Heavy Metals in Bioenergy Crop Production, Biomass Quality, and Biorefinery: Global Impacts and Sustainable Management Strategies

Abstract

Heavy metals (HMs) including cadmium (Cd), lead (Pb), arsenic (As), zinc (Zn), copper (Cu), chromium (Cr), and nickel (Ni) pose significant challenges to bioenergy crop production due to their persistence, toxicity, and bioaccumulation in soils and plants. This study not only summarizes the mechanisms of HM absorption, translocation, and accumulation in bioenergy crops, but also critically assesses their impact on crop development, biomass quality, and biorefinery processes. Heavy metals disrupt key physiological processes and modify lignocellulosic composition, which is important for biofuel and biogas production. Global soil contamination from sources like industrial emissions, mining, and agricultural activities exacerbates these problems, posing a threat to both energy security and environmental sustainability. Sustainable management strategies, including phytoremediation, microbial bioremediation, soil amendments, and genetic engineering, are explored to mitigate HM effects while enhancing crop resilience. This review emphasizes the importance of integrating techniques to balance bioenergy production with environmental and human health and safety, including the use of HM-tolerant crop varieties, enhanced biorefinery processes, and robust policy frameworks. Future research should focus on developing scalable remediation technologies and interdisciplinary solutions that align with the United Nations’ Sustainable Development Goals and meet global bioenergy needs.

1. Introduction

The global shift toward renewable energy has positioned bioenergy crops as key contributors to sustainable energy systems [1]. Species such as miscanthus (Miscanthus spp.), switchgrass (Panicum virgatum L.), giant reed (Arundo donax), willow (Salix spp.), and jatropha (Jatropha curcas) are valued for their high biomass yields, adaptability to marginal lands, and low input requirements [2,3,4,5,6,7]. However, heavy metal (HM) pollution in soils due to mining, industrial emissions, and waste disposal, along with certain agricultural practices, threatens the sustainability of bioenergy crop production. Heavy metals, including Cd, Pb, As, Zn, Cr, and Ni, are non-biodegradable, persist in soil, and bioaccumulate in plant tissues, posing risks to crop growth, biomass quality, and biorefinery efficiency (Figure 1) [8,9,10,11].

Agricultural soils in regions such as China, India, Europe, and the United States have been contaminated with HMs [12]. In China, Cd and Pb contamination have been reported to limit land availability for crops, including bioenergy crops [13]. These contaminants disrupt soil microbial activity, nutrient cycling, and plant physiology, reducing ecosystem services and posing health risks through food chain transfer [14,15,16]. Bioenergy crops, which often grow on marginal or contaminated land to prevent competition with food crops, are particularly susceptible to HM stress, necessitating a thorough analysis of their interactions and effects. Crops, particularly bioenergy crops, take up HMs, which can impact plant growth, development, harvestable biomass, and biomass quality, with implications for biorefinery processes. It is worth mentioning that certain heavy metals such as Zn and Cu at optimum concentrations could benefit crop growth and support the yield potential of crops including bioenergy crops.

High HM concentrations in feedstock can contaminate bioenergy products, inhibit enzymatic and microbial processes, and generate toxic residues, complicating waste management [17]. For instance, Ni-contaminated soil can reduce switchgrass yield by up to 55% [18] and thus bioethanol production, which is related to the amount of biomass generated. Due to these risks, regulatory frameworks such as the European Union’s Renewable Energy Directive (RED II) and US EPA guidelines impose strict limits on HM levels in bioenergy feedstocks, emphasizing the importance of sustainable management [19]. Heavy metal accumulation in plant tissues can lead to environmental and health risks through food chain transfer, occupational exposure, and environmental release, underscoring the importance of United Nations Sustainable Development Goal (SDG) 3 (Good Health and Well-being) and in line with SDG 7 (Affordable and Clean Energy) and SDG 15 (Life on Land). This review provides a comprehensive examination of the interactions between HMs and bioenergy crops, focusing on uptake and translocation mechanisms, their effects on plant performance and biomass quality, and the implications for biorefinery efficiency. It also explores sustainable management strategies such as phytoremediation, microbial remediation, nanotechnology, soil amendments, and genetic engineering aimed at mitigating HM-induced stress.

2. Mechanisms of Heavy Metal Uptake and Translocation in Bioenergy Crops

2.1. Soil–Plant Interactions

The bioavailability of HMs in soil is governed by physicochemical properties, including pH, organic matter (OM) content, cation exchange capacity (CEC), and redox potential [20]. Acidic soils (pH < 6) increase the solubility of Cd, Pb, and Zn, enhancing their uptake by plant roots [21]. Conversely, alkaline soils promote the precipitation or complexation of many HMs with carbonates, reducing bioavailability. Organic matter, such as humic and fulvic acids, can mobilize HMs by forming soluble complexes or immobilize them through adsorption, depending on other soil conditions [22]. For example, in high-OM soils, it is expected that Cd bioavailability decreases but As mobility increases as OM increases due to competition with phosphate ions [23,24].

Root exudates, including carboxylates (e.g., citrate, oxalate), amino acids, and sugars, play a critical role in HM mobilization. These compounds chelate HMs, increasing their solubility and facilitating uptake. In switchgrass, citrate exudates enhance Cd and Zn uptake by forming stable complexes, with uptake rates increasing by 25% in acidic soils [8]. Similarly, amino acids such as serine (for Cd), threonine (for Cr), and lysine and arginine (for Ni) enhance HM mobilization through chelation [25,26,27]. Soil microbial communities also influence HM bioavailability through processes like methylation (e.g., As to monomethylarsonic acid), oxidation (e.g., As(III) to As(V)) or reduction (e.g., Cr(VI) to Cr(III)), altering toxicity and plant uptake potential [28,29].

2.2. Uptake and Translocation Mechanisms

HMs enter plant roots via passive diffusion, facilitated diffusion, or active transport mediated by metal transporters. The ZIP (Zn/Fe permease) family of proteins mediates Cd and Zn uptake, while phosphate transporters facilitate As uptake due to its chemical similarity to phosphate [30,31]. In Arundo donax, Cd is absorbed via ZIP transporters and translocated to shoots via xylem, driven by transpiration, with concentrations reaching 15 mg/kg in leaves under high soil levels [32]. Willow exhibits hyperaccumulation, with Cd and Zn accumulating to about 1000 mg/kg for Zn and 70 mg/kg for Cd, while only exhibiting mild phytotoxicity symptoms for excess Zn. This makes willow suitable for phytoextraction but challenging for bioenergy crop production due to contaminated biomass issues [33].

Plants employ chelation and sequestration to mitigate HM toxicity. Metallothioneins and phytochelatins, cysteine-rich peptides, bind HMs and sequester them in vacuoles, reducing cytosolic toxicity. In bioenergy crops, phytochelatin synthase genes are upregulated under heavy metal stress, enhancing metal sequestration and limiting translocation to photosynthetic tissues [34]. However, these mechanisms increase HM content in harvestable biomass, affecting biorefinery processes. When switchgrass is grown on Pb contaminated soil, the presence of HMs reduces the energy return on investment (EROI) for the biorefinery system from 2.54 to 1.53 due to additional energy required for metal removal, precipitation, and disposal [35].

2.3. Physiological and Biochemical Responses

Heavy metals trigger oxidative stress in plants by generating reactive oxygen species (ROS), which damage cellular components such as lipids, proteins, and DNA. To mitigate this, plants activate antioxidant defense systems, including enzymes like superoxide dismutase, catalase, and ascorbate peroxidase to neutralize ROS. For example, exposure to metals like Zn or Cd enhances antioxidant enzyme activity in various plant species, but high HM concentrations can overwhelm these defenses, leading to cellular damage and reduced growth [36,37].

Heavy metals disrupt plant photosynthesis by inhibiting chlorophyll synthesis, damaging photosystem II, and impairing electron transport, leading to reduced photosynthetic efficiency. HMs also compete with essential nutrients such as Ca and Fe, causing deficiencies that manifest as chlorosis. Furthermore, HM stress influences gene expression by activating genes involved in metal detoxification and antioxidant production, diverting resources away from developmental activities. These consequences have been observed across many plant species exposed to metals such as Cd, Pb, or Ni [38].

While it is well established that excessive concentrations of HMs are toxic to plants, certain HMs such as Zn and Cu are essential micronutrients with key functions in plant physiology when present at low to moderate levels (

Table 1. Zinc (Zn) and copper (Cu) thresholds in soil and plants.

Metal	Growth Medium/Tissue	Deficient/Minimum Adequate	Adequate/Normal Range	Excess/Toxic Threshold	Remarks	Reference
Zn	Leaf tissue (µg g−1 dry weight)	<20–30	30–100	200–300	Zn is the least toxic HM; essential for enzymes and auxin metabolism	[40]
	Soil (mg kg−1)	~6–20	20–80	>100	Soil adsorption is moderate; tolerance higher than that to Cu
Cu	Leaf tissue (µg g−1 dry weight)	<5	5–20	>20–30	Narrower range than Zn; deficiency more common	[41]
	Soil (mg kg−1)	~6–20	20–80	20–100	Cu is highly bioavailable; toxicity impacts roots/photosynthesis

). Zinc is a structural or catalytic cofactor for a large number of enzymes, including those involved in protein synthesis, auxin metabolism, and antioxidant defense, and it contributes to membrane stability and chlorophyll production [39]. Copper is also essential for crop growth as it impacts photosynthetic electron transport (plastocyanin), cell wall lignification (as a cofactor for polyphenol oxidases), and oxidative stress mitigation [39].

2.4. Species-Specific Responses

Bioenergy crops display diverse physiological and anatomical adaptations to HM stress, influencing their suitability for cultivation on contaminated soils. Some species act as excluders, limiting metal translocation to shoots, others as hyperaccumulators, concentrating metals in above-ground biomass. For instance, miscanthus tolerates metals like Cd and Zn by sequestering them in roots, limiting translocation to shoots, and thereby preserving biomass quality for bioenergy use. In contrast, switchgrass has low tolerance to As, often exhibiting reduced growth in contaminated soils, which can compromise biomass yield and phytoremediation efficiency [42].

Other species like willow and Arundo donax act as hyperaccumulators, effectively extracting HMs which promotes phytoremediation but accumulates high metal concentrations in biomass, which can complicate biorefinery processes. Similarly, jatropha shows tolerance to Ni, but its accumulation in tissues may negatively affect biodiesel quality [43]. Understanding these species-specific HM tolerance and accumulation issues, as well as the tradeoffs between metal uptake and biomass quality, is essential for selecting appropriate crops for phytoremediation and bioenergy production on contaminated lands.

3. Impacts of Heavy Metals on Bioenergy Crop Production

3.1. Growth and Yield Reduction

Heavy metals impair plant root development, nutrient assimilation, and water uptake, leading to stunted growth and reduced biomass yield. In switchgrass, Cd exposure inhibits root elongation by disrupting cell division, resulting in decreased biomass accumulation in contaminated soils [44]. Miscanthus shows similar effects under Pb and As stress, with reductions in shoot growth and tiller density [42]. Willow exhibits relative tolerance to Zn and Cu due to its deep root system and ability to sequester metals, though high concentrations can still reduce yields [45]. These species-specific responses highlight the importance of selecting suitable bioenergy crops for areas contaminated with HMs. HM-induced oxidative stress disrupts plant metabolic processes, including carbohydrate synthesis and protein metabolism, which limits energy allocation and growth. In Arundo donax, As exposure impairs enzymes involved in starch synthesis, reducing growth potential [42]. Ni stress inhibits chlorophyll production, gas exchange, and nutrient uptake in Jatropha curcas, resulting in reduced biomass and seed yields. The reduction in reproductive output not only reduces the total amount of oil available for biodiesel synthesis but also alters its quality, reducing the overall efficiency and viability of the biofuel system (Table 2) [43].

Seasonal variability in soil properties, particularly during wet seasons, has, been reported to increase HM bioavailability due to soil saturation and redox changes, resulting in decreased crop yields, including those from bioenergy crops [46]. Interestingly, miscanthus and switchgrass grown on soils with Pb, Cd and Zn concentrations exceeding threshold limits have produced comparable biomass yield to those from uncontaminated land (Table 2) [47]. However, mixed results across the study sites highlight the need for site-specific trails. Understanding the interactions between plant metabolic responses and environmental factors such as climate, soil type, and seasonal variability are essential for the potential production of bioenergy crops on contaminated soils.

3.2. Soil Health and Microbial Interactions

Heavy metals disrupt soil microbial communities, reducing populations of microbes responsible for nutrient cycling, OM decomposition, and plant growth promotion. A comprehensive meta-analysis showed that heavy metal pollution reduces bacterial abundance by ~38%, fungal abundance by ~18%, microbial biomass carbon by ~42%, and dehydrogenase enzyme activity by ~66% [48]. Long-term field studies further reveal that chronic Pb and Cd contamination shifts microbial community structure, altering bacteria and fungi diversity and accelerating SOC loss by up to ~13% [49]. Many arbuscular mycorrhizal fungi (AMF), which facilitate phosphorus uptake and enhance root function, are impaired under heavy metal stress. In one study at Zn–Pb mining sites, increasing HM levels were consistently associated with declines in both AMF abundance and enzymatic activities in situ [50]. Soil enzymes crucial for nutrient cycling such as dehydrogenase, urease, and phosphatase are particularly sensitive. Moreno et al. [51] demonstrated that soils with higher carbon content buffer the impact of HMs on enzymes but nonetheless show meaningful decreases in urease and dehydrogenase activity under Cd and Zn exposure. Furthermore, chronic heavy metal exposure is linked with reduced soil organic carbon storage due to accelerated microbial respiration and altered community composition. Heavy metals, as mentioned in previous sections, can negatively influence carbon inputs due to reductions in energy crop yields leading to less carbon addition to soil, thus reducing carbon storage/increase over time. It is also important to mention that building and protecting soil carbon requires improved soil structure [52,53,54], which is facilitated by fungi such as AMF. The effect of heavy metals on soil microorganisms involved in many physical and chemical characteristics of soils depends on a combination of factors including quantity of pollutants, soil type, temperature, water content in soil, pH, soil mineralogy, and others, making these interactions complex [55].

3.3. Global and Regional Impacts

Heavy metal contamination poses a significant barrier to sustainable bioenergy production, especially in industrial and agriculturally intensive regions worldwide. Globally, an estimated 14–17% of cropland is contaminated with HMs like As, Cd, Pb, and Cr, threatening suitable land for bioenergy crops [56]. In China, about 19% of agricultural soils exceed national HM safety limits, which constrains large-scale crop production, including bioenergy crops [57]. Many post-mining areas in Europe are now used for willow production, especially in soils contaminated with HMs, to bioremediate the HMs and improve soil fertility [58]. Lynch and Satrio [35] conducted a life cycle analysis under controlled conditions, showing that it took 3.5 years to reduce Pb levels from 120 to 10 mg/kg through switchgrass-based phytoremediation. These HM-impacted lands threaten energy security by reducing available arable land for biofuel crops and degrading ecosystem services such as carbon sequestration and biodiversity [59,60]. Addressing HM contamination is essential for expanding bioenergy production without undermining sustainability goals.

3.4. Socioeconomic Implications

The productivity and economic benefits of bioenergy crops can be optimized with appropriate site-specific choices [61]. HM contamination in agricultural soils is a factor that may increase production costs for farmers. They are likely to experience lower yields and require soil remediation. In developing regions, smallholder farmers cultivating bioenergy crops on contaminated lands may face significant economic losses, which could limit their adoption of these crops [62]. On the other hand, bioenergy crops like cassava can be used for phytoremediation of HM-contaminated lands, potentially offering economic benefits through biomass production for bioenergy [63]. In industrialized nations, such as those in the European Union, regulatory compliance with strict sustainability criteria for bioenergy, which include limits on heavy metals in biomass, seems to increase processing costs, thereby potentially affecting the economic viability of bioenergy systems.

4. Impacts of Heavy Metals on Biomass Quality and Biorefineries

4.1. Lignocellulosic Composition

The lignocellulosic structure of bioenergy crops, consisting of cellulose, hemicellulose, and lignin, is essential for efficient biofuel production [64,65]. Heavy metals, such as Cd and Pb, can disrupt this composition, compromising biomass quality and downstream processing. For example, Cd stress in miscanthus reduces cellulose content while increasing lignin accumulation, which impedes enzymatic hydrolysis during bioethanol production (Table 2) [66]. This effect stems from heavy metal ions interfering with cellulose synthase enzymes at the plasma membrane, disrupting cellulose synthesis. Similarly, Cd exposure in certain maize hybrids decreases cellulose content, altering cell wall properties [67].

Heavy metal stress often triggers adaptive changes in cell wall composition as a defense mechanism. These changes can include increased lignin or pectin content, which may indirectly affect cellulose levels and biomass digestibility. For instance, Pb treatment can thicken cell walls in some species, potentially increasing cellulose deposition but reducing cell wall extensibility, which complicates biomass processing [68]. These alterations in lignocellulosic balance reduce biofuel production efficiency by increasing resistance to enzymatic breakdown, resulting in lower yields and higher processing costs.

4.2. Contaminant Transfer to Biomass

Heavy metals accumulate in biomass, posing risks to biorefinery processes and product safety. In Arundo donax, Cd and As accumulation in shoots can contaminate bioenergy feedstocks and impact biorefinery processes [32]. Heavy metals can be transferred during the valorization of contaminated biomass, compromising product quality and safety and posing significant challenges to achieving cleaner production and environmentally sustainable disposal of contaminated biomass [69]. Lignin, the non-fermentable component of lignocellulosic biomass, is a primary factor contributing to the challenging thermal decomposition of woody biomass across a wide temperature range (160–900 °C). Lignin preferentially binds Pb and Zn compared to cellulose, leading to reduced biofuel production efficiency [70].

Beyond contaminating biomass, HMs can benefit or interfere with different stages of biorefinery processes [71]. For instance, in a review article, Guo et al. [71] reported that trace amounts of several heavy metals including Cu, Fe, Ni, Cd, and Zn can enhance biogas production in the anaerobic digestion process. These trace elements could act as cofactors boosting cellulase activities, leading to greater methanogen growth [72]. In contrast, high levels of these HMs can disrupt protein structures, inhibit enzyme function, and thus decrease anaerobic digestion processes including hydrolysis and acidification, leading to reduced biogas production.

Extending beyond biochemical pathways, HMs undergo significant redistribution during thermochemical conversion. Volatile metals such as Cd and Pb readily migrate into bio-oil and syngas, lowering product quality and raising risks of secondary environmental contamination. Less volatile metals including Cr and Ni tend to remain concentrated in biochar, complicating its safe use as a soil amendment. Furthermore, transition metals such as Cu, Ni, and Zn may act as unintended catalysts, altering pyrolysis and gasification pathways and ultimately influencing both the yield and composition of biofuels [73]. These effects are particularly pronounced in lignin-rich biomass, where strong metal binding amplifies contaminant transfer, exacerbating efficiency losses in biofuel production. Collectively, this evidence highlights that contaminant transfer from biomass to energy products is a critical barrier to sustainable biorefinery operations, underscoring the need for mitigation strategies such as pretreatment, controlled combustion, or immobilization techniques to reduce heavy metal mobility [73].

4.3. Quality Standards and Safety

Biomass with elevated HM levels can fail to meet regulatory standards for bioenergy applications, leading to increased costs and reduced marketability. In the European Union, the Renewable Energy Directive II (RED II) does not explicitly set HM feedstock limits in biofuels; instead, member states and EU regulators rely on derived sustainability criteria and mass balance systems to ensure biomass quality [19]. Although RED II focuses on greenhouse gas savings and sourcing criteria, it encourages monitoring of contaminants in feedstocks through delegated acts and MS level controls. These measures effectively discourage the use of contaminated biomass by linking sustainability certification to feedstock quality [74].

In the United States, EPA regulations under 40 CFR Part 503 establish limits for HMs in biosolids and digestate used as soil amendments [75]. For example, biosolids applied to land must not exceed ceiling concentrations such as Cd ≤ 85 mg/kg, Pb ≤ 840 mg/kg, etc. Although these standards pertain to digestate rather than fuel-grade biomass, they highlight regulatory concern over HM residues in agricultural and energy crops.

Biomass exceeding HM thresholds is often declassified, reducing its market value and requiring additional processing such as contaminant removal or blending to meet emission and ash content standards for combustion or anaerobic digestion. Beyond compliance, even HM concentrations below regulatory ceilings can compromise biorefinery performance. For instance, Cd and Cr significantly inhibited biogas production during anaerobic digestion, causing a marked decrease in both methane yield and volatile organic matter removal [76]. Similarly, Cd contamination in maize reduced shoot and root biomass, with direct implications for feedstock availability and energy output [77].

Overall, these findings indicate that regulatory frameworks serve a dual role: they safeguard environmental and health standards while also indirectly protecting biorefinery performance by discouraging contaminated feedstocks. Adhering to HM standards is therefore critical for maintaining reliable conversion efficiency, minimizing processing disruptions and ensuring safer management of byproducts.

4.4. Impacts on Biorefinery Processes

Heavy metals affect multiple biorefinery processes, including enzymatic saccharification, fermentation, anaerobic digestion, and thermochemical conversion, reducing yields and increasing operational costs.

4.4.1. Bioethanol Production

Second-generation biofuels, derived from lignocellulosic biomass, are valued for their potential to deliver sustainable energy with positive environmental, economic, and social impacts [78,79,80]. The four basic stages of converting lignocellulosic biomass into ethanol are pretreatment, enzymatic hydrolysis, fermentation, and distillation [80,81]. Pretreatment is crucial because it makes biomass components more accessible for subsequent hydrolysis and fermentation. The inherent recalcitrance of lignocellulosic biomass, driven by its complex matrix of lignin, hemicellulose, and highly crystalline cellulose, poses a significant challenge to efficient ethanol production [82,83]. Among pretreatment techniques, steam explosion is widely recognized for its ability to increase the surface area available for enzymatic action, thereby facilitating hydrolysis [80,83].

Heavy metals in biomass can inhibit enzymatic saccharification and fermentation, reducing the bioethanol yields. However, the impact varies markedly across different metals. Ko et al. [84] reported that when napier grass (Pennisetum purpureum) was grown in HM-contaminated soil, the hydrolysis efficiency of Zn-polluted biomass was ~90%, while Cd reduced it to 77% compared to the control. However, Cr had no negative effect, highlighting the complex influence of heavy metals on bioethanol production.

The inhibitory effects of HMs are even more pronounced during fermentation, where Saccharomyces cerevisiae is highly sensitive to HM stress. Cd levels above 50 mg/L can reduce ethanol yields by 25% [85], while Pb at similar concentrations slows fermentation by extending the lag phase and reducing growth [86]. Copper toxicity is also common at >30 mg/L, and fermentation often becomes sluggish or stuck, with reduced alcohol production and yeast viability [87,88]. Together, these effects lower ethanol yields and often require mitigation strategies such as detoxification pretreatments or the use of metal-tolerant yeast strains, each of which increases processing complexity and costs.

Apart from reducing yield, HMs accelerate catalyst deactivation (loss of catalyst effectiveness to support a chemical reaction over time), promote fouling (blocking the active sites of the catalyst) and scaling in boilers (formation of a hard, mineral-based deposit on the inner surfaces of the boiler tubes and other components) and heat exchangers, and intensify corrosion in reactors and pipelines. These raise maintenance costs, place infrastructure under pressure, and reduce processing efficiency. Mitigation options include feedstock blending to dilute metal loadings, detoxification via acid or water leaching or sorbents, and the use of HM-tolerant microbes [89,90]. Circular approaches that recover HMs from digestates or ash further mitigate risks while adding value [91]. Integrating these measures into biorefinery design is essential to protect infrastructure, sustain efficiency, and ensure regulatory compliance.

4.4.2. Biodiesel and Biogas Production

Heavy metals exert profound effects on anaerobic digestion—a critical process in converting organic biomass (including energy crops and oilseeds used for biodiesel) into biogas and digestate byproducts. These effects are of particular concern in biodiesel systems where digesters are integrated into closed-loop waste-to-energy operations or coupled with oil-extracting crops grown on marginal lands [92].

Heavy metals are known to inhibit both acidogenesis and methanogenesis—two central microbial stages in anaerobic digestion. Methanogens, essential for biogas and biodiesel co-product generation (e.g., methane-rich gas from press cake), are especially sensitive to metals. The order of toxicity observed in methanogens is often Zn > Ni > Cu > Cr > Cd > Pb. Acidogenic bacteria show slightly more resistance, but metals such as Cd and Cu still substantially inhibit volatile fatty acid production at high concentrations of these metals [93].

At the biochemical level, HMs impair microbial function by (i) binding to enzyme thiol groups and replacing cofactors in prosthetic enzyme sites, disrupting energy generation in methanogens; and (ii) causing oxidative stress and altering microbial metabolic pathways critical to hydrolysis and fatty acid conversion [92]. Also, different metals exert unique effects based on solubility, oxidation state, and interaction with other ions or OM. For example, Cd and Cr exhibit toxicity at very low concentrations, with Cd particularly lethal to methanogenic activity even at 1–5 mg/L. Iron may be beneficial at lower levels (up to 8.1 mmol/L), enhancing substrate utilization and granule formation in digesters; however, excess Fe precipitates can inhibit microbial activity. Mixtures of metals (e.g., Cr–Cd–Pb) could have synergistic inhabitation effects that are stronger than individual metals [93,94]. Heavy metal interactions with biomass production, quality, and biorefinery processes are summarized in Table 2.

Table 2. Impact of heavy metals on biomass yield, quality, and biorefinery value of second-generation bioenergy crops.

Heavy Metal	Observed Impact (Biomass Yield, Quality and Biorefinery)	Energy Crop	Heavy Metal Concentration (mg/kg)	Effect Category	Country	Reference
Cd, Pb, Zn	Reduced macronutrient status, notably N and K drought-induced senescence. Compromised mineral nutrition and yield stability.	Miscanthus × giganteus, Spartina pectinata	Cd: 20.6–21.1 (M. × giganteus), 13.6–14.0 (S. pectinata); Pb: 532–535 (M. × giganteus), 363–373 (S. pectinata); Zn: elevated, strongly influenced by fertilization.	Negative	Poland	[95]
Cu, Zn, Pb, Cd	HMs reduced shoot and root biomass.	Sorghum, Maize	Cd: 1.8; Cu: 75; Zn: 50–75; Pb: 85–130.	Negative	Nigeria	[96]
Cd, Pb, Cu, Zn, Cr	HM-contaminated biomass reduced the quality of biorefinery products.	Bioenergy crops	Maize: Cu 327–338, Pb 340, Zn 365–384; Willow: Zn 822–4636, Cd 40–80, Cu 11–15, Pb 14–26; Arundo: Cd 5–16, Cu 5–6, Pb 17–27.	Negative	China or Global	[69,97]
As Pb, Sb	Significant reduction in biomass yield; compromised biomass quality and biorefinery efficiency.	Miscanthus × giganteus	As 1700–83,000; Pb < 500–15,200; Sb 18–27. Plant: roots 602–1285 As, 38–327 Pb, 18–27 Sb; shoots 4–17 As, 1–43 Pb, 0.2–1.1 Sb.	Negative	France	[98]
Cd, Pb, Zn	Significant increase in biomass when remediated with mycorrhizal fungi.	Miscanthus × giganteus	Cd 12–15, Pb 675–815, Zn 819–1081. Roots accumulated much more than shoots.	Positive	France	[99]
Cd, Pb, Zn, Cu, Ni	M. × giganteus and S. pectinata: high yield, unaffected by contamination; P. virgatum: low yield, high metal uptake.	Miscanthus × giganteus, Spartina pectinata, Panicum virgatum	Cd 23–27; Pb 621–720; Zn 2590–3312.	Negative to Neutral	Poland	[47,100]
As, B, Cd, Cr, Cu, Pb, Hg, Ni, Zn	Miscanthus and willow showed poor yields; switchgrass failed to establish, and reed canary grass grew well with consistent high yields.	Miscanthus sp., willow, switchgrass, and reed canary grass	As: 145; B: 54; Cd: 5.5; Cr: 117; Cu: 229; Pb: 701; Hg: 2.7; Ni: 52; Zn: 3890.	Negative and Positive	England	[101]
Pb	The presence of HMs reduced the efficiency of the biorefinery system.	Switchgrass	120 (initial), reduced to 10 after 3.5 years	Negative	USA	[35]
Cd, Pb	Significant reduction in biomass yield.	Switchgrass	Cd: 30–110.46; Pb: 400–1204.6	Negative	China	[44]
Cd, Cr, Cu, Ni, Zn	High Cd and Zn caused severe leaf chlorosis; Cd, Cu, and Ni caused significant biomass reduction; Cd stress reduced photosynthesis.	Jatropha curcas	Cd: 11.2; Cu: 6.35; Ni: 5.9; Zn: 654; Cr: 5.2.	Negative	Japan	[43]
Cd	Cd reduced total biomass, hastened leaf senescence, reduced root length, and increased root diameter.	Miscanthus sinensis	Cd: 62–86.	Negative	Italy	[102]
Cd, Zn, Pb	Phytoattenuation of maize resulted in minimal removal of Cd and Pb, while Zn removal was significant.	Maize	Cd: 2; Pb: 9–10; Zn: 450–550.	Negative	Belgium and The Netherlands	[103]
Cd, Hg	Slight reduction in yield; low Cd and Hg in biomass; suitable for phytostabilization and biofuel.	Miscanthus × giganteus	Cd: 6.76; Hg: 0.109.	Positive and Negative	Croatia	[104]
Cd	Increased lignin accumulation; reduced bioethanol production.	Miscanthus sp.	Cd: 100.	Negative	China	[66]
Cd, Cr, Cu, Mn, Ni, Pb, Zn	HMs have no negative impact on biomass yield, and their concentration in ash remains below threshold limits.	Arundo donax and Phragmites australis	Arundo: Cd: 0.06–1.76; Cr: 1.56–4.96; Cu: 25–121; Mn: 62–94; Ni: 5–11; Pb: 0.31–1.76; Zn: 24–180. Cd < 0.10; Cr 0.15–0.08; Cu 2.60–1.12; Mn 23.0–5.65; Ni 3.98–1.27; Pb 5.82–3.61; Zn 10.2–6.32.	Positive	Italy	[105,106]
Cd, Pb, Zn	Biomass retained thermal quality; Miscanthus and Spartina suited for combined phytoremediation and energy use.	Miscanthus × giganteus, Spartina pectinata, Sida hermaphrodita, Panicum virgatum	Not specified.	Positive	Poland	[107]
Pb	Increased biomass under Pb stress by limiting translocation to shoots.	Salix matsudana	Pb: 9000–27,600.	Positive	China	[108]
Fe, As, Cr, Cu, Mn, Ni, Pb, Zn	Biomass unaffected by HM contamination under in vitro conditions.	Arundo donax	Cr: 100; Cd: 500 (lethal at 1000); Cu: 3000; Ni: 280; Pb: 270.	Neutral	Spain	[109]
Cd, Zn	High biomass production; suitable for bioenergy production.	Pennisetum purpureum, Arundo donax, Miscanthus sp., Panicum virgatum	Cd: 1.6–47; Zn: 2000.	Positive	China	[110]
Cd, Zn, Pb	Biomass is unaffected by HM contamination.	Miscanthus × giganteus	Cd: 1.8–1.9; Zn: 6.9–62.9; Pb: 0.6–10.6.	Neutral	Germany	[111]
Cd, Pb, Cu, Zn, Ni, As	Significant reduction in biomass yield.	Miscanthus × giganteus	Cd: 2.1–2.2; Ni: 2.9–3.2; Zn: 206–241; Pb: 4.7–4.9; Cu: 8.7–9.6; Cr: 4–5; As: 6.1–8.1.	Negative	Belgium	[112]
Zn	Biomass yield and tolerance varied by genotype; some were tolerant while others were sensitive.	Miscanthus sp., Arundo donax	Not specified.	Positive and Negative	Italy	[113]

Table 2. Impact of heavy metals on biomass yield, quality, and biorefinery value of second-generation bioenergy crops.

Heavy Metal	Observed Impact (Biomass Yield, Quality and Biorefinery)	Energy Crop	Heavy Metal Concentration (mg/kg)	Effect Category	Country	Reference
Cd, Pb, Zn	Reduced macronutrient status, notably N and K drought-induced senescence. Compromised mineral nutrition and yield stability.	Miscanthus × giganteus, Spartina pectinata	Cd: 20.6–21.1 (M. × giganteus), 13.6–14.0 (S. pectinata); Pb: 532–535 (M. × giganteus), 363–373 (S. pectinata); Zn: elevated, strongly influenced by fertilization.	Negative	Poland	[95]
Cu, Zn, Pb, Cd	HMs reduced shoot and root biomass.	Sorghum, Maize	Cd: 1.8; Cu: 75; Zn: 50–75; Pb: 85–130.	Negative	Nigeria	[96]
Cd, Pb, Cu, Zn, Cr	HM-contaminated biomass reduced the quality of biorefinery products.	Bioenergy crops	Maize: Cu 327–338, Pb 340, Zn 365–384; Willow: Zn 822–4636, Cd 40–80, Cu 11–15, Pb 14–26; Arundo: Cd 5–16, Cu 5–6, Pb 17–27.	Negative	China or Global	[69,97]
As Pb, Sb	Significant reduction in biomass yield; compromised biomass quality and biorefinery efficiency.	Miscanthus × giganteus	As 1700–83,000; Pb < 500–15,200; Sb 18–27. Plant: roots 602–1285 As, 38–327 Pb, 18–27 Sb; shoots 4–17 As, 1–43 Pb, 0.2–1.1 Sb.	Negative	France	[98]
Cd, Pb, Zn	Significant increase in biomass when remediated with mycorrhizal fungi.	Miscanthus × giganteus	Cd 12–15, Pb 675–815, Zn 819–1081. Roots accumulated much more than shoots.	Positive	France	[99]
Cd, Pb, Zn, Cu, Ni	M. × giganteus and S. pectinata: high yield, unaffected by contamination; P. virgatum: low yield, high metal uptake.	Miscanthus × giganteus, Spartina pectinata, Panicum virgatum	Cd 23–27; Pb 621–720; Zn 2590–3312.	Negative to Neutral	Poland	[47,100]
As, B, Cd, Cr, Cu, Pb, Hg, Ni, Zn	Miscanthus and willow showed poor yields; switchgrass failed to establish, and reed canary grass grew well with consistent high yields.	Miscanthus sp., willow, switchgrass, and reed canary grass	As: 145; B: 54; Cd: 5.5; Cr: 117; Cu: 229; Pb: 701; Hg: 2.7; Ni: 52; Zn: 3890.	Negative and Positive	England	[101]
Pb	The presence of HMs reduced the efficiency of the biorefinery system.	Switchgrass	120 (initial), reduced to 10 after 3.5 years	Negative	USA	[35]
Cd, Pb	Significant reduction in biomass yield.	Switchgrass	Cd: 30–110.46; Pb: 400–1204.6	Negative	China	[44]
Cd, Cr, Cu, Ni, Zn	High Cd and Zn caused severe leaf chlorosis; Cd, Cu, and Ni caused significant biomass reduction; Cd stress reduced photosynthesis.	Jatropha curcas	Cd: 11.2; Cu: 6.35; Ni: 5.9; Zn: 654; Cr: 5.2.	Negative	Japan	[43]
Cd	Cd reduced total biomass, hastened leaf senescence, reduced root length, and increased root diameter.	Miscanthus sinensis	Cd: 62–86.	Negative	Italy	[102]
Cd, Zn, Pb	Phytoattenuation of maize resulted in minimal removal of Cd and Pb, while Zn removal was significant.	Maize	Cd: 2; Pb: 9–10; Zn: 450–550.	Negative	Belgium and The Netherlands	[103]
Cd, Hg	Slight reduction in yield; low Cd and Hg in biomass; suitable for phytostabilization and biofuel.	Miscanthus × giganteus	Cd: 6.76; Hg: 0.109.	Positive and Negative	Croatia	[104]
Cd	Increased lignin accumulation; reduced bioethanol production.	Miscanthus sp.	Cd: 100.	Negative	China	[66]
Cd, Cr, Cu, Mn, Ni, Pb, Zn	HMs have no negative impact on biomass yield, and their concentration in ash remains below threshold limits.	Arundo donax and Phragmites australis	Arundo: Cd: 0.06–1.76; Cr: 1.56–4.96; Cu: 25–121; Mn: 62–94; Ni: 5–11; Pb: 0.31–1.76; Zn: 24–180. Cd < 0.10; Cr 0.15–0.08; Cu 2.60–1.12; Mn 23.0–5.65; Ni 3.98–1.27; Pb 5.82–3.61; Zn 10.2–6.32.	Positive	Italy	[105,106]
Cd, Pb, Zn	Biomass retained thermal quality; Miscanthus and Spartina suited for combined phytoremediation and energy use.	Miscanthus × giganteus, Spartina pectinata, Sida hermaphrodita, Panicum virgatum	Not specified.	Positive	Poland	[107]
Pb	Increased biomass under Pb stress by limiting translocation to shoots.	Salix matsudana	Pb: 9000–27,600.	Positive	China	[108]
Fe, As, Cr, Cu, Mn, Ni, Pb, Zn	Biomass unaffected by HM contamination under in vitro conditions.	Arundo donax	Cr: 100; Cd: 500 (lethal at 1000); Cu: 3000; Ni: 280; Pb: 270.	Neutral	Spain	[109]
Cd, Zn	High biomass production; suitable for bioenergy production.	Pennisetum purpureum, Arundo donax, Miscanthus sp., Panicum virgatum	Cd: 1.6–47; Zn: 2000.	Positive	China	[110]
Cd, Zn, Pb	Biomass is unaffected by HM contamination.	Miscanthus × giganteus	Cd: 1.8–1.9; Zn: 6.9–62.9; Pb: 0.6–10.6.	Neutral	Germany	[111]
Cd, Pb, Cu, Zn, Ni, As	Significant reduction in biomass yield.	Miscanthus × giganteus	Cd: 2.1–2.2; Ni: 2.9–3.2; Zn: 206–241; Pb: 4.7–4.9; Cu: 8.7–9.6; Cr: 4–5; As: 6.1–8.1.	Negative	Belgium	[112]
Zn	Biomass yield and tolerance varied by genotype; some were tolerant while others were sensitive.	Miscanthus sp., Arundo donax	Not specified.	Positive and Negative	Italy	[113]

5. Environmental and Health Risks

Heavy metal-contaminated biomass poses risks to environmental and human health.

5.1. Atmospheric Emissions

During thermochemical processes like combustion, pyrolysis, or gasification, HMs in biomass can volatilize, contributing to air pollution [114,115] and ultimately to soil pollution. Mercury is particularly volatile and is emitted as elemental (Hg⁰) and oxidized (HgCl₂) forms. In municipal solid waste incinerators in Taiwan, oxidized mercury (Hg²⁺) accounted for 80–97% of Hg emissions captured by air pollution control systems (APC), decreasing to 75–80% post-APC, indicating that oxidized Hg is more effectively captured than other forms of Hg [116]. Atmospheric emissions of HMs are linked to respiratory disorders, cardiovascular diseases, and neurological impairments [16,117]. Lead exposure through inhalation is linked to cognitive deficits in children, with chronic exposure levels above 0.1 µg/m³ exceeding WHO safety thresholds [118].

5.2. Ecological Impacts

Heavy metals from sources like industrial emissions, smelting, and agricultural inputs (e.g., fertilizers, pesticides [9,11]) contaminate soil and water, posing severe ecological risks and threatening sustainable crop production [119]. These non-biodegradable pollutants persist in ecosystems, disrupting soil fertility, water quality, and biodiversity, with cascading effects on food chains and ecosystem services.

Heavy metals accumulate in soil surface layers, altering physicochemical properties and impairing ecosystem functions. Cadmium and Pb, for instance, reduce soil microbial diversity and activity, disrupting OM decomposition and nutrient cycling [120]. Li et al. [119] also reported that Cd in Chinese agricultural soils resulted in a significant decrease in microbial biomass, compromising soil health. Elrys et al. [121] found that Cd significantly reduced microbial biomass carbon and N. This reduction was associated with direct suppression of microbial growth and activity due to high Cd levels in the soil. Heavy metals also bind to soil particles, reducing the bioavailability of essential nutrients (e.g., N, P), stunting plant growth, and lowering productivity [122]. This often exacerbates under soil pH that is more acidic. In addition, ions in the soil can prevent uptake of other ions with similar chemical behaviors though a process called antagonism. Common antagonisms associated with HMs include As antagonizing the uptake of P, Cu antagonizing the uptake of Ca, Fe, Mn, and Zn, Sr antagonizing the uptake of Ca, and Zn antagonizing the uptake of Fe, Mg, and Mn [123].

Ecologically, HM-contaminated soils harm soil fauna, such as earthworms and nematodes, which are vital for soil aeration and nutrient cycling [124]. A study by Nahmani et al. [125] found that Pb concentrations above 100 mg/kg reduced earthworm populations by up to 50%, disrupting soil structure and ecosystem stability. These effects ripple through trophic levels, as HM accumulation in soil organisms transfers to predators, amplifying toxicity in food webs. For example, Cd bioaccumulation in insects can reduce bird populations, threatening biodiversity [126]. Such ecological disruptions undermine the sustainability of agricultural systems reliant on healthy soils for crop production, including bioenergy crops.

Heavy metal contamination of water occurs via runoff, leaching, and atmospheric deposition from contaminated soils or thermochemical processes (e.g., combustion, pyrolysis). Hou et al. [127] documented Cd leaching from Chinese farmland soils into nearby streams, threatening aquatic ecosystems. Mercury and As bioaccumulate in fish and algae, impairing reproduction and growth. High Hg concentrations can substantially reduce fish fertility, disrupting aquatic food webs [128]. Cadmium and Pb toxicity in phytoplankton reduces primary productivity, affecting higher trophic levels, including amphibians and waterfowl [129]. These disruptions destabilize wetland ecosystems, which are critical for water purification and biodiversity. Moreover, HM-contaminated water used in agriculture perpetuates a cycle of soil and crop contamination, threatening long-term bioenergy production.

5.3. Human Health Consequences

According to Lal et al. [130], soil contamination with HMs poses severe health risks, particularly in vulnerable populations through exposure to water, air, and food. There are occupational exposure pathways for farmers and workers involved in managing bioenergy crops in HM-contaminated soils. One of the most common ways people are exposed to HMs is through inhalation. Heavy metals can enter farmers’ or workers’ bodies through dust inhalation as fine particulate-bonded metals when, for example, soils are tilled or biomass is chopped. Heavy metals can also enter the food chain via crops and biofuel byproducts grown with contaminated soil and water [15,131]. The relative toxicity of HMs to humans is determined by their concentration, emission rate, and duration of exposure, and follows the general order Hg > Cd > Cu > Zn > Ni > Pb > Cr > Al > Co [132] (

Table 3. Heavy metals and their impacts on human health.

Heavy Metal	Major Health Effects	Reference
Mercury (Hg)	Skin lesions, hyperkeratosis, cancers, cardiovascular disease, diabetes.	[135]
Cadmium (Cd)	Respiratory damage, lung cancer, bone disorders, metabolic diseases.	[118,135,136]
Copper (Cu)	Gastrointestinal distress, liver and kidney problems, neurogenerative disorders.	[137]
Zinc (Zn)	Immune dysfunction, impaired copper absorption, neurological issues.	[137]
Nickel (Ni)	Dermatitis, respiratory cancers, cardiovascular effects.	[136]
Lead (Pb)	Neurotoxicity, hypertension, cancer, reproductive toxicity.	[133,136]
Chromium (Cr)	Lung cancer, nasal perforation, skin irritation, DNA damage.	[135]
Aluminum (Al)	Neurotoxicity, bone disorders, lung fibrosis, dialysis encephalopathy.	[138]
Cobalt (Co)	Cardiomyopathy, lung disease, thyroid dysfunction, neurotoxicity.	[137]

). Contact through skin is another exposure pathway to HMs, especially while handling contaminated soil, plant tissues, or residues with no or inadequate protective equipment. Ingestion of contaminated materials can also occur. Processing stages such as combustion, gasification, etc., can release airborne HM particles that could create respiratory issues and severe human health problems. In particular, three metals, Hg, Cd, and Pb, have attracted increased attention in recent decades due to their persistence and harmful effects on human health. Cadmium accumulation in crops grown on HM-contaminated soils is linked to kidney damage and bone disorders, with dietary intake above 0.025 mg/kg body weight/day exceeding safety thresholds [118]. Lead and As exposure through contaminated water or food increases the risk of cardiovascular diseases and cancers, respectively [133]. Vulnerable populations, including children and agricultural workers, face heightened risks near bioenergy facilities processing HM-contaminated biomass [134].

Mitigation strategies can often reduce human health risks by decreasing exposure to HM contamination. These include mechanized handling to reduce dust generation, local exhaust ventilation in processing facilities, personal protective equipment such as respirators and gloves, and regular occupational health monitoring for workers in high-exposure settings. All of these measures, collectively, should allow for a safer work environment while reducing health risks associated with HM-contaminated products.

6. Sustainable Management Strategies

6.1. Phytoremediation

Biofuel crops offer several advantages over conventional plants in phytoremediation (Table 4). First, many species, such as miscanthus, switchgrass, sunflower (Helianthus annuus), and giant reed exhibit strong tolerance to heavy metals (HMs) and produce high biomass under stressful conditions [34]. Second, they are often non-edible, which avoids introducing contaminants into the food chain [139]. Third, utilizing contaminated or marginal lands that would not support good food crop yields for energy crop cultivation alleviates land competition with food crops and creates value from otherwise degraded landscapes [139,140,141]. Fourth, energy crops have shown the potential to maintain or improve soil health [142,143], which can assist with future crop production in reclaimed soils. However, careful handling and processing of biomass is essential to prevent the re-entry of metals into the environment and food chain.

Biofuel crops engage in several key phytoremediation mechanisms including (i) phytoextraction, (ii) phytostabilization, (iii) phytovolatilization, and (iv) rhizofiltration [144]. Phytoextraction involves the uptake of heavy metals into plants’ above-ground tissues (e.g., Cd and Zn in Cannabis sativa). Phytostabilization refers to the immobilization or binding of heavy metals in roots or the surrounding rhizosphere. This prevents the spread of heavy metals in the soil. Phytovolatilization allows plants to convert certain heavy metals like As and Hg into volatile forms which then are released into the atmosphere. Rhizofiltration refers to the absorption and concentration of contaminants (in this case heavy metals) from water via roots, often seen in water hyacinth (Eichhornia crassipes). Among these mechanisms, phytoextraction and phytostabilization are the most widely adopted strategies for successful phytoremediation [145]. The phytoremediation potential of bioenergy crops is summarized in Table 4.

Table 4. Phytoremediation potential of bioenergy crops on heavy metal-contaminated soils.

Heavy Metals	Phytoremediation Potential	Heavy Metal Concentration (mg/kg)	Energy Crops	Country	Reference
Cd	High phytoextraction potential under well-drained conditions; phytostabilization under flooded conditions.	Cd: 63–159	Salix sps. Willow	China	[146]
Zn, Cu, Cd	Removed Zn, Cu, and Cd; suitable for bioenergy.	Zn: 24.0–121.0; Cu: 4.4–11.0; Cd: 0.02–0.35.	Arundo donax	Italy	[105]
Cd, Al	Suitable for phytoremediation-accumulated Cd and Al in two years.	Al: 10.4–116; Cd: 0.55–8.9.	Populus sps.	Belgium	[147]
Cd, Zn, V, Pb, Cu, Ni, Sb, Mn, As, Th, Hg, Sn, Cr, Co, Al	Miscanthus giganteus: High biomass; multi-HM removal. Phalaris arundinacea: Moderate biomass; effective HM uptake.	Cd: 0.094–0.211; Pb: 1.06–1.81; Cu: 2.73–9.89; Zn: 36.9–61.9; Mn: 10.0–32.5; Cr: 1.21–1.82; Ni: 0.021–0.036; As: 0.003–0.005; Co: 0.0023–0.0058; Hg: 0.087–0.163.	Miscanthus giganteus Phalaris arundinacea	Ukraine	[148]
Cd, Cr, Cu, Pb, Hg, Ni, Zn	Arundo donax—Accumulates Cd, Cr, and Cu; strong phytoextraction and rhizofiltration. Miscanthus × giganteus—Zn accumulator; suited for marginal soils. Panicum virgatum-Cd removal; Cr phytoextraction. Pennisetum purpureum—Similar to P. virgatum; efficient in Cr rhizofiltration. Sida hermaphrodita—Strong accumulator of Cd, Ni, Pb, and Zn. Sorghum x drummondii—Mycorrhizal-assisted HM uptake.	Not specified.	Arundo donax, Miscanthus × giganteus, Panicum virgatum, Pennisetum purpureum, Sida hermaphrodita and Sorghum × drummondii	Croatia	[149]
Zn, Pb, Cr	Suitable for phytostabilization.	Not specified.	Miscanthus sps. and Arundo donax	Italy	[150]
Zn, Cr	High Zn and Cr tolerance and uptake.	Zn: 1105; Cr: 348.	Arundo donax, Miscanthus sacchariflorus	China	[151]
Cd, Ni, Zn	Year 1: high Cd, Zn, and Ni; declines in year 2; potential for phytoextraction.	Cd: 0.35; Ni: 5.0; Zn: 123.	Miscanthus × giganteus, Phalaris arundinacea	Poland	[152]
Cu, Ni, Zn	Zn stabilization or extraction; low Cu or Ni potential.	Cu: 43; Ni: 126; Zn: 1385.	Miscanthus × giganteus, Spartina pectinata	Poland	[153]
Cr, Zn, Cu, Ni	Phytoremediation potential of HMs: Cr > Zn > Cu > Ni.	Cr: 250; Zn: 1616; Cu: 223; Ni: 75.	Salix schwerinii	Finland	[154]
Cd, Zn, Cu	Salix clones showed higher potential than willow clones.	Willow: Cd: 6.8; Zn = 909; Cu = 17.7.	Clones of willow and poplar trees	Czech Republic	[155]
		Populus: Cd: 2.06; Zn: 463, Cu: 11.8.
Cd	Enhanced Cd phytoextraction through synergistic inoculation with Cd-tolerant Bacillus spp. and arbuscular mycorrhizae.	Cd: 2.3.	Arundo donax	India	[156]

Table 4. Phytoremediation potential of bioenergy crops on heavy metal-contaminated soils.

Heavy Metals	Phytoremediation Potential	Heavy Metal Concentration (mg/kg)	Energy Crops	Country	Reference
Cd	High phytoextraction potential under well-drained conditions; phytostabilization under flooded conditions.	Cd: 63–159	Salix sps. Willow	China	[146]
Zn, Cu, Cd	Removed Zn, Cu, and Cd; suitable for bioenergy.	Zn: 24.0–121.0; Cu: 4.4–11.0; Cd: 0.02–0.35.	Arundo donax	Italy	[105]
Cd, Al	Suitable for phytoremediation-accumulated Cd and Al in two years.	Al: 10.4–116; Cd: 0.55–8.9.	Populus sps.	Belgium	[147]
Cd, Zn, V, Pb, Cu, Ni, Sb, Mn, As, Th, Hg, Sn, Cr, Co, Al	Miscanthus giganteus: High biomass; multi-HM removal. Phalaris arundinacea: Moderate biomass; effective HM uptake.	Cd: 0.094–0.211; Pb: 1.06–1.81; Cu: 2.73–9.89; Zn: 36.9–61.9; Mn: 10.0–32.5; Cr: 1.21–1.82; Ni: 0.021–0.036; As: 0.003–0.005; Co: 0.0023–0.0058; Hg: 0.087–0.163.	Miscanthus giganteus Phalaris arundinacea	Ukraine	[148]
Cd, Cr, Cu, Pb, Hg, Ni, Zn	Arundo donax—Accumulates Cd, Cr, and Cu; strong phytoextraction and rhizofiltration. Miscanthus × giganteus—Zn accumulator; suited for marginal soils. Panicum virgatum-Cd removal; Cr phytoextraction. Pennisetum purpureum—Similar to P. virgatum; efficient in Cr rhizofiltration. Sida hermaphrodita—Strong accumulator of Cd, Ni, Pb, and Zn. Sorghum x drummondii—Mycorrhizal-assisted HM uptake.	Not specified.	Arundo donax, Miscanthus × giganteus, Panicum virgatum, Pennisetum purpureum, Sida hermaphrodita and Sorghum × drummondii	Croatia	[149]
Zn, Pb, Cr	Suitable for phytostabilization.	Not specified.	Miscanthus sps. and Arundo donax	Italy	[150]
Zn, Cr	High Zn and Cr tolerance and uptake.	Zn: 1105; Cr: 348.	Arundo donax, Miscanthus sacchariflorus	China	[151]
Cd, Ni, Zn	Year 1: high Cd, Zn, and Ni; declines in year 2; potential for phytoextraction.	Cd: 0.35; Ni: 5.0; Zn: 123.	Miscanthus × giganteus, Phalaris arundinacea	Poland	[152]
Cu, Ni, Zn	Zn stabilization or extraction; low Cu or Ni potential.	Cu: 43; Ni: 126; Zn: 1385.	Miscanthus × giganteus, Spartina pectinata	Poland	[153]
Cr, Zn, Cu, Ni	Phytoremediation potential of HMs: Cr > Zn > Cu > Ni.	Cr: 250; Zn: 1616; Cu: 223; Ni: 75.	Salix schwerinii	Finland	[154]
Cd, Zn, Cu	Salix clones showed higher potential than willow clones.	Willow: Cd: 6.8; Zn = 909; Cu = 17.7.	Clones of willow and poplar trees	Czech Republic	[155]
		Populus: Cd: 2.06; Zn: 463, Cu: 11.8.
Cd	Enhanced Cd phytoextraction through synergistic inoculation with Cd-tolerant Bacillus spp. and arbuscular mycorrhizae.	Cd: 2.3.	Arundo donax	India	[156]

6.2. Microbial Bioremediation

Microbial bioremediation is a promising eco-friendly strategy for decreasing the toxicity of HMs in polluted soil and water. Microorganisms, including bacteria, fungi, algae, and actinomycetes, possess diverse metabolic and enzymatic capabilities that enable them to immobilize, transform, or extract HMs from the environment. This process plays a pivotal role in restoring contaminated ecosystems, particularly when paired with sustainable practices such as bioenergy crop cultivation [34,157]. Microbes mitigate HM toxicity through a variety of mechanisms: biosorption, bioaccumulation, biotransformation, precipitation, and efflux pumping [157,158,159,160]. The ability of organisms to accumulate, use, and eliminate HMs depends on pH, moisture, and temperature [161]

Biosorption refers to the passive binding of metals to microbial cell walls or extracellular polymeric substances (EPSs). This process often involves carboxyl, hydroxyl, and phosphate functional groups. Dead microbial biomass, particularly from fungi like Aspergillus niger and Rhizopus arrhizus, has demonstrated high metal affinity and is extensively studied for Cd, Pb, and Cu removal [157]. Bioaccumulation involves the active transport of metals into the microbial cytoplasm, where they are sequestered or transformed into less toxic forms. Biotransformation, especially redox conversions, allows microbes to decrease the toxicity of metals by altering their valence state (oxidation status; loss of electron), for example, reducing Cr(VI) to Cr(III) or U(VI) to U(IV) via dissimilatory metal reduction by Geobacter spp. [162]. EPSs significantly enhance metal binding and make these metals unavailable (immobilization). EPSs produced from Bacillus subtilis and Pseudomonas putida have been shown to facilitate the removal of Cu(II) from a solution by forming insoluble or semi-insoluble complexes that precipitate out, a process called micro-precipitation [163]. Several native microbes show effective HM resistance and removal capabilities. Two main bacteria species that are great at remediating HMs include Pseudomonas aeruginosa and Bacillus spp. Pseudomonas aeruginosa is known for its ability to remediate Cd, Zn, Ni, Hg, and Pb from various sources [164]. It is also capable of producing EPSs, which can help in the sequestration of HM ions. Bacillus spp. have been studied for their capacity to remediate Cd, Zn, Ni, Hg, and Pb. This genus uses strategies such as biosorption, EPS-mediated biosorption (binding metals to cell surfaces), bioaccumulation (actively taking up heavy metals into their cells), or bioprecipitation (form insoluble metal complexes) to reduce heavy metal contamination. Two main fungi that are often used in remediating HMs are Rhizopus arrhizus and Aspergillus niger. These are commonly studied for their remediation of Cd, Zn, Ni, Hg, and Pb. Fungi possess cell walls rich in functional groups like carboxyl, hydroxyl, and amine groups that can bind metal ions through mechanisms such as ionic exchange (swapping metal ions with other cations), complexation (forming coordination complexes with metal ions), and chelation (binding metals tightly with multiple molecular sites) [157,165,166].

Two other effective strategies are bioaugmentation and biostimulation. Bioaugmentation involves the introduction of microbial strains resistant to HMs into contaminated environments to enhance degradation efficacy. This is especially advantageous in situations where native microbial communities lack the metabolic capacity to detoxify specific chemicals. On the other hand, biostimulation enhances indigenous microbial activity through the addition of nutrients, electron donors/acceptors, or organic substrates like molasses or vegetable oil [157]. These strategies are increasingly applied to contaminated groundwater and soils, particularly where multi-metal contamination or complex organo-metal compounds are present.

6.3. Soil Amendments

Amendments such as biochar, lime, compost, gypsum, and phosphorus can reduce HM bioavailability. The advantage of using organic amendments such as compost, lime, and gypsum is that they are relatively inexpensive and facilitate the revegetation of contaminated soils. Biochar is a carbon-rich substance generated through the pyrolysis of organic residues such as straw, manure, and wood in an oxygen-restricted environment [167,168,169]. Biochar increases soil pH and adsorbs HMs, decreasing Cd uptake by crops [170]. Lime also increases soil pH and, since many HMs are most available when pH < 6, it significantly reduces HM availability and thus the absorption of HMs by crops. For example, switchgrass responded positively to an increase in soil pH caused by liming, with limited HM accumulation in its tissues [171,172]. Manure and compost can also increase soil pH, especially if they are rich in calcium carbonate [141,173]. Manure and compost, however, also have all sorts of nutrients in them, including some HMs such as Zn [174,175,176,177]. Thus, how these soil amendments affect HM accumulation is less straightforward. The effectiveness of composted amendments also depends on soil type, the HMs to be remediated, and the characteristics of the amendment (pH, EC, CEC, and humification potential) [178]. Figure 2 shows the change in availability of several HMs in relation to soil pH [179,180].

Gypsum, both naturally occurring and as an industrial byproduct, is commonly used in the remediation of HM-contaminated soils. Its application led to decreased availability of As, Cr, and Pb in soil [181,182]. Phosphate compounds are effective in immobilizing HMs such as Cd, Cu, Pb, and Zn by reducing their bioavailability through direct metal adsorption or substitution, anion-induced metal adsorption, and precipitation [183]. It has been recommended that combining amendments, such as biochar and lime, achieves synergistic effects in reducing HM uptake and is often advantageous [184].

6.4. Crop Selection and Genetic Engineering

The uptake of nutrients largely relates to the biomass production of the crop [3,185,186]. Model crops for HM soil remediation should have (a) rapid growth and high biomass yields; (b) deep and extensive root systems with the ability to accumulate or degrade contaminants; (c) high resource use efficiency, strong pest tolerance, adaptability to varied soil and climatic conditions, and minimal ecological requirements; and (d) known agronomic techniques with ease of harvesting [22]. Selecting species that have high affinity for HMs coupled with high biomass yields offers great potential for accumulating HMs, especially if HM-tolerant cultivars are selected [187]. Genetic engineering, including CRISPR-Cas9, enhances HM detoxification. Overexpression of phytochelatin synthase genes can decrease Cd translocation to shoots and increase biomass quality in bioenergy crops [188].

6.5. Policy Framework for Heavy Metal Management in Bioenergy Systems

Effective HM governance is essential to safeguarding soil health, bioenergy feedstock safety, and downstream processing. A robust policy framework should include monitoring standards, economic incentives, and international collaboration, supported by advanced real-time detection technologies.

Governments must mandate regular HM assessments in bioenergy crop fields and feedstocks using standardized analytical protocols. The FAO’s forthcoming “Technical Guidelines for Assessing, Mapping, Monitoring and Reporting Soil Pollution” aligns with ISO soil quality standards, offering clear steps for sampling, analysis, and data quality control geared toward global comparability. Implementing these protocols will strengthen regulatory coherence and support soil protection strategies under the soil health guidelines [189]. Regulations that actually cap heavy metals in bioenergy value chains sit outside the bioenergy-specific directives. For example, Directive—86/278 [190] sets limit values for seven metals (Cd, Cu, Ni, Pb, Zn, Hg, Cr) in sewage sludge used on agricultural land and in sludge-treated soils. If energy crops are grown on sludge-amended fields, producers must document compliance and ensure that they do not exceed metal inputs, thus not feeding bioenergy feedstock that is contaminated for biorefinery processes. In China, GB 15618-2018 [191] sets soil HM risk control thresholds (pH-dependent), determining where agricultural production, including energy crops, can continue or requires intervention.

To drive the adoption of sustainable remediation technologies, governments should offer financial incentives such as tax credits, subsidies, or low-interest loans for practices like phytoremediation and lime or biochar application. Lime and biochar significantly reduce the bioavailability of HMs (e.g., Cd and Zn) not only by increasing soil pH, but also through additional mechanisms. Lime promotes the precipitation of low-solubility metal compounds (e.g., carbonates, oxides, hydroxides), while biochar immobilizes metals via surface complexation, ion exchange, and physical adsorption [184,192,193].

Global HM contamination varies widely. Multilateral initiatives, such as the FAO’s Global Soil Partnership, facilitate region-specific guideline development and hotspot prioritization. While not for bioenergy crops, in a regional evaluation of HMs, Kaur et al. [194] found dire HM pollution situations with vegetable production in several countries including China, Bangladesh, India, and Pakistan.

There is an urgent need to monitor and control HM concentrations in environmental and human samples, which drives the development of advanced analytical strategies. Recent studies have explored innovative methods, including spectroscopic, optical, electrochemical, and nanotechnology-based approaches, for detecting HMs at trace levels, as summarized in a recent review paper by Inobeme et al. [195]. Techniques such as atomic absorption spectrometry combined with solid-phase extraction using adsorbents like graphene, graphene oxides, and quantum dots enable ultra-trace HM detection, while electrochemical advancements have led to portable, calibration-free potentiostats with customizable electrodes. Portable detection technologies, such as laser-induced breakdown spectroscopy (LIBS) and X-ray fluorescence (XRF), enable on-site, real-time HM measurement of both soil and plant tissue samples, significantly reducing lab turnaround and costs [196,197]. Recently, the integration of unmanned aerial vehicles (UAVs) with XRF has been proposed as a novel technique to enable rapid and efficient regional detection of HM pollution [195,198]. Furthermore, utilization of deep learning and AI to facilitate regional HM detection can greatly advance our detection capacity of HMs at large scale [197]. Integration into national soil monitoring frameworks can facilitate timely intervention and regulatory enforcement.

Apart from setting regulatory limits for HMs, policies such as financial incentives for farmers dealing with HM-contaminated soils could support sustaining bioenergy production especially on marginal lands. Financial mechanisms such as subsidies, tax credits, low-interest loans, or cost-sharing programs can offset the expenses of soil testing, remediation, and adoption of HM-mitigating practices (e.g., phytoremediation, biochar application, lime amendment). For example, in the European Union’s Common Agricultural Policy [191], farmers can be paid to implement soil conservation and contamination mitigation practices, which could be adapted to explicitly include HM remediation for bioenergy crops. Putting these policies into practice not only helps farmers absorb the costs of compliance but also encourages the integration of bioenergy production with soil restoration. This could create a win–win outcome for securing sustainable energy production and ensuring environmental health [199].

In summary, management of HMs in bioenergy systems involves several approaches that together ensure the sustainable production of bioenergy crops and the related processes. Phytoremediation uses HM-tolerant, high-biomass crops such as miscanthus, switchgrass, etc., to extract or immobilize HMs while producing biomass that can be used in biorefinery processes. Microbial bioremediation uses bacteria and fungi to take up, transform, or precipitate HMs. To achieve this, several strategies including bioaugmentation and biostimulation have been shown to be effective. Soil amendments such as biochar, lime, compost, gypsum, and phosphates can immobilize HMs by raising pH or binding to contaminants, while combining amendments often yields desirable outcomes. Crop selection and genetic engineering (e.g., CRISPR-Cas9-mediated overexpression of metal-binding proteins) can enhance tolerance and limit metal translocation to harvestable tissues. Policy frameworks from the EU’s Sewage Sludge Directive to China’s GB 15618-2018 [191] set contaminant limits in soils and amendments demonstrating real-world implications of HMs contamination control in crop–environment systems. Advanced methods of HM monitoring have been established including XRF, LIBS, etc., that improve the assessment of HMs and help with regulatory efforts. Together, these measures aim to reduce HM bioavailability, protect biomass quality, and ensure compliance with regulatory and market standards while maintaining bioenergy productivity.

7. Conclusions and Future Directions

Heavy metals pose multifaceted challenges to bioenergy crop production, biomass quality, and biorefinery efficiency, threatening the sustainability of global bioenergy systems. Their uptake and translocation disrupt plant physiology, reducing biomass yields and altering lignocellulosic composition critical for biofuel and biogas production. Heavy metal accumulation in biomass contaminates feedstocks, inhibits enzymatic and microbial processes, and generates toxic residues, increasing processing costs and environmental risks. Sustainable management strategies, including phytoremediation, microbial bioremediation, soil amendments, and genetic engineering, provide promising answers for mitigating HM effects while improving crop resilience and biorefinery output.

Future research should prioritize the development of HM-tolerant bioenergy crop varieties through advanced breeding and gene editing technologies, such as CRISPR-Cas9, which could reduce HM translocation. Optimizing biorefinery processes to handle contaminated biomass, such as through ionic liquid pretreatments or the use of HM-tolerant microbial strains, is crucial for improving efficiency and reducing costs. Providing scalable remediation technologies, particularly microbial consortia and soil-based amendments, should be explored to address HM contamination in diverse agroecosystems.

Policy frameworks must enforce HM monitoring using advanced techniques, such as LIBS and XRF, coupled with UAVs and deep learning, to ensure compliance with regulatory standards. Incentives for adopting remediation technologies, such as subsidies for amendment application, can promote sustainable practices. Integrating bioenergy production with environmental restoration, such as coupling bioenergy crop phytoextraction with biochar and lime application, offers a pathway to maximize land use efficiency and support circular economies. Addressing HM issues through transdisciplinary approaches can help the bioenergy sector contribute to global energy security, climate change mitigation, and environmental sustainability. In the long term, such steps will ensure that bioenergy crops can survive on polluted soil, thereby facilitating the transition to a low-carbon future.