibition of metal uptake and translocation, decrease in oxidative stress, improvement of plant growth, and reduction in metal toxicity via chelation, compartmentalization and changes in metal species. Rizwan et al. (2021) showed the optimal Se doses to decrease toxicity of As, Cd, Sb and Hg in plants and illustrated how they function in plants and rhizosphere. Ali et al. (2021) discussed the As and Se interactions in soil-plant system and the associated toxicity mechanisms in plants, animals and humans. Dang et al. (2019) explored the interactions between Se and methylmercury, and illustrated the role of Se in reducing methylmercury bioaccumulation in plants and deposit-feeders.

4. Arsenic bioaccessibility and remediation of As-contaminated soils

Important pathways for human exposure to As include incidental ingestion of As-contaminated soils as well as consumption of As-contaminated rice. Animal models including swine and mouse have been developed to measure the As bioavailability to humans. However, they are expensive and time-consuming. As such, in vitro assays using simulated human gastrointestinal fluids have been used to evaluate bioaccessible As, i.e., extractable As from soils (Li et al., 2020). Based on 107 soils pooled from different studies with paired bioavailability and bioaccessibility values, the SBRC method (Solubility Bioaccessibility Research Consortium) is the best assay to determine As bioaccessibility in As-contaminated soils.

Besides ingestion of As-contaminated soils, human exposure to As through rice consumption is of health concern, especially in Asian countries, as such much efforts have focused on measures to reduce their exposure. Kumarathilaka et al. (2020) reviewed various approaches to lower As accumulation in rice. These include water management, application of Si fertilizer, Fe/Mn (hydr)oxides and biochar, bioremediation using As-hyperaccumulator P. vittata and As-tolerant microbes, and screening of low-As rice cultivars, which can help to decrease As level in rice grains.

Given the widespread of As-contaminated sites in the environment, it is important to develop cost-effective technologies to reduce its adverse impact on plant-soil-human ecosystem. As such, remediation technologies including sorption, stabilization, and encapsulation have been developed. Yu et al. (2018) reported rare-earth based sorbents including lanthanum/cerium/yttrium (hydr)oxides for As sorption. They also summarized their chemical properties and sorption performance. Mining activities are important sources for As-contamination in soils. To reduce As toxicity, Álvarez-Ayuso (2021) compared various approaches to stabilize and encapsulate As-bearing mine waste. Further, they also determined factors affecting the effectiveness of various treatment technologies.

5. Arsenic research across spatial and temporal scales

Arsenic has long been used in medicinal and industrial fields, but it is raised as a global concern only recently. To better understand the role of As in our society as a double-edged sword, it is necessary to know the progresses of As research regarding its benefits and risks over the years. Based on a scientometric analysis, Li et al. (2021) summarized the research progresses and identified the research trends on As during the past 120 years. Three milestones are highlighted regarding its toxic and beneficial effects: 1) the wide applications of As in semiconductor doping and agricultural pesticides in 1960s, 2) arsenic poisoning incidents in West Bengal and Bangladesh in the early 1990s, and 3) the application of arsenic trioxide to treat acute promyelocytic leukemia in the late 1990s.

Arsenic contamination in soils and groundwater is of global concern. While most efforts focus on anthropogenic sources, groundwater contamination by As from geological sources was reported by Wang et al. (2021). They demonstrated the hydrogeological patterns of As, which often co-exists with anions F and I. Particularly, they proposed four basic genetic types of geologically-contaminated groundwater, and provided a theoretical framework to understand the complex genetic mechanisms and predicting their spatial and temporal distribution (Wang et al., 2021). Bundschuh et al. (2021) summarized information regarding As pollution in 20 Latin American countries. They focused on the developments during the past 10 years and provided a country-specific overview of the occurrence and impacts of As exposure in different environmental matrixes including soil, water and sediment.

6. Summary

In this special issue, 17 publications in CREST during 2018–2021 focusing on As and Se were selected. The sources, transformation and biological effects of organoarsenicals (Chen et al. 2020; Xue et al. 2021), the molecular mechanisms of As uptake by microbes and plants (Deng et al., 2020; Tang & Zhao, 2021), the biogeochemical processes of Se in soil-microbe-plant system (Chauhan et al., 2019; Dinh et al., 2019; Kushwaha et al., 2021), and the interactions between Se and toxic metals (Ali et al., 2021; Dang et al., 2019; Rizwan et al., 2021) were covered. Besides, human exposure assessment and control of As in soils and rice (Kumarathilaka et al. 2020; Li et al. 2020), and remediation of As-contaminated water and mine waste via sorption and stabilization/encapsulation processes were reviewed (Álvarez-Ayuso, 2021; Yu et al., 2018). Further, the 120 years of As research history (Li et al., 2021) and As contamination in groundwater and Latin America were reported (Bundschuh et al., 2021; Wang et al., 2021).

Based on the 17 publications, the following research areas need further attention: 1) analytical methodologies to better understand the cycling and bioavailability of As/Se species in the environment, especially the organic species; 2) dynamic cycling of As and Se at regional and global scale to help formulate better regulations to reduce As toxicity; 3) biotransformation of As and Se in plants and associated mechanisms to improve crop yield and food safety; and 4) understanding the interactions between As and Se in plants and humans to help reduce their adverse effects on biota. Further, breeding of As-poor and Se-rich crops has attracted much attention lately. In short, we need to develop integrated approaches to reduce the risk of As/Se and harness their benefits from One Health perspective by linking soil-plant-microbe-animal-human in the environment.

Acknowledgements

This work was supported in part by the National Natural Science Foundation of China (21637002) and the Fundamental Research Funds for the Central Universities (2021QNA6004). The authors would like to thank Drs. Jörg Rinklebe, Robert Letcher and Yong Sik Ok for their constructive comments to improve this virtual special issue.

Disclosure statement

No potential conflict of interest was reported by the authors.