Mitigating toxic metals contamination in foods: Bridging knowledge gaps for addressing food safety

Abstract

Background:

Reducing exposure to harmful substances in food is highly desired, especially for infants, young children, and pregnant women. A workshop focused on understanding and reducing toxic metal contamination in food was conducted involving leading scientists, educators, practitioners, and key stakeholders in conjunction with the USDA National Institute of Food and Agriculture.

Scope and approach:

The goal of this review and the workshop was to advance the current knowledge of major toxic metals concerning food safety, viz. arsenic (As), lead (Pb), cadmium (Cd), mercury (Hg), and chromium (Cr), preventive measures, identify critical knowledge gaps, and the need for research, extension, and education. Being a part of the “Closer to Zero (C2Z)” initiative of the USDA, FDA, and other federal agencies, the workshop adopted a “One Health” approach to mitigate dietary exposure and environmental pollution of hazardous elements.

Key findings and conclusions:

The experts discussed the accumulation of toxic metals in food crops and drinking water in relation to soil biogeochemistry, plant uptake, and multidisciplinary factors such as food processing, detection, regulatory standards, etc. To forward food safety, this workshop critically examined toxic metals contamination, exposure and toxicity along the farm-to-fork-to-human continuum, research gaps, prevailing regulations, and sustainable remediation approaches, and offered significant recommendations. This review paper provides perspective on key findings of the workshop relative to addressing this important aspect of food safety, emphasizing interdisciplinary research that can effectively investigate and understand the complex and dynamic relationships between soil biogeochemistry, the microbiome, plant tolerance and accumulation strategies, uniform standards for acceptable and safe toxic element levels in food and water, and raising public awareness. This article also provides a foundation for decision-making regarding toxic metal fate and effects, including risk management strategies, in the face of modern industrialization and a changing climate.

1. Introduction

Heavy metals or metalloids (HMs) are significant environmental pollutants, and their toxicity and carcinogenicity have emerged as an alarming threat to human health globally (Jallad, 2015). Due to their high and non-threshold toxicity, toxic elements such as arsenic (As), cadmium (Cd), lead (Pb), mercury (Hg), and chromium (Cr) are among the most hazardous toxic substances of public health concern (Liu, Zhang, et al., 2020; Niede and Benbi, 2022). Inorganic As has been classified as a serious threat to human health by the Department of Health and Human Services’ Agency for Toxic Substances and Disease Registry (ATSDR), followed by Pb, Hg, and Cd. HMs are released naturally into the terrestrial and aquatic environment through geogenic leaching from enriched rocks and sediments, volcanic eruptions, weathering of rocks, and forest fires, among other processes (Tchounwou et al., 2012). However, various anthropogenic practices contribute to the biogeochemical cycling of HMs and the deposition of much more toxic and mobile forms of these pollutants. Increased incineration of fossil fuels, mining of ores, modern industrialization, use of HM-based pesticides, herbicides, fertilizers, excessive irrigation with contaminated groundwater, and refuse dumping have reportedly increased the HM content in air, soil, and drinking water (Briffa et al., 2020; Cullen & McAlister, 2017; Upadhyay et al., 2019). These non-degradable toxic elements persist in the environment and exhibit chronic contamination as they can accumulate in the body and food chain over time (Das et al., 2004; Upadhyay et al., 2019).

Indeed, As, Cd, Cr, Pb, and Hg are systemic toxicants that can induce damage in multiple organs, even at low exposures (Bilge et al., 2021). A low concentration of As (6.0 mg/L), Hg (0.03 mg/L), and Pb (0.10 mg/L) in the blood can produce adverse health hazards such as cancer and damage to vital body organs in children below six years of age (Engwa et al., 2019; Kalish et al., 2014; Téllez-Rojo et al., 2006; Tsuji et al., 2015). Reports suggest that exposure to toxic elements is associated with a permanent decrease in IQ, hindered brain and neurological development in infants, and increased risk of antisocial behavior in children (Bair, 2022; Bansal, 2023). Importantly, high-dose HM exposure may cause more severe damage (Johri et al., 2010). Gastrointestinal and cardiovascular dysfunction; kidney failure; nervous system disorders; respiratory and vascular damage; skin lesions; birth defects; and lung, liver, and kidney cancers are some of the acute and chronic complications associated with exposure to toxic elements (Abdul et al., 2015; Balali-Mood et al., 2021; Brown & Ross, 2002). In addition to dose, HM toxicity depends on several other factors, such as route of exposure, chemical species, age, gender, genetics, and nutritional status of the exposed individuals. A schematic representation of the source of contamination of toxic elements, their uptake and accumulation in plants, and associated health risks to consumers is presented in Fig. 1.

Fig. 1.

Schematic showing the source of contamination of toxic elements, their uptake and accumulation in plants, and associated health risks to consumers.

There are global reports of high concentrations of As, Hg, Cd, Cr, Pb, and other hazardous elements in soil and drinking water. Wetland soils and sediments, in particular, have been reported to have a high content of HMs, including Pb, As, Cd, and Hg (Meharg & Rahman, 2003). High-pH aquifers in countries like Bangladesh, India, China, Chile, and the USA have been contaminated with As, resulting in extensive contamination of drinking water (Podgorski et al., 2017; Rodríguez-Lado et al., 2013). It has been estimated that almost one billion people are exposed to As through food, and more than 200 million people are negatively impacted by As exposure in drinking water, with the situation being most dire in West Bengal (India) and Bangladesh (Stanton et al., 2015; Takahashi et al., 2004; Uppal et al., 2019). The uptake of toxic elements by crop plants plays a vital role in transferring these xenobiotics into the food chain (Meharg & Rahman, 2003). Numerous studies have shown that crops grown on contaminated soil or irrigated with polluted water can accumulate high levels of As and other toxic metals in roots, shoots, and grains (Bianucci et al., 2020; Das et al., 2004; Meharg & Rahman, 2003). However, these metals (loids) are phytotoxic at higher levels and can negatively affect plant growth, development, grain quality, and yield, leading to significant agronomic loss (Pathare et al., 2013).

Rice, a major wetland crop, is known to accumulate comparatively higher levels of As and Cd in the edible grains (Abedin et al., 2002; Awasthi et al., 2017; Wang, Huang, et al., 2019; Williams et al., 2005). Wheat, barley, and maize are other crops responsible for As exposure among the human population (Bianucci et al., 2020). In Madeira, an evaluation of HM in different cereal species reported that oats contained the highest Cd levels of 0.307 mg/kg, followed by rye 0.237 mg/kg in rye. Rice was marked by the highest Hg accumulation of 0.0013 mg/kg, with 0.001 mg/kg of Hg in wheat (Rubio et al., 2023). Being an efficient accumulator of HMs compared to other cereals, rice alone may contribute to more than 50% of the maximum tolerable dietary intake (MTDI) for toxic metals (Munir et al., 2021). Asian countries consuming rice as a staple food are more prone to As poisoning (Bianucci et al., 2020). Recently, two US congressional reports have highlighted levels of As, Cd, Hg, and Pb in many food commodities, particularly baby foods, that are higher than the allowed levels under existing regulations (Subcommittee on Economic Consumer Policy Committee on Oversight Reform U.S. House of Representatives, 2021a; 2021b; Gray, 2023). Detection of HMs in leading baby food brands at excessive levels is a serious health risk for infants and young children, particularly given their increased susceptibility to HM toxicity due to their developing organ systems (Parker et al., 2022).

HM toxicity is clearly a matter of grave concern for human health, ecological safety, and plant productivity (Mishra et al., 2019). In Australia, where guidelines for As consumption do not align with WHO standards, daily exposure to As is estimated to exceed the benchmark dose lower confidence limit (BMDL) of 0.3–8 μg/kg of average body weight, indicating a potential increase in health risks (Gu et al., 2020). Due to the prevalent risk of HM toxicity in infants and lactating mothers, there is an urgent need to address HM contamination in food to protect human health. To minimize the absorption of these toxic elements by food crops, it is crucial to understand the complex interactions of these elements with soil components. Simultaneously, to reduce the presence of hazardous elements in food, understanding the mechanisms of uptake, tolerance, and accumulation in plant tissues is necessary. Additionally, promoting modern remediation technologies like phytoremediation, genetic modification of crops, suitable soil amendments, and agronomic practices, as well as the combined efforts of plant researchers and soil scientists, is necessary to achieve the necessary mitigation of toxic elements in food crops.

To promote food safety and environmental health, USDA-NIFA funded an expert workshop to discuss these topics. This review paper discusses the key findings of the workshop, including the current understanding of five hazardous elements in food, preventive measures, major research gaps, and key recommendations to minimize the presence of toxic metals in foods to protect public health and environmental safety.

2. Background: toxic heavy metals in the environment

Arsenic (As), a toxic metalloid, is a Group I carcinogen recognized by the International Agency for Research on Cancer (IARC) (Martinez et al., 2011). In 2001, the US Environmental Protection Agency (USEPA) set the Maximum Contaminant Level (MCL) of 10 μg/L of As in drinking water, while in soil, 5–20 mg/kg is generally considered safe (Matta & Gjyli, 2016). Moreover, irrigation with contaminated groundwater can elevate As levels up to 40 mg/kg in soil, which can be phytotoxic (Abedin et al., 2002; Takahashi et al., 2004). Among various natural forms of As chemical species, the inorganic forms viz., arsenate (AsO₄^‒3, AsV) and its reduced form, i.e., arsenite (AsO₃^‒3, AsIII), are more toxic because of their higher solubility, mobility, and bioavailability (Upadhyay et al., 2019). AsIII is more toxic than AsV and exhibits a different mode of impact. AsIII binds to thiol groups present in biomolecules and affects their catalytic function. AsV, a chemical analog of inorganic phosphate (Pi), metabolically competes with Pi for phosphorylation and ATP synthesis, thereby disrupting glucose and energy metabolism. Organic form of As occurs in the form of monomethylarsonic acid (MMA^V), monomethylarsonous acid (MMA^III), dimethylarsinic acid (DMA^V), and dimethylarsinous acid (DMA^III), which are far less toxic than the inorganic As species. However, the MMA^III is cytotoxic and is reported to inhibit the electron transport chain in mitochondria, causing DNA damage, and impaired gene expression (Moe et al., 2016).

Lead (Pb) is the second most toxic HM after As and is a Group II carcinogen, accounting for about 10% of total HM pollution (Collin et al., 2022; Rousseau et al., 2005). Anthropogenic activities such as fossil fuel combustion and the recycling and disposal of Pb-containing products like batteries and paints dominate the anthropogenic contributions to biogeochemical cycling (Cullen & McAlister, 2017). Affected soils can contain 400–1000 mg/kg Pb (Khatik et al., 2006). Moreover, Pb is toxic to plants, affecting growth, photosynthetic activity, and yield (Rahman et al., 2024). For humans, no level of Pb in the blood is considered safe. Studies suggest that Pb levels above 30 μg/dL can cause renal impairment in adults (Kuraeiad & Kotepui, 2021). Moreover, Pb exposure can induce neurological, respiratory, cardiovascular, and cognitive disorders and trigger associated diseases such as anemia, hypertension, and immunosuppression (Jaishankar et al., 2014; Mitra et al., 2022). Pb may occur as a free metal ion [Pb(II)], inorganic compounds (e.g., ${\text{CO}}_3^{2-}$and${\text{SO}}_4^{2-}$), organic ligands (e.g., fulvic acids and humic acids), or be adsorbed onto biological material and organic matter. Organic forms such as tetraethyl-Pb and tetramethyl-Pb are more harmful to biota than inorganic forms [Pb(II) and Pb(IV)] (Kumar et al., 2020).

Cadmium (Cd) is predominantly derived from anthropogenic sources such as the smelting and refining of copper and nickel, fossil fuel combustion, phosphate fertilizers, and Ni-Cd batteries (Cullen & McAlister, 2017; Genchi et al., 2020). Due to its high mobilization potential, Cd is readily leached into groundwater. The WHO recommends a guideline value for Cd of 3.0 μg/L in drinking water (Kubier et al., 2019). Based on animal studies, the IARC has classified Cd and Cd compounds as Group I carcinogens to humans (Rahman & Singh, 2019). High intake of Cd can result in renal and hepatic dysfunction, osteomalacia, and acute pneumonitis with pulmonary oedema. Long-term and occupational Cd exposure can cause chronic obstructive pulmonary disease, osteoporosis, liver and kidney defects, and cancer of various organs (Genchi et al., 2020). Cd generally occurs as the divalent Cd(II) ion or water-soluble complexes. Plants can accumulate inorganic Cd species from the soil, causing overt phytotoxicity (Moravčíková & Žiarovská, 2023).

Chromium (Cr) is a toxic HM and Group I carcinogen that occurs naturally in sediments and rocks, mainly as ferrochromite (Zulfiqar et al., 2023). The valence states of Cr include Cr(II) to Cr(VI). The hexavalent Cr(VI) and trivalent Cr(III) species are the most stable and relevant to human toxicity. Cr(VI) is far more toxic than Cr(III) due to stability, solubility, and cellular permeability, and is primarily released into the environment through anthropogenic activities (Ao et al., 2022). Cr is extensively used for industrial applications such as leather tanning, textile dyeing, production of wood preservers, anti-corrosive cooking systems, chrome plating, and boilers. In soil, Cr contamination can exceed 350 mg/kg and harm native microbial diversity (Yang, Tan, et al., 2022). In addition, Cr can disturb water homeostasis and nutrient uptake in crops such as maize, wheat, barley, and cauliflower, resulting in inhibited root growth, reduced biomass, leaf chlorosis, and yield loss (Jaishankar et al., 2014; Zulfiqar et al., 2023). Cr can enter the food chain to cause significant toxicity, such as renal damage, tumor formation, chromosomal aberration, genotoxic abnormalities, and hearing impairment (Genchi et al., 2020; Wang et al., 2021; Yang, Tan, et al., 2022). Animal studies reported a median lethal dose of 50–150 mg/kg for Cr(VI) species (Bojarski et al., 2021). Indeed, Cr(VI) levels found in ground and surface water often exceed the WHO recommendations for drinking water, i.e., 50 ppb (Tchounwou et al., 2012).

Mercury (Hg), though found in low concentrations in polluted wetlands and coastal sediments, can biomagnify to highly toxic levels and can produce gastrointestinal toxicity, pulmonary toxicity, neurotoxicity, and nephrotoxicity (Balali-Mood et al., 2021; Mishra et al., 2019). Coal-burning power plants are a major source of anthropogenic Hg emissions. Hg exists in three forms: elemental [Hg (0)], inorganic [Hg (I) and Hg [II)], and organic mercury (methyl/ethyl-Hg) having diverse toxicity and bioavailability. The order of toxicity is Hg (0) < Hg (I) and Hg [II) < Methyl-Hg (Mishra et al., 2019). Inorganic Hg(II) species generally accumulate in the form of mercuric sulfide (β-HgS) and dithiolate complexes (Hg(SR)₂) in the environment.

3. Workshop structure

Uptake of toxic metals by food crops and vegetables cultivated in polluted soil and post-harvest contamination presents a significant risk to human health (Pavlíková et al., 2023). However, there are significant knowledge deficits and complex challenges regarding the interactions of toxic metals in soil, as well as the mechanisms of their uptake, transport, and accumulation into plants. To address these important knowledge gaps, USDA-NIFA sponsored a virtual workshop titled “Toxic Elements in Food: Identification of Critical Knowledge Gaps to Ensure a Safe Food Supply” on April 4–5, 2022. The workshop began with an introductory plenary session, which was followed by many breakout discussion sessions centered around three thematic areas: (1) Soil biogeochemistry, soil amendments, and microbiome interactions with toxic elements; (2) Plant uptake and accumulation of toxic elements; and (3) Multidisciplinary concerns: food processing, detection, traditional knowledge, and regulatory standards. The participants included national and international scientists with expertise in toxic metal contamination in the US food supply chain, from crop cultivation through manufacturing and retail to consumers. This workshop aimed to improve our understanding of toxic element contamination in soils and subsequent uptake, transport, and accumulation into food crops. The workshop sought to pinpoint the crucial knowledge gaps concerning harmful elements in food so that strategies could be developed to ensure a safe food supply. A schematic representation of the workshop structure is provided in Fig. 2.

Fig. 2.

Structure of USDA-NIFA sponsored workshop.

4. Theme 1: soil biogeochemistry, soil amendments, and microbiome interactions with toxic elements

Soil geochemistry and the rhizosphere microbial community play critical roles in controlling the speciation, toxicity, solubility, and bioavailability of HMs, which influence their subsequent uptake and accumulation in food crops (Mawia et al., 2021). Understanding such soil-metal interactions is crucial to devising action plans and strategies to reduce HMs transfer in food. To outline key knowledge gaps, the soil and microbial panelists discussed vital points, including (a) the effect of soil geochemistry on the bioavailability and transport of HMs; (b) the influence of soil microbial community on metal speciation; (c) measures to alleviate the bioavailability of toxic HMs to reduce their uptake in plants.

4.1. Role of soil biogeochemistry in influencing metal speciation, solid-liquid partitioning, acquisition, and biotransformation

Soil physicochemical properties such as pH, redox potential, cation exchange capacity, texture, porosity, clay minerals, mineralogy, and organic ligand concentrations significantly influence the speciation, solubility, and mobility of HMs (Kumar et al., 2020). For instance, a lower soil redox potential converts AsV to the more toxic form AsIII. However, both low and high pH enhances As bioavailability by different mechanisms. An acidic environment promotes the solubility of As-binding species such as Fe-oxyhydroxide. While at pH > 8.5, desorption of As from iron oxides into soil increases. Importantly, Pb is the most persistent toxic metal. Irreversible adsorption onto particles makes Pb relatively immobile in soil and water systems. Only 0.1% of Pb contamination in soil is soluble and bioavailable for plant uptake and/or phytoextraction. Pb solubility is significantly impacted by cation exchange capacity, pH, and the size of soil particles (Pourrut et al., 2013). Conversely, Cd has a high mobilization potential in soil and is readily released into groundwater. Cd generally occurs as the divalent Cd(II) ion or water-soluble complexes. The presence of hydrous oxides, clay, and organic matter favors Cd sorption, while its mobility is facilitated by acidic pH and ionic strength (Kubier et al., 2019). The more toxic Cr(VI) is also more mobile than Cr(III), regardless of soil type and pH. However, in the presence of ferrous and sulfide ions or organic matter, Cr(VI) is reduced to Cr(III) ions (Choppala et al., 2013). To estimate the health risks posed by HMs, it is important to understand the sorption–desorption reactions of different metal species while considering the variable soil properties.

Compared to bulk soil, the rhizosphere region is characterized by dynamic metal mobility due to root exudation. Plant root exudates are rich in H⁺ ions, dissolved organic matter (DOM), and low molecularweight organic acids that influence the rhizosphere pH, metal sorption characteristics, and diffusion rates. Such mechanisms promote the mobility, acquisition, and bioaccumulation of HMs by reducing their sorption on soil. For instance, the hyperaccumulator ecotype of Sedum alfredii secretes Cd-induced dissolved organic matter (DOM) such as oxalates, lowering soil pH by 0.2–0.3 units and inducing the formation of soluble DOM-metal complexes that enhance Cd phytoextraction (Li et al., 2013). By contrast, metal-complexation agents such as carbonate, sulfate, and phosphate can reduce HMs mobility and minimize entry into the roots by chelating metal on the soil-root surface or precipitating the metal complexes in extracellular spaces (apoplasts), effectively controlling uptake and metal tolerance (Gupta et al., 2014; Pasricha et al., 2021).

Furthermore, rhizosphere microbial activity plays an important role in HM biogeochemistry through various biotransformation pathways. For instance, bacteria such as Desulfovibrio strain Ben-RB and Desulfosporosinus auripigmentum contribute to the release of As by inducing the weathering of As-bearing rocks under limited nutrition (Punshon et al., 2017). Conversely, supplying microbial inoculants such as Brevundimonas diminuta-NBRI012, Bacillus aryabhattai-MCC3374, and KKU2500 strains can minimize As uptake in rice by altering speciation and solubility (Mawia et al., 2021). Microbes can also oxidize AsIII to less toxic AsV and methylated species or assimilate AsV to produce more mobile organic species, such as MMA and DMA. Several bacterial strains such as Bacillus sp., Pseudomonas putida, Microbacterium sp., Arthrobacter sp., Vogococcus fluvialis, Sporosarcina saromensis, and Shewanella sp. can reduce Cr(VI) to less toxic and immobile Cr(III) species (Shahid et al., 2017). Moreover, the adsorption of As can be affected by the occurrence of mineral nutrients such as Fe, S, and P in the soil, which can directly compete for the available binding sites and indirectly influence the mobility and bioavailability of As for bioaccumulation (Mawia et al., 2021). Similarly, the presence of Ca, Mg, Mn, K, and Si has inhibitory effects on Cd uptake as they compete for shared ion channels and carrier proteins in plants. For example, high S levels stimulate Pb uptake, while Ca²⁺ ions competitively inhibit Pb absorption (Pourrut et al., 2011). Moreover, Cr(VI) uptake interferes with the absorption and subsequent assimilation of essential elements such as Fe, P, S, K, and Mg (Shahid et al., 2017).

4.2. Soil amendment practices to limit metal accumulation in food crops

As discussed above, the bioavailability of toxic HMs is one of the key determinants for their accumulation in plants. Low bioavailability favors food safety by preventing HM entry into crops, while high bioavailability is desired for bioremediation efforts. Soil amendments aim to modulate the intrinsic solubility and soil binding of toxic HMs by adding natural or artificial substances to immobilize HM contaminants through precipitation, complexation, adsorption, and ion exchange. Some of the proposed amendments to reduce HM bioavailability and accumulation in food include biochar, compost, plant exudates, hydroxyapatite (HAP), lime, ethylenediamine tetraacetic acid (EDTA), malic acid, and nanomaterials, among others (Wang et al., 2020). HAP is one of the most effective treatments for Cd and Pb while also serving as an inorganic P fertilizer (Zhu et al., 2019). Its unique hydroxyl group elevates the soil alkalinity and reduces metal mobility by forming chelates to prevent plant uptake. Application of nano-HAP in soil decreased the desorption percentage from 77.7 % to 0.8 % and 54.3 %–9.5 % for Cd(II) and Pb(II) ions, respectively (Chen et al., 2010). Biochar, having excellent adsorption capacity and nanoscale structure, can adsorb HMfrom soil to reduce migration to plants, thereby supporting growth by reducing accumulation and phytotoxicity (Zhang et al., 2021). Organic manure is a low-cost organic fertilizer that can also alleviate HM toxicity through adsorption and complexation reactions (Wang et al., 2020). Certain nanomaterials, when applied in soil or water, are highly effective in preventing the uptake and accumulation of toxic metals in plants (Ma et al., 2021; Zhou et al., 2020). Nanosulfur reduced As accumulation in rice roots and grains by 69% and 54%, respectively, and Hg accumulation in Brassica juncea roots and shoots by 6–8 folds (Meselhy et al., 2021; Yuan et al., 2021). Similarly, graphitic carbon nitride (C₃N₄) diminished the uptake of Cd (32%) and As (25%) in rice roots (Ma et al., 2021). Conversely, strong chelators such as EDTA can solubilize the common inorganic fraction of Pb to enhance its bioavailability and phytoextraction (Lebrun et al., 2023; Yang, Jiang, et al., 2022). Thus, the addition of EDTA in contaminated soil significantly enhanced Pb absorption in roots (51.8%) and aboveground tissue (210.8%) in bamboo (Zhang et al., 2018). However, increasing Pb mobility may further increase the concerns about its leaching into water. Notably, the effects of soil amendments on metal bioavailability vary significantly with the intrinsic properties of the metal contaminant, physicochemical soil properties, microbiome activity, and plant-metal interactions.

4.3. Soil-microbe-plant relations and microbial remediation

The rhizosphere microbial community and endophytes play a major role in metal speciation and phytoaccumulation. Microbes can alter metal speciation, solubility, toxicity, and sequestration through geo-microbial processes such as biosorption, biomineralization, intracellular accumulation, and biotransformation (Kurniawan et al., 2022). Several metal-resistant bacteria, fungi, and microalgae have been evaluated for HM remediation in the environment. For instance, Methanothermobacter thermautotrophicus, Bacillus cereus, and Shewanella can reduce Cr (VI) to Cr (III), with subsequent immobilization as hydroxides/oxides (Mishra et al., 2019). Other microbes investigated for targeted HM remediation include Pseudomonas aeruginosa (for Hg), Bacillus megaterium (for Cd), and Micrococcus luteus DE 2008 (for Pb) (Kurniawan et al., 2022). Furthermore, several bacteria, fungal, and microalgae species have been genetically modified to improve their remediation potential, including Escherichia coli, Pseudomonas putida, Mesorhizobium huakuii, Caulobacter crescentus, Aspergillus flavus, Aspergillus niger, and Chlorophyta C reinhardtii (Saravanan et al., 2022). For instance, Hg-resistant bacterial strains have been tailored using the mer operon-mediated detoxification mechanism for wastewater treatment (Hui et al., 2023). In addition, some endophytic microbes improve the remediation potential of plants (phytoremediation) and other soil microbes. For example, the phytoremediation capacity of hyperaccumulators can be enhanced by ‘endophytic bioaugmentation,’ which involves the inoculation of cultured endophytic species to promote the local community of metal-resistant microbes by interacting and exchanging genes with rhizosphere and phyllosphere communities. For instance, Pseudomonas putida and Pseudomonas sp. HU002 have been applied with willow trees for Cd remediation (RedfernLauren & GunschClaudia, 2016). Phytoaugmentation-assisted remediation has the potential for higher HM phytoextraction than phytoremediation or bioaugmentation alone. However, limited understanding of plant-microbe interactions, the dynamics of rhizosphere microbiome, and the impact of environmental variations limit phytoaugmentation-based strategies. Hence, exploring endophytic microbes suitable to remediate HMs and their interaction with rhizosphere microbiomes is a promising area of research. Furthermore, detailed insight into the genome of relevant plants and microbes can enable a greater understanding of the genetic route to improve species for HM remediation or to restrict uptake and accumulation in food crops.

4.4. Existing knowledge gaps in the understanding of soil and metal interactions

Soil, being an extremely complex medium, makes it more challenging to devise solutions to resolve HM contamination. The fate of some elements in the soil is better understood than others, but to improve the understanding of system complexity, simplified spatial or temporal scale techniques should be taken into account. Soil biogeochemistry is complex and requires extensive investigation to understand how contaminants interact and respond to seasonal and temporal variations, and how climate affects metal fate and disposition. Since different chemical species of metals have varying effects on their biogeochemical nature, the total metal contamination in a given soil does not always reflect the toxic profile. As a result, speciation data on heavy metal ions is crucial for risk evaluation and remediation studies (Shahid et al., 2017). Developing effective remediation solutions requires a deeper mechanistic knowledge of the impacts of soil amendments on metal availability, including the relative contributions of pH and sorption components. Particularly under varying moisture regimes, there is a knowledge gap regarding the biotic and abiotic-driven mobilization mechanisms of metals in the rhizosphere.

5. Theme 2: uptake, translocation, and accumulation of toxic heavy metals in plants

Once toxic metals become bioavailable in contaminated soil or water, their transfer and bioaccumulation in food are primarily governed by the metal-plant interactions in the rhizosphere. Research suggests that the HM accumulation decreases in the order as leafy vegetables > stalk vegetables/root vegetables/solanaceous vegetables > legume vegetables/melon vegetables (Zhou et al., 2016). Vegetables such as spinach, lettuce, sweet potatoes, and cabbage, planted in contaminated soil can accumulate HM, which can be hazardous for human consumption (Zhou et al., 2021). An explicit understanding of the mechanisms governing HM transfer in plants and detoxification pathways can assist in formulating mitigation and remediation strategies. The panelists in this theme discussed key topics such as (a) current knowledge of molecular mechanisms for HM uptake, accumulation, and tolerance in food crops; (b) technologies to prevent uptake of toxic HM; (c) understanding the role of endophytes and rhizosphere microbial communities in plant metal tolerance and absorption; (d) plant-based remediation strategies to alleviate HM contamination; (e) the need to uncouple nutrient and contaminant uptake pathways; and (f) critical knowledge gaps limiting the development of tolerant and safe crops to ensure food and nutritional security.

5.1. Current understanding of molecular mechanisms governing toxic metals uptake, transport, and phytoaccumulation

The uptake of toxic HMs by plants occurs through two routes: (a) apoplastic pathway (passive diffusion) and (b) symplastic pathway (active energy-dependent transport). The latter is the more prevalent route for HM absorption in plants. Here, HMs soluble in soil are cotransported to roots and translocated to the aerial parts of the plant due to imperfect substrate selection via ion transporters mediating nutrient uptake. Plants may deploy distinct strategies to accumulate different bioavailable chemical species of HMs. This section discusses the understanding of the genetic basis for the uptake, translocation, accumulation, and detoxification of five major toxic elements in plants.

5.1.1. Arsenic

Arsenate (AsV), the most predominant form in aerobic soil, is cotransported into the roots with inorganic phosphate (Pi) and translocated via high-affinity phosphate transporters (Wu et al., 2011). In Arabidopsis, several phosphate transporters (PHTs), viz. AtPHT1; 1, AtPHT1; 4, AtPHT1; 8, and AtPHT1; 9 have been demonstrated to facilitate AsV uptake, translocation, and tolerance (LeBlanc et al., 2013; Li et al., 2016; Srivastava et al., 2016) (Fig. 3). In rice, the function of three phosphate transporters, viz. OsPT1, OsPT4, and OsPT8 have been demonstrated roles in governing the uptake and accumulation of both AsV and Pi in roots, shoots, straw, and grain (Kamiya et al., 2013). Conversely, under reducing conditions, members of the Nodulin-like Intrinsic Proteins (NIP) subfamily of aquaporins viz. AtNIP1; 1, AtNIP1; 5, AtNIP1; 7, are predominantly responsible for arsenite (AsIII) uptake in Arabidopsis. In rice, AsIII is accumulated by OsNIP2; 1, also known as Lsi1, a silicon (Si) transporter in root cells (Bienert & Jahn, 2010). While some accumulated AsIII is effluxed back into the rhizosphere, the remainder is transported towards the stele for xylem loading, with the help of Lsi2, an efflux protein channel having bidirectional permeability for As and Si (Ma et al., 2008). Some members of the Plasma Membrane Intrinsic Proteins (PIPs) subfamily of aquaporins, such as OsPIP2; 4, OsPIP2; 6 and OsPIP2; 7, also reduce AsIII accumulation by active efflux and influx of AsIII in roots when overexpressed in Arabidopsis (Mosa et al., 2012). Once in roots, AsV can be either translocated to shoot via PHTs present in xylem vessels or readily reduced to AsIII by arsenate reductases such as OsHAC1; 1, OsHAC1; 2, and OsHAC4, which also facilitate AsIII efflux back to the rhizosphere (Xu et al., 2017). Notably, the reduction of AsV to AsIII is necessary for detoxification in plants, primarily by forming thiol-complexes with glutathione (GSH) and phytochelatins (PCs) in the cytosol (Dhankher et al., 2002). The resultant AsIII-PC or AsIII-GSH complex is transported for vacuolar sequestration by transporters such as AtABCC1 and OsABCC1 in the endodermal cells (Song et al., 2014). In rice, xylem loading of AsIII and AsIII-thiol complexes is mainly facilitated by efflux transporters, OsLsi2 and OsABCC7, for translocation to shoots (Chen et al., 2017). Inositol transporters, AtINT2 and AtINT4, govern AsIII loading into phloem tissues in Arabidopsis (Duan et al., 2015). Recently, a xenobiotic transporter, OsMATE2, has been implicated in the translocation and accumulation of As in rice seeds (Tang & Zhao, 2021). Phytochelatin synthases (PCS) catalyzing the synthesis or turnover of thiol-rich peptides, such as OsPCS1 and OsPCS2 in rice, contribute significantly to the detoxification of As by providing chelating agents. Moreover, Glutathione (GSH), a precursor for PCs and substrate for thiol-complexation of AsIII, plays a crucial role in As detoxification (Dhankher et al., 2002; Paulose et al., 2013; Singh et al., 2024). A detailed schematic highlighting the mechanisms of As uptake, transport, accumulation, and detoxification in rice is provided in Fig. 3. Importantly, investigations supporting an in-depth understanding of As transport and detoxification pathways are needed in a range of grains and vegetables to better understand the risk of As accumulation.

Fig. 3.

Schematic overview of the mechanisms of arsenic uptake, transport, detoxification, and accumulation in rice.

5.1.2. Cadmium

The entry of Cd in roots is facilitated by transporters for essential elements (Ca, K, Zn, and Fe), such as natural resistance-associated macrophage proteins (NRAMPs), heavy metal transporting ATPases (HMAs), zinc and iron-regulated transporter proteins (ZIP), ATP-binding cassette (ABCs), and yellow stripe-like (YSL) families (Sterckeman & Thomine, 2020; Tao & Lu, 2022) (Fig. 4). For instance, in rice, OsNRAMP5, a metal transporter for constitutive Fe and Mn uptake, plays a major role in Cd absorption (Chang et al., 2022). In fact, Fe deficiency in soil can stimulate Cd uptake through an iron-regulated transporter (IRT1) in Arabidopsis, rice, brassica, and Vicia sativa (Nakanishi et al., 2006; Zhang et al., 2020). Metal exporters such as OsZIP1 and OsHMA9 efflux excess Cd(II) to limit the Cd accumulation (Liu et al., 2019). Similarly, Cd(II) and its conjugates can be exported by OsABCG36, a G-type ATP-binding transporter in mature root zones, and root tips to impart tolerance against high Cd burdens in rice (Fu et al., 2019). In rice, which is well known to accumulate Cd in shoots and grains, root absorption and translocation of Cd towards xylem is regulated by efflux transporters expressed in the vascular bundles, such as OsHMA2 (a P_1B-type ATPase), OsCCX2 (a putative cation/calcium exchanger transporter), OsCAL1 (a defensin-like protein) (Feng et al., 2021; Takahashi et al., 2012). Furthermore, for long-distance transport to the stems and leaves, Cd is translocated in the form of Cd–phytochelatin (Cd-PC) and Cd–glutathione (Cd-GS₂) conjugates by transporters such as OsLCT1, OsHMA2, and OsZIP3. Such transporters are also accountable for Cd redistribution in phloem and accumulation in rice grains (Hu et al., 2023). For Cd detoxification, most plants compartmentalize Cd complexes into the vacuoles by ABC and HMA family transporters. For instance, OsHMA3, OsABCC9, and OsABCG43 proteins have been implicated in vacuolar transportation and sequestration of Cd chelates from the cytosol to alleviate Cd toxicity in rice (Yang et al., 2021). However, the mechanisms of Cd accumulation in other food crops, such as barley, maize, and wheat, are poorly understood.

Fig. 4.

Schematic overview of the mechanisms of cadmium uptake, transport, detoxification, and accumulation in plants.

5.1.3. Lead

Plants with well-developed root systems can adsorb free Pb(II) ions by capillary action from the soil, with subsequent binding to the charged ion-exchangeable locations in the cell walls. This results in non-uniform Pb adsorption on the root surface, with the highest concentration at the acidic zones of the root apex favoring Pb solubility (Collin et al., 2022). Pb fixed on the rhizoderm cells can passively enter the root through the water conduction system; however, the molecular mechanism of Pb entry to the roots is still unclear. It is possible that Pb penetrates the root cells through Ca²⁺ permeable cation channels, non-selective pathways such as cyclic nucleotide-gated ion channels (AtCNG1, AtCNG11, AtCNG13) in Arabidopsis and calmodulin-binding protein (NtCBP4) or low-affinity cation transporters (TaLCT1) in tobacco (Moon et al., 2019; Park & Shin, 2022; , Pourrut et al., 2011; Sunkar et al., 2000 ) (Fig. 5). Recently, OsNRAMP5, also involved in the transportation of Cd, Fe, and Mn, has been reported as a Pb carrier in rice (Chang et al., 2022). Several transporter protein subfamilies, such as pleiotropic drug resistance (AtPDR8), leucine-rich repeat (LRR) protein, and P-type ATPases, have been implicated in regulating resistance by pumping Pb and Pb-complexes out of the cytoplasm in Arabidopsis and tobacco (Bali et al., 2019; Kumar & Prasad, 2018; Lee et al., 2005). However, 90% of the penetrated Pb is immobile due to its high-affinity linkage to external cellular components and precipitation in intercellular spaces. Unlike other HM, the translocation factor for Pb is relatively low for most plant species, restricting transfer to the shoots. The endoderm also acts as a physical barrier where Pb may precipitate by the Casparian strips, enforcing symplastic transport of remaining unbound Pb(II) ions (Pourrut et al., 2013). Vacuolar transporters such as AtATM3 regulate the symplastic sequestration of Pb in inactive cell compartments to limit its xylem loading in Arabidopsis (Kim et al., 2006). Despite low translocation, Pb(II) ions in the air can directly enter leaves via the cuticle and stomata. However, various complexation, sequestration, and detoxification mechanisms for Pb still need to be investigated for this exposure route.

Fig. 5.

Schematic overview of the mechanisms for uptake, transport, detoxification, and accumulation of chromium, mercury, and lead in plants.

5.1.4. Chromium

Despite extensive studies on Cr phytotoxicity, the precise mechanism of Cr uptake, transport, detoxification, and accumulation remains unknown. Studies have shown that Cr(III) is adsorbed passively through an energy-independent mechanism, while active adsorption of Cr(VI) is mediated by carriers of other essential anions, such as sulfate and phosphates, due to structural similarity (de Oliveira et al., 2015; Schiavon et al., 2008; Xu et al., 2021) (Fig. 5). Brassica species known for high Fe and S accumulation also show greater uptake of Cr, indicating the involvement of iron/sulfate transport proteins (da Conceicao Gomes et al., 2017). Cr(VI) complexes are carried by symplastic pathways and subsequently reduced to Cr(III) by unidentified endogenous Cr reductases, whereas the Cr(III) complexes enter through the apoplastic route. Due to limited translocation to aerial tissues, Cr is sequestered in the cortex as Cr(III). The remaining Cr(VI) is sequestered in the vacuoles as soluble Cr-EDTA, which can enter the xylem and be translocated to aerial tissues (Pasricha et al., 2021). If not reduced, Cr (VI) ions trigger ROS formation and significant oxidative damage.

5.1.5. Mercury

Although no Hg-specific transporters have been identified in plants, root cells can readily import Hg, possibly through broad-substrate systems such as Fe, Cu, or Zn transporters/channels (Chen & Yang, 2012) (Fig. 5). Hg accumulated by roots is primarily retained within this tissue due to interactions with anionic compounds in the cell wall to form insoluble precipitates that limit symplastic mobilization; however, a small fraction of Hg can be translocated to leaves, flowers, and developmental tissues (Pasricha et al., 2021). In addition to roots, stomatal and cuticular uptake in foliage are important ways to adsorb the gaseous Hg (0) from the atmosphere, as observed in maize and wheat. (Sommar et al., 2016; Sun et al., 2020). However, the precise mechanism by which Hg enters leaves remains elusive. Inside the leaves, Hg (0) is oxidized and incorporated in epidermal and stomatal cell walls as divalent Hg(II) ions (Zhou et al., 2021). Indeed, a greater understanding of the genes regulating Hg uptake and accumulation in plants could facilitate the development of an efficient phytoremediation strategy suitable for field scenarios or to effectively reduce Hg accumulation in food crops for food safety.

5.2. Strategies for reducing toxic elements in food

Since inorganic HM species cannot be degraded, they must be either removed from the soil and water to prevent bioaccumulation or transformed into non-toxic or non-bioavailable forms. Conventional physical and chemical remediation methods involve water treatment, soil removal, and re-burial, soil incineration and washing, Soil vapor extraction, thermal desorption, electrokinetic remediation, etc., but are expensive, environmentally destructive, and impractical on the scale required (Gaur et al., 2021). New safer plant-based HM removal technologies, such as phytoremediation, phytoaugmentation, and genetically modified plants for reduced uptake, are proving to be viable, environmentally friendly, and cost-effective alternatives for remediation.

5.2.1. Phytoremediation

Phytoremediation is an eco-friendly plant-based technique for the clean-up of hazardous contaminants from polluted soils, sediments, and water (Dhankher et al., 2002; Dhankher et al., 2012). Plant tolerance to HM varies with species but is primarily governed by two strategies: (a) metal exclusion and (b) metal accumulation followed by sequestration or detoxification. Some plants can be excluders that retain HMs only in the root system and exhibit a low shoot/soil metal concentration coefficient (<1). Metallophyte species like Armeria maritima ssp. Helleri can immobilize 10–80 times higher Cd and Pb in roots and restrict translocation to shoots. Conversely, species such as Cardaminopsis helleri can translocate and sequester high quantities of Cd in the harvestable aerial tissues without any adverse effects on growth and metabolism (Dahmani-Muller et al., 2000). Such ‘hyperaccumulator’ species exhibit a high shoot/soil metal concentration coefficient (>1) and have considerable phytoremediation potential. Hyperaccumulators are marked by strong mobilization, uptake, chelation, faster root-to-shoot translocation, and an ability to detoxify and sequester HM in aerial tissues. Hyperaccumulator species can accumulate more than 10 mg/kg of Hg, 100 mg/kg of Cd, and 1000 mg/kg of Cr in shoot tissues (Pasricha et al., 2021). Pteris. Vittata is a hyperaccumulator of As and can achieve 7500 mg/kg (Ma et al., 2001). Some other hyperaccumulator species are Brassica juncea, Thlaspi caerulescens, and Youngia japonica (for Cd); Eremochloa ciliaris (for Hg); Cannabis sativa and Allium griffithianum (for Cr); Tagetes minuta and Bidens pilosa (for Pb); and P. cretica and P. vittata (for As) (Ma et al., 2001; Salazar & Pignata, 2014). Importantly, most hyperaccumulators employ a common mechanism for phytoremediation that involves (a) HM bioactivation in the rhizosphere, (b) enhanced uptake by root cells through metal transporters, (c) detoxification of HMs by binding to cell-wall and various chelating peptide ligands such as phytochelatins, metallothioneins, and metal-binding proteins in the cytosol, and (d) sequestration of HM-ligand complexes in vacuole to prevent phytotoxicity (Yang et al., 2005). The harvested biomass can be processed, and incinerated to recover the metals.

5.2.2. Food waste as an adsorbent of toxic metals

Using dietary fibers for adsorption is another method for remediating metal-contaminated soil, leachates, or groundwater. This technique has been investigated extensively over the past two decades. Plant cell walls contain most of the functional groups necessary for binding metal ions. Dietary fibers (DF) are made up of various indigestible plant components, including cellulose, hemicellulose, lignin, pectin, and small amounts of protein, all of which come from agricultural by-products (Demirbas, 2008). The metal-binding capacity of DF is attributed to functional groups such as carboxyl, phenolic, lactonic, and hydroxyl groups, which help remove heavy metals from polluted environments. These functional groups can substitute for hydrogen ions and interact with metal ions. The adsorption ability may be enhanced by the electrostatic attraction between positively charged metal ions and the negatively charged functional groups in DF (Shaheen et al., 2019). Additionally, metal adsorption on fiber surfaces may involve forces such as hydrophobic interactions, van der Waals forces, and hydrogen bonding (Huang et al., 2020).

For example, cocoa shells, which are rich in fibers (pectin and cellulose), proteins, and polyphenols, were utilized as a natural adsorbent to effectively remove lead (Pb) and other metals like copper (Cu) and zinc (Zn) from acidic soil leachates (Meunier et al., 2004). The results indicated that cocoa shells could remove approximately 1060–2730 mg of Pb per kg from contaminated leachates. The ion removal process in cocoa shells was largely driven by ion-exchange reactions with calcium, magnesium, potassium, and protons, with carboxyl and amine groups being crucial for Pb uptake. Additionally, Derakhshan-Nejad & Jung (2019) demonstrated that raw rice husks and maple leaves could purify agricultural soil from Pb, Cu, Cd, and Zn using immobilization techniques. Yang, Tan, et al. (2022) developed a two-stage sequential washing method using extracts from food wastes like pineapple peel, lemon peel, grapefruit peel, and crab apple to remediate metal-contaminated soil. The mechanisms for removing cadmium (Cd) and copper (Cu) with pineapple-peel washing agents involved acid activation, cation exchange, and complexation with carboxyl groups. Dietary fibers can bind both harmful heavy metals and essential elements like Ca, Cu, Fe, and Zn, which poses challenges for their use in selectively removing toxic metals (El-Bayaa et al., 2009). Since heavy metals rarely exist in isolation, understanding the competitive adsorption of multiple metals on DF is crucial for effective ion-exchange processes. Future research should focus on optimizing conditions, identifying suitable fibers for specific metals in multi-metal scenarios, and exploring immobilization, reuse, and recovery of DF. Additionally, advancements in nanotechnology, such as nano-coating or nano-impregnation of DF, could enhance their efficacy and selectivity in heavy metal removal.

5.2.3. Genetic engineering and genome editing approaches for reducing HMs in food crops

Genetic engineering can enhance the phytoremediation potential by increasing the plant’s catalytic potential and toxic metal bioavailability by altering the existing removal mechanisms or introducing novel metabolic pathways. Harnessing these rate-limiting steps for uptake, translocation, and HMs detoxification can be utilized to develop transgenic hyperaccumulators with enhanced phytoextraction capacity, tolerance to HM phytotoxicity, and suitability for cultivation on HM-polluted soil. For instance, genes encoding ATP-binding cassette (ABC) type C tonoplast transporters, viz. AtABCC1 and AtABCC2, have been shown to directly govern As, Cd, and Hg detoxification by facilitating the mobility and compartmentalization of their PC-conjugates in the vacuoles of Arabidopsis (Park et al., 2012). Overexpression of an ABC transporter from poplar (PtABCC1) enhanced Hg tolerance and accumulation in Arabidopsis and poplar (Sun et al., 2018). Such mechanisms provide a promising strategy to develop HM-tolerant plants for cultivation in polluted areas. Moreover, others have expressed bacterial genes (merA and/or merB) that encode the mercuric ion reductase and organomercurial lyase in Arabidopsis thaliana to convert more toxic and environmentally relevant organic mercury (CH₃Hg) to less toxic Hg(II) ion, followed by its reduction to the elemental mercury [Hg (0)] (Meagher, 2000). Following codon optimization, researchers have successfully translated this approach into tobacco, poplar, rice, Eastern cottonwood, peanut, and other species to sustain up to 25–100 μM HgCl₂ (Ruiz & Daniell, 2009). However, successful demonstration in the field is limited by low Hg bioavailability, plant uptake, and translocation to aerial parts (Gworek et al., 2020). In addition, manipulating genes involved in the biosynthesis of crucial metal chelators can promote HM tolerance. For instance, the expression of CdPCS1, a gene encoding phytochelatin synthase (PCS) enzyme in Ceratophyllum demersum L., a metal accumulating aquatic plant, enhanced PC synthesis and the accumulation of As and Cd in the aerial tissues of transgenic Arabidopsis (Shukla et al., 2013). Enhancing the antioxidation capacity is another widely used strategy for developing HM tolerance. Expression of the bacterial γ-glutamylcysteine synthetase (γ-ECS) gene that encodes a key enzyme catalyzing glutathione synthesis conveyed tolerance to Hg and As in Arabidopsis (Li et al., 2006) and Cd resistance in poplar due to increased HM ion influx, allocation, and detoxification via glutathione-dependent pathways (He et al., 2015). Furthermore, combined and tissue-specific expression of bacterial arsenate reductase ArsC and γ-glutamylcysteine synthase (γ-ECS) enhanced As tolerance and hyperaccumulation of As in the aboveground shoots of Arabidopsis (Dhankher et al., 2002).

Gene editing and engineering approaches can also reduce metal uptake in crops for food safety. Knockouts of OsNRAMP5, which encodes a key regulator of root uptake for Cd, resulted in a significant decrease in Cd accumulation in shoots and grains in rice (Tang et al., 2017). Similarly, CRISPR/Cas9 mediated mutation of OsLsi2, a major transporter of AsIII in roots, reduced As accumulation in rice by more than 60% (Xu et al., 2024). Similarly, RNAi-silencing of a membrane intrinsic protein OsPIP2; 6 significantly reduced As accumulation in rice shoots (Meselhy et al., 2024). Several other metal transporters can be exploited by genetic engineering approaches for food safety. For instance, overexpression of OsABCC1, a tonoplast-localized ABC transporter gene in rice, can enhance vacuolar sequestration of As in the phloem companion cells in nodes to limit transport to grains, hence reducing the risk of As exposure (Song et al., 2014). The ectopic expression of an ABC transporter from poplar (PtoABCG36) functions as a Cd extrusion pump which can reduce Cd content in crop species (Wang, Liu, et al., 2019). The γ-glutamyl cyclotransferase (GGCT2; 1), a GSH recycling enzyme, has been implicated in regulating tolerance against As and Cd in Arabidopsis. Overexpression of AtGGCT2;1 and CsGGCT2;1 in Arabidopsis and Camelina sativa, respectively, significantly reduced the phytoaccumulation of As (Paulose et al., 2013; Singh et al., 2024). In fact, inoculation with an engineered bacterial strain (WH16–1-MT) expressing surface metallothionein for increased Cd absorption capacity has reduced Cd accumulation in rice grains (Yu et al., 2022). Such genetic modification approaches can be translated further to develop HM-tolerant crops that can be cultivated on contaminated soil while reducing HM uptake and bioaccumulation in food crops, hence ensuring food security and safety.

5.3. Safer disposal of HM-enriched biomass

Cultivation of microbial and plant species for remediation of contaminated sites produces large amounts of HM-enriched biomass. Traditional disposal practices such as in-situ combustion, landfilling, composting, etc, intending to quickly reduce the waste volume and provide organic matter to the fields, indeed impose the risks of migration and re-entry of the pollutant in the environment. The usage of these disposal methods is still in effect because of their time and cost-effectiveness (Chai et al., 2022). Incineration of HM-enriched biowaste converts the biomass into fly ash which requires further stabilization to curb the risks of further leaching of HM into the environment. Thus, safer and sustainable solutions for longer term applications are warranted to dispose of HMs. Pyrolysis is a widely used thermochemical technique to effectively reduce HM-enriched biomass and recover HMs after transforming and stabilizing the non-volatile HM species in less toxic and stable chemical form under high temperature and reduced oxygen conditions. Pyrolysis can convert HM-enriched biowaste into value-added by-products such as biochar and bio-oil that can serve as a low-cost absorbent and energy-source, respectively (Raheem et al., 2022). In addition to the above mentioned thermal procedures, hydrothermal carbonization is a superior effective way to recycle HM-enriched biomass into value-added solid fuel in presence of water, given a certain temperature and pressure, particularly for hyperaccumulator plants after phytoremediation. For instance, this approach reduced Cd concentrations in sunflower grown in HM contaminated site from 23.6 mg/kg to 5.31 mg/kg and 3.12 mg/kg in the hydrochars at temperatures ranging from ranging between 160 °C and 260 °C, which is lower than the maximum permissible level for bio-solid refuse fuel (Lee & Park, 2021).

5.4. Limits to HM accumulation and remediation

Green technologies, such as phytoremediation, have limitations. Even hyperaccumulators cannot sustain healthy growth at higher contamination levels. Several hyperaccumulators have high metal tolerance, but they grow slowly and produce small harvestable aboveground tissue, which limits their phytoextraction capacity and their use in the field. In addition, the implementation of phytoremediation is limited by low bioavailability and absorption of metal (oid)s. Phytoremediation may only be effective in remediating low levels of pollution in sites where plant cultivation is possible, and the HMs are accessible to roots. Under these circumstances, significantly reducing the HM burden could take years to decades. Methods to dispose of contaminated biomass, such as pyrolysis and incineration, can significantly decrease the waste volume, but the further burial and recycling of metal concentrate is expensive. Improper biomass disposal after remediation may exacerbate the risk of food chain contamination. Phytostabilization of HMs in soil using biochar and other nanomaterials is a valuable approach to limit HM uptake in food crops. However, developing non-edible hyperaccumulators with high biomass, tolerance to HM toxicity, disease resistance, and climate adaptability is desirable for effective phytoremediation.

Manipulation of key genes controlling the uptake, mobilization, resistance/tolerance, and bioaccumulation of toxic elements can increase the remediation capacity of high biomass and non-food plants, or even limit the uptake of HMs in food crops. However, an understanding of genetic and metabolic pathways governing HM transport is still incomplete in plants. With the exceptions of intensively studied As and Cd uptake mechanisms in rice, the molecular mechanistic understanding of Pb, Cr, and Hg in food crops is limited. The lack of knowledge of Cr (VI) reductases in plants is a major limiting factor in Cr remediation and detoxification. In addition, HM tolerance is highly species-specific, and a detailed investigation of species-to-species variation is necessary to understand underlying molecular mechanisms. Additionally, a significant overlap of pathways of nutrient and toxic metal uptake makes it difficult to uncouple both phenomena in order to develop resistant plants with reduced HM uptake without trading beneficial growth and nutritional status. Metal speciation is an important aspect in terms of understanding phytotoxicity and phytoaccumulation. However, in-planta toxicodynamics of HMs is understudied. Additionally, climate factors such as precipitation, solar radiation, temperature, and atmospheric CO₂ may have positive or negative impacts on the plant-metal interactions and plant-soil dynamics depending on exposure conditions. For instance, changing temperature may alter the solubility and bioavailability of certain HMs by affecting soil biogeochemistry. The correlation of metal uptake and toxicity with growth conditions and environmental stresses such as drought, salinity, and temperature extremes needs to be understood. Promising technologies like genome editing via CRISPR/Cas9 and/or genetic engineering approaches should be explored for developing new crop varieties with reduced accumulation of toxic metals in edible tissues. In addition to genetic modification, molecular breeding can combine the traits of high-yielding crop cultivars with crops exhibiting low HM uptake. Thus, associated genetic markers and linked Quantitative trait loci (QTLs) for yield and low HM accumulation in vegetative tissues and seeds should be explored.

6. Theme 3: multidisciplinary concerns

Food chain contamination is a transdisciplinary problem between crop science, soil biology, and soil biogeochemistry and requires a cooperative approach to develop successful solutions. Moreover, the diversity of agricultural products and the complexity of food processing and cooking practices demand the collaborative attention of multiple disciplines to alleviate food safety concerns.

6.1. Soil-metal-plant dynamics

The migration dynamics and solid-liquid distribution of HMs in soil are not well understood and depend on interaction with soil components such as clay fractions, ion content, and organic matter. A thorough assessment of the factors influencing metal solubility is an essential prerequisite of any attempt to prevent HM uptake in crops or remediate contaminated soils. For instance, organic matter in soil can immobilize Pb and Hg and bioavailability, preferably at low pH (Chen et al., 2023). Conversely, anions like Cl⁻ and OH⁻ have more affinity for ions such as Cd²⁺ than for soil, and can enhance metal mobility (Tian et al., 2017). Similarly, complexation with organic matter in soil facilitates Cr(III) solubility and uptake (Hao et al., 2022). Understanding such complex and dynamic soil-metal interactions is a critical knowledge gap for implementing remediation and food security strategies, especially when considering realistic scenarios of multi-metal exposure and the confounding impacts of a changing climate (Xiao et al., 2024). The topography of the landscape with respect to hydrology can affect HM contamination levels. For instance, high temperatures promote the mobility and bioavailability of HMs resulting in greater transport, loading, enrichment, and pollution of Pb and Cd in the watersheds of sub-tropical areas than in the temperate area (Liu, Ouyang, et al., 2020). Extended longitudinal studies would facilitate investigations to assess the impact of weathering and the ensuing changes in the bioavailability profile. Also, with the advent of modern agricultural practices to maximize the crop-yield, it is difficult to predict the variations in the metal bioavailability in bulk soil and soil-to-crop metal transfer in the rhizosphere. The disturbance in the synergistic rhizobacteria-plant interactions may inhibit the natural defense mechanisms against HM stress from being be established (Barra Caracciolo & Terenzi, 2021). Advance knowledge of complex soil-metal-plant interactions can help to build better agroecosystem to enrich food yield and quality. To reduce toxic compounds in food, more realistic, affordable, deployable, and sustainable agronomic techniques and soil amendments are needed. Public education on toxic metals in food crops and site-specific cropping systems is also crucial. It is also important to support free or inexpensive soil testing through government-sponsored initiatives to increase awareness among stakeholders and sensitive populations.

6.2. Food processing and cooking practices risking HM contamination

In addition to intrinsic factors such as soil, water, and crop exposure, extrinsic factors such as post-harvest handling, food processing, packaging, storage, transportation, cooking tools, and methods can also result in HM contamination of food (Letuka et al., 2023). For instance, processing techniques such as dehydration and lyophilization may elevate the overall quantity of toxic elements in processed foods (Adenitan et al., 2022). Many manufacturers use additional components, such as vitamin premixes, proteins, and enzymes, in processed infant meals that may further contribute to the contamination (Subcommittee on Economic Consumer Policy Committee on Oversight Reform U.S. House of Representatives, 2021a; 2021b). However, some traditional cooking and processing practices, such as washing, parboiling, boiling, steaming, frying, and roasting, can effectively leach out toxic metal contamination from vegetables and cereals (Adjei-Mensah et al., 2021; David et al., 2020). HMs such as Pb, Cd, and As were reduced by extracting oil from oilseeds, boiling noodles, and infusing teas (Lee et al., 2019). However, these methods may have varying effects on different food products, especially seafood and meat products, a major source of As and Hg in food. For instance, grilling and frying increased the concentration of As in sardine fish. In potatoes, Cd concentration increased from 0.007 mg/kg in raw state to 0.012 mg/kg after frying. In contrast, smoking and grilling can lower the Pb content in mush meat. While frying, followed by boiling, decreased Hg concentrations in tuna fish (Perello et al., 2008). Contact of food with packaging material such as metal cans may also result in metal contamination (Chera-Anghel & Stefan-van Staden, 2023). Using metal vessels, especially anti-corrosive cooking tools, can increase the risk of the leaching of toxic metals like Cr and Pb into foods (Collado-López et al., 2022; Kamerud et al., 2013).

6.3. HM detection and monitoring

A variety of techniques are used to detect heavy metals in foods. Traditional methods include inductively coupled plasma mass spectrometry (ICP-MS), ICP optical emission spectroscopy (OES), atomic absorption spectrometry (AAS), atomic fluorescence spectrometry (AFS), X-ray absorption spectroscopy (XAS), X-ray fluorescence spectrometry (XRF), laser ablation ICP-MS (LA-ICP-MS), and non-invasive micro-test technology (NMT) (Yang, Tan, et al., 2022; He et al., 2024). These methods are highly selective and capable of detecting multiple heavy metal ions simultaneously, but they are complex, require expensive equipment, and demand skilled operators (Yu et al., 2021). They are not ideal for rapid or on-site detection of trace metal ions in foods. To address these limitations, newer techniques have been developed, including electrochemical methods with Metal-Organic Frameworks (MOFs) and MXenes (Zheng et al., 2024; Pan et al., 2024), colorimetric methods using metal nanoparticles and Nanozymes (Sharifi et al., 2022), and fluorescence methods employing semiconductor quantum dots, carbon nanomaterials, and metal nanoparticles (Chen et al., 2022). These advanced methods often offer simpler operation, higher sensitivity, and equivalent accuracy compared to traditional techniques (Lim et al., 2021; Si et al., 2024).

The detection of concerning levels of toxic HMs in several baby food products suggests that widespread metal contamination may be a major concern for infants and toddlers. Non-governmental organizations have been contributing to ensure that food products, particularly those intended for infants, toddlers, and teenagers, are tested for HM presence (Parker et al., 2022). Surveys conducted by multiple governments (Food and Drug Administration, FDA and European Union, EU) and non-governmental organizations have reported on the presence of Pb and As in baby food brands (Bair, 2022; Parker et al., 2022). Rice, an accumulator of As and Cd, is the main ingredient of baby food formulations. In a survey, 75% of rice-based baby products contained As levels higher than 100 μg/kg inorganic As, the maximum recommended level by the European Union (Gu et al., 2020). Recent Congressional Reports have strongly recommended food processing industries test finished products instead of raw ingredients for HM content. The increasing use of nanotechnology and its integration with sensors/biosensors strategies have led to the fabrication of portable instruments for detecting HM in foods. Many sensors designed for detecting trace heavy metal ions have primarily been used with simple samples such as drinking water rather than complex food matrices. This limitation arises because complex food matrices contain various interfering substances that can affect the accuracy of the sensing system. To overcome this, it is crucial to enhance not only the sensitivity but also the anti-interference and selectivity of these sensors to make them suitable for detecting trace heavy metal ions in diverse food products. Additionally, most existing sensors are capable of detecting only one or a few heavy metal ions at a time. There is a need for sensors that can simultaneously detect multiple heavy metal ions. Future advancements in sensing arrays and the application of deep learning algorithms are expected to enable the sensitive and accurate detection of multiple heavy metal ions in high-throughput settings.

6.4. Regulatory standards for HM

The Agency for Toxic Substances and Disease Registry (ATSDR) and the US Environmental Protection Agency (EPA) collaborate to assess, address, and evaluate the health risks related to known HMs in the environment. To ensure food safety, the US Food and Drug Administration (FDA) have been regulating the maximum permissible concentration of HM in food products. Governmental programs have prioritized the monitoring and reduction of As, Pb, Hg, and Cd in food. An FAO/WHO joint committee set a maximum tolerable daily intake (TDI) based on average adult body weight at 50 μg/kg for As, 1.0 μg/kg for Cd, 3.6 μg/kg for Pb, and 0.7 μg/kg for Hg (Jallad, 2015). However, a wide range of standards exist for maximum HM content in drinking water and food as set by different agencies (Table 1) (Bair, 2022; Karim et al., 2023). Based on the risk assessment studies, the FAO and WHO have established an international set of guidelines for HMs in food i.e., CODEX Alimentarius or ‘Food Code’, to protect consumer health (CODEX Alimentarius, 2023). As per the ‘Food Code’, As should not be found above 0.1 mg/kg in edible fats and oils, 10 μg/L in mineral water, 0.2 mg/kg in polished rice, 0.35 mg/kg in husked rice, 0.5 mg/kg in salt. Cd should be limited to 0.2 mg/kg in wheat and leafy vegetables, 0.1 mg/kg in pulses, 0.4 mg/kg in polished rice, and 0.003 μg/L in mineral water. For Pb, 0.05 mg/kg is permitted in fruiting vegetables, 0.02 mg/L in milk, and 0.01 mg/kg in infant food, 0.1 mg/kg in oils and fats, 1 mg/kg in salt. While Hg is limited to 1.0 μg/L in mineral water, 0.1 mg/kg in salt (Scutarașu & Trincă, 2023).

Table 1.

Government proposed and existing standard concentrations for maximum toxic metal content in food and water.

Agencya	Standards for maximum HM content
	Drinking water	Baby food	Adult food
FAO	10 μg/L As; 5.0 μg/L Pb; 3.0 μg/L Cd; 1.0 μg/L Hg	100 μg/kg As; 10 μg/kg Pb	0.1 mg/kg As
EPA	10 μg/L As; 15 μg/L Pb; 5.0 μg/L Cd, 2.0 μg/L Hg	NA	NA
WHO	10 μg/L As; 3.0 μg/L Cd; 50 μg/L Cr; 1.0 μg/L Hg; 50 μg/L Pb	NA	NA
EU	10 μg/L As	0.02 mg/kg Pb	NA
EC	NA	0.1 mg/kg As	0.2 mg/kg As

^aFAO: Food and Drug Administration; EPA: Environmental Protection Agency; WHO: World Health Organization; EU: European Union; EC: European Commission (Bair, 2022; CODEX Alimentarius, 2023; Karim et al., 2023).

However, the regulatory standards are variable across different countries. For instance, in Australia, the current guideline for As in rice 1.0 mg/kg, which is higher than the standards of FAO/WHO, i.e., 0.3 mg/kg. However, there are no set federal standards or specific guidelines pertaining to HM in baby foods, considering the higher vulnerability of the infant population (Gu et al., 2020). In 2021, the US FDA released the Closer to Zero (C2Z) action plan for foods consumed by infants and young children, which aims to monitor and reduce toxic element exposure through food to the lowest possible concentration (Flannery & Middleton, 2022). In 2022, as a stepwise part of the C2Z action plan, the FDA lowered its interim reference levels (IRLs) for Pb in food to 2.2 μg/day for children and 8.8 μg/day for females of childbearing age which are much lower than the harmful blood level reference value (BLRV) as per Center for Disease Control and Prevention (CDC) guidelines. Updated and global standard guidelines should be imposed by CODEX Committee on Contaminants in Food (CCCF), taking into account the risk evaluation for different populations.

7. Conclusions

HM contamination can exceed than the permissible limit in raw agricultural commodities, processed food products, and drinking water and is therefore a rising concern for food safety. Human exposure to such hazardous elements is inevitable but their direct ingestion can be effectively prevented by controlling their uptake by food crops from contaminated soil, remediating contaminated agricultural soils, and enforcing global regulatory standards. This USDA-NIFA workshop highlighted several significant knowledge gaps regarding the farm-to-fork-to-human continuum. The molecular mechanisms underlying the accumulation of concerned elements like Pb, Cr, and Hg in plants are only partially understood and the successful application of current knowledge to engineer safer food crops is limited. More focused research is needed to understand metal uptake mechanisms in concerned crops to breed or engineer safer varieties. In addition, uncoupling the mechanisms for nutrient and HM uptake should be prioritized to prevent unforeseen repercussions on food/nutrition quality, such as eliminating high nutritional value or reducing essential elements while lowering toxic constituents. Modern remediation strategies such as microbial remediation, phytoremediation, soil amendments, CRISPR/Cas9 engineered crops, etc. have gained attention and have been progressively evaluated over the last two decades, but their practical implementation at the field level is still often uneconomical. It is abundantly clear that many of the knowledge gaps limiting the prevention of HM transfer from soil-to-plant-to-food commodities are interdisciplinary, meaning that a system-level approach will be necessary for successful solutions to this complex issue. For example, use of advanced biosensor technologies in food industries can limit the post-harvest HM contamination. It is incumbent on funding agencies to supply greater center-level resources to design programs that can effectively investigate and understand the complex and dynamic relationships between soil biogeochemistry, the microbiome, plant tolerance and accumulation strategies, and the changing climate. Considering the extensive global import/export of agricultural and food products, uniform standards for acceptable and safe toxic element levels in food and water need to be established and enforced by international, national, and regional regulatory bodies. The FAO’s Closer-to-Zero (C2Z) approach offers a suitable framework to support the efforts to understand and prevent toxic metal contamination of food. However, this initiative cannot succeed without public awareness of the risks and levels of safe exposure, particularly to sensitive or disadvantaged populations.

Data availability

No data was used for the research described in the article.