The Impacts of Elevated CO₂ Levels on Environmental Risk of Heavy Metal Pollution in Agricultural Soils: Applicable Remediation Approaches for Integrated Benefits

Abstract

Heavy metal pollution in agricultural fields is a serious health concern because of the high bioavailability and persistent toxicity of heavy metals. Much progress has recently been made with respect to elucidating the impacts of climate change (e.g., elevated atmospheric CO₂ concentrations) on the environmental behavior of heavy metal pollutants and the associated ecological and health risks. The microbiological responses to elevated CO₂ levels are primarily mediated by the C balance in agricultural activities; however, the underlying mechanisms involved in plant–soil–microbe interactions under heavy metal stress are still unclear. Thus, in this study, the challenges and perspectives with regard to controlling heavy metal pollution and optimizing crop yields while reducing greenhouse emissions in agricultural ecosystems responsive to elevated CO₂ levels are discussed. Considering the integrated benefits of intensive agriculture and food security under a future changing climate, the summarized findings provided in this study may help to develop applicable remediation approaches for sustainably managing heavy metal polluted soils.

1. Introduction

Soil is the largest organic carbon (C) reservoir in terrestrial ecosystems and plays a key role in regulating the global carbon cycle and atmospheric CO₂ concentrations. The carbon stock in soil is approximately three times that of the vegetation carbon pool and twice that of the stock of carbon in the atmosphere [1]. Soil is also a source and a sink of trace greenhouse gases (GHG), such as CH₄ and N₂O, in the atmosphere [2]. As an important source of global GHG emissions, agricultural activities account for 1.4–1.7 Gt of CO₂-Ce emissions per year (on average) and 10–12% of total anthropogenic GHG emissions [3]. Thus, any minor changes in soil environments will greatly affect C and N transformations in agricultural ecosystems, bringing consequences of uncertain impacts on food security and environmental sustainability in a changing climate.

The global food and agricultural industries are challenged by various issues, the most important of which concerns enhancing soil productivity such that it meets the food demand of an increasing global population. In agriculture, the pollution of the environment with heavy metals is unambiguously becoming a widely common problem for food safety [4,5,6]. Heavy metal pollution predominantly occurs as compound pollution stemming from many complex sources, often involving more than one metal. Soils are the main sink for contaminants, and heavy metals are highly likely to accumulate in areas of anthropogenic influence, such as areas of agricultural intensification [7,8]. In particular, heavy metals can enter the human body through the soil–crop–food chain [9,10], thereby threatening human health globally.

2. Impacts of Elevated CO₂ Levels on the Environmental Behavior of Heavy Metal Pollutants

The trend of global climate change is persistent and seemingly inevitable [11]. The atmospheric CO₂ level has risen from ~ 280 ppm in preindustrial times to the current level of ~400 ppm. The latest Six Assessment Report of the Intergovernmental Panel on Climate Change (IPCC AR6) shows that the atmospheric CO₂ level will likely reach 600 ppm by the end of this century [12]. Soil pH influences the chemical properties and mobility of heavy metals in agricultural soils. Excess heavy metals can also decrease the uptake of macro- and micronutrients by plants [13]. Previous studies have shown that the combined impacts of elevated CO₂ concentrations and heavy metal pollution can affect crop quality [14,15,16] and increase the bioavailability of heavy metals via lowering soil pH [17,18].

Recent research has demonstrated that elevated CO₂ levels can lead to higher concentrations of dissolved As in soil pore water [19]. Elevated CO₂ levels can also increase Cd retention in amorphous Fe oxides in soils while promoting the binding of Cd to low-crystalline Fe fractions deposited on surfaces of roots [20]. Plants have evolved various resistance mechanisms to alleviate the toxicity of heavy metals, but the detrimental impacts of these metals on plant growth are observed even at low concentrations [21]. Moreover, rising CO₂ concentrations have also been reported to dramatically alter plant–soil feedback (i.e., root secretion processes) and soil fertility maintenance (i.e., soil organic C dynamics) [22,23,24], which may influence the capacity of croplands to produce sufficient amounts of food [25].

As one of the most toxic heavy metals, Cd mainly accumulates in crop grains via the root uptake pathway. Evidence shows that about 15% of soil Cd can enter into rice grains, and up to 3.19% can be transferred from rice grains to the human body [26]. In one study, it was shown that under conditions of elevated CO₂ levels, the accumulation of Cd and Pb in rice grains increased by 48.4–75.4% and 20.5–39.1%, respectively [18]. These serious impacts of elevated CO₂ levels on the mobilization, bioavailability, and accumulation of heavy metals in agricultural soils will greatly increase the risk of consuming heavy metals via crop grains (Figure 1).

3. The Applicable Approaches for Mitigating Heavy Metal Accumulation in Crop Grains

The mobilization and bioavailability of heavy metals in soils significantly affect such metals’ uptake and accumulation in plant roots, leaves, and crop grains, precipitating a collective impact on food security and human health risk. Therefore, it is critical to reduce the heavy metal content in crop plants in order to mitigate risks under elevated CO₂ conditions. In general, the applicable remediation approaches for heavy metal pollution in soils mainly include physical, chemical, and bio-remediation; additionally, photocatalytic applications have recently been used for the highly reactive degradation of organic pollutants [27,28]. Previous reviews have summarized several existing cost-effective management options for mitigating heavy metal accumulation in agricultural soils, including chemical remediation via the use of soil amendments (e.g., biochar, compost/plant residues, and liming materials), co-planting with hyperaccumulators, and water/fertilization management in heavy metal polluted paddy fields [29,30].

Recent studies suggest that managing well-cultivated crops is a promising method for developing climate-smart and productivity-sufficient agriculture ecosystems [31,32,33]. Generally, sustainable yield improvements for staple crops should be achieved without concomitantly lowering food quality and increasing GHG emissions or depleting soil fertility. To achieve this goal in heavy metal polluted soils, for example, weakly accumulative cultivars of crops can potentially decrease the phyto-availability of soil heavy metals in agriculture [34,35,36]. The incorporation of biochar and crop residues (e.g., wheat/maize straw) into soils is a well-known agricultural practice used to enhance soil fertility [37,38]. The combination of biochar and zerovalent iron (ZVI) as a soil ameliorant can effectively immobilize Cd in the soil, but it can also enhance Fe and Zn accumulation in rice grain by 11% and 8%, respectively [39]. In anaerobic environments, such as submerged paddy soils, there are significant differences among rice cultivars in terms of grain Pb content [40]. Under elevated CO₂ conditions, Indica rice has a higher yield response (20.4%) than Japonica rice (12.7%) [41]. Thus, the management of cultivars with low accumulation and high CO₂ responses constitutes an attractive potential method of achieving low accumulation in grains without reducing yields.

Soil microorganisms inhabit the rhizosphere of crop plants, which can play a key role in mediating nutrient cycling (e.g., nitrogen fixation and phosphorus solubilization) and improving tolerance to stress (e.g., drought, pathogen infection, and hazardous contamination). Microbial remediation has recently attracted interest because many soil microbes are tolerant of heavy metals, leading to a reduction in the content of heavy metals in soils through the following main mechanisms: biosorption, bioaccumulation, complexation, and biomineralization [42,43,44,45,46]. It should be noted that the application of microbial remediation holds enormous potential to mitigate heavy metals due to its high efficiency, cost-effectiveness, eco-friendliness, etc. However, short-term or long-term exposure to heavy metals may inhibit microbial activity, specifically via causing changes in microbial biomass carbon, basal respiration, and metabolic entropy (qCO₂) [47,48,49]. Previous studies have demonstrated that the selective inhibition of N₂O reductase can enhance N₂O production in soil polluted with heavy metals, which may have consequences relating to the contribution of agriculture to the accumulation of atmospheric N₂O concentrations [50,51]. It has been confirmed that the presence of heavy metals can precipitate a decrease in microbial abundance and diversity, leading to altered community structures [46]. Evidence also shows that heavy metal pollution can inhibit CO₂ emission but enhance CH₄ emission [52,53]. Therefore, trade-offs relating to the application of microbial remediation approaches are expected in intensive agriculture due to the insidious effects of heavy metal pollution on specific microbial communities, ultimately influencing C/N cycling and GHG emissions (Figure 2).

4. Perspectives

Agricultural intensification is a globally common practice for increasing food production using limited sources (e.g., water, fertilizer, and energy). The increase in atmospheric CO₂ concentrations directly affects plant photosynthesis, water utilization, and nutrient uptake [54,55,56]. Numerous studies have highlighted the positive/negative effects of ‘CO₂ fertilization’ on plant growth and crop productivity in intensive agriculture. However, there are few systematic assessments of the impacts of environmental pollution and climate change (i.e., elevated CO₂ concentrations and global warming) on plant physiological responses, root traits, and microbial dynamics in plant–soil systems.

Regarding plant–soil-systems-based investigations, isotope tracing is commonly used to estimate photosynthetic C assimilation and belowground C allocation. Nevertheless, commercial ¹³CO₂ isotope labeling for an entire growth period is costly. It is also limited by the availability of appropriate equipment (i.e., gas-tight plant growth chambers) providing well-controlled, continuous, near-natural conditions. In this regard, we highlight one research priority that needs to be addressed to improve our understanding of the impact of well-cultivated crop management on heavy metal translocation in plant–soil systems. The presence of heavy metals may change the patterns of new C proportions allocated to root, soil, and microbial metabolism. Therefore, it is critical to explore the potential of elevated CO₂-driven C newly allocated to belowground locations in heavy metal polluted soils.

An increasing content of heavy metals is being found—and being found to be persistent—in agricultural soils due to chemical fertilizer usage, livestock manure and sludge application, sewage irrigation, and atmospheric deposition [57,58,59]. Thus, it is essential to prevent and control the release of heavy metals into the soil environment and ensure the sustainability of agricultural systems. Nevertheless, various remediation strategies have been reported, such as phytoremediation [60,61], the use of soil amendments [62,63,64], specific microbial communities-driven remediation [65], and combined remediation approaches [66] to address the potential environmental risks posed by heavy metals in intensive agriculture.

Generally, soil microbes play a vital role in the decomposition of SOC, thus influencing GHG fluxes [67,68]. Evidence shows that the microbial degradation of plant litter and residues in warming soils can release more CO₂ back into the atmosphere [69]. Potential CO₂ release, however, may also be stimulated by plant–soil interactions and their associated microbes responsive to agricultural management practices [70,71]. Dark CO₂ fixation (the non-phototrophic assimilation of CO₂) by specific microbial communities can recycle some of the released soil CO₂ [72]. However, there is still a gap with respect to evaluating the contribution of dark CO₂ fixation by microbes, especially in soils contaminated with single or multiple pollutants (e.g., heavy metals, organic pollutants, antibiotic residues, and antibiotic resistance genes).

Additionally, with respect to the application of microbial remediation in heavy metal polluted soils, it is imperative to optimize the microbe-mediated C management strategy and improve agricultural resilience to the changing climate, ultimately contributing to global C neutralization. With the collective impacts of elevated CO₂ levels and heavy metal pollution on agricultural productivity, more attempts are needed to regulate the allocation of photosynthates to optimize plant–soil–microbe interactions. Moreover, the underlying mechanism linking microbe-mediated C balance and the environmental behavior of soil pollutants is also poorly understood. Thus far, it is still challenging to decipher the plant–soil–microbe interactions in soils polluted by heavy metals in the background of future changing CO₂ concentrations.

5. Conclusions

Agricultural soil pollution via heavy metals poses one of the biggest challenges to food safety and sustainability, particularly with respect to staple crops. Elevated CO₂ concentrations may aggravate the impacts of heavy metal pollution on the plant–soil–microbe interactions in agricultural systems. This study demonstrates the impacts of elevated CO₂ levels on the mobilization, bioavailability, and accumulation of heavy metals in agricultural soils. To minimize the human health risks related to the dietary intake of accumulated heavy metals from crop grains, in this study, we have summarized alternative options for effective remediation strategies, such as cultivar management and the application of soil ameliorants and microbial community-driven remediation approaches in intensive agriculture. We suggest that there is a need to develop and manage well-cultivated crops with genetic features enabling low accumulation. Selective cultivars (e.g., low-Cd rice varieties) with high yields that are responsive to elevated CO₂ levels, if harnessed appropriately, can provide sustainable yield improvements for staple crops. Considering the integrated benefits of intensive agriculture and food security in the background of a future changing climate, our findings may help to develop climate-smart and productivity-sufficient agriculture ecosystems.