Agromining: Farming for Metals

The concept of phytomining is a natural extension of botanical prospecting and the study of metal biochemistry and biogeography of metal hyperaccumulator plants. Some elements may be phyto-extracted to remediate soils, but the recovered biomass would have little economic value (Cd, As, etc.) and disposal of the biomass would be a cost. A few elements may have sufficient economic value in phytomining biomass to support commercial practice (Ni, Co, Au). The development of phytomining requires (1) selection of high-biomass hyperaccumulator plant species; (2) evaluation of genetic diversity and breeding of improved strains with higher yields of the phytoextracted element; (3) development of agronomic practices to maximize economic return; and (4) development of methods to recover the phytomined element from the plant biomass. Plant species and methods for phytomining of soil Ni have been demonstrated for several species and locations (temperate and tropical climates). Production of Ni metal in an electric arc furnace smelter, and of Ni(NH₄)₂SO₄ using a hydrometallurgical method, have been demonstrated. Full commercial phytomining of Ni is beginning in Albania using Alyssum murale, and major trials in Malaysia are underway using Phyllanthus securinegioides. Variable prices of commodity metals add confusion to the development of commercial phytomining.

Agromining involves growing selected hyperaccumulator plant species (‘metal crops’) on low-grade ore bodies or mineralized (ultramafic) soils, or anthropogenic metal rich materials (e.g. contaminated soils, mine spoils, industrial sludge), prior to biomass harvesting and incineration to recover valuable metals or salts. This chapter begins with an introduction that explains the concepts of phytomining and agromining. We then acknowledge the role of agronomy in enhancing metal yield of ‘metal crops,’ with emphasis on Ni. Highlighted in the selection of sites section is the issue of potential agromining substrates, and the role of metal phytoavailability in economic agromining. We present criteria for selecting potential ‘metal crops’ and possible regions where these species are most suited for successful agromining operations. We then discuss thoroughly the soil and plant management practices that have been proposed to increase biomass and metal yield of ‘metal crops.’ Also reported is progress of the tropical agronomic trials. Finally, we provide a conclusion and present an outlook on the agronomy of ‘metal crops’ used in agromining.

Hyperaccumulator plants may contain valuable metals at concentrations comparable to those of conventional metal ore and can be significantly upgraded by incineration. There is an incentive to recover these metals as products to partially counter-balance the cost of disposing the contaminated biomass from contaminated soils, mine tailings, and processing wastes. Metal recovery is included in the agromining chain, which has been developed over the past two decades for Ni and Au. More than 450 Ni-hyperaccumulator species are currently known and some grow quickly providing a high farming yield. Nickel recovery involves an extraction step, ashing and/or leaching of the dry biomass, followed by a refining step using pyro- or hydrometallurgy. The final products are ferronickel, Ni metal, Ni salts or Ni catalysts, all being widely used in various industrial sectors and in everyday life. Gold can be recovered from mine tailings using a number of plant species, typically aided by a timed addition of an Au-chelating extractant to the soil. Dry biomass is ashed and smelted. This approach enables the treatment of resources that could not be effectively processed using conventional methods. In addition to nickel and gold, the recovery of other metals or elements (e.g. Cd, Zn, Mn, REEs) has been investigated. Further effort is required to improve process efficiency and to discover new options tailored to the unique characteristics of hyperaccumulator plant biomass.

Starting from the concept of sustainability and the need for metrics to assess it, this chapter presents the basics of the Life Cycle Assessment (LCA) methodology and its different versions (attributional versus consequential, static versus dynamic). Key issues related to the application of LCA to agromining, either on natural soils (such as ultramafic soils) or on anthropogenically polluted areas (such as mine tailings) are highlighted. Land use impacts are described more specifically: these are linked to the ecosystem services rendered by land systems and characterized via indicators that attempt to quantify soil organic carbon content, biodiversity, and land erosion by rainfall and wind. In spite of the actual limitations on quantification of land use impacts, which are not specific to agromining projects, Life Cycle Assessment offers a framework for agrominers to discuss assess their projects in terms of sustainability.

A large body of analytical data is available on the inorganic composition of many thousands of plant species, for which typical concentration ranges have been tabulated for major, minor, and trace elements. These elements include those that have been shown essential for plant growth, as well as others that lack this status, at least universally. Metalliferous soils, having abnormally high concentrations of some of the elements that are generally present only at minor (e.g. 200–2000 μg g⁻¹) or trace (e.g. 0.1–200 μg g⁻¹) levels, vary widely in their effects on plants and have attracted increasing attention during the last 50 years. The effects depend on the species, the relevant elements, and soil characteristics that influence the availability of metals to plants. Some of these soils are toxic to all or most higher plants. Others have hosted the development of specialized plant communities consisting of a restricted and locally characteristic range of metal-tolerant species. These plants often show a slightly elevated concentration of the elements with which the soil is enriched, but in places a species exhibits extreme accumulation of one or more of these elements, to a concentration level that may be hundreds or even thousands of times greater than that usually found in plants on the most common soils. These plants, now widely referred to as hyperaccumulators, are a remarkable resource for many types of fundamental scientific investigation (plant systematics, ecophysiology, biochemistry, genetics, and molecular biology) and for applications such as phytoremediation and agromining, and are discussed in detail below.

Some trace elements are essential for plants but become toxic at high concentration. Remarkably, about 500 plant species worldwide are able to accumulate tremendous amounts of metals in their leaves and are therefore called metal hyperaccumulators. In the context of sustainable development, there is a regain of interest for metal hyperaccumulation mechanisms that may become instrumental for improving metal phytoextraction from contaminated soils to produce metals with a lower net impact on the environment. In addition, studying the molecular mechanisms of hyperaccumulation in diverse plant species is necessary in order to understand the evolution of this extreme and complex adaptation trait. Our current knowledge of metal hyperaccumulation is mostly based on the analysis of a few species from the Brassicaceae family, and suggests that the underlying mechanisms result from an exaggeration of basic mechanisms involved in metal homeostasis. However, the development of Next Generation Sequencing technologies opens today the possibility for studying new hyperaccumulator species that therefore may reveal more diversity in these mechanisms. The goal of this chapter is to provide background information on metal hyperaccumulation and give a clear picture of what we know currently about the molecular mechanisms involved in this trait. We also attempt to outline for the reader the future scientific challenges that this field of research is facing.

Globally the discovery of hyperaccumulator plants has been hindered by systematic screening of plant species, and is highly biased towards Ni hyperaccumulators. This is mainly due to the existence of a reagent paper test that is only specific to nickel (based on dimethylglyoxime) such that more than 400 of the approximately 500 known hyperaccumulators species are for Ni. New technical advances now permit massive screening of herbarium specimens using non-destructive, portable X-Ray Fluorescence Spectroscopy (XRF), an approach that has already led to the discovery of numerous hyperaccumulator species new to science. The elemental distribution in selected hyperaccumulator plant tissues can then be further studied using techniques such as desktop or synchrotron micro-XRF, nuclear microprobe (PIXE), scanning/transmission electron microscopy with energy-dispersive spectroscopy (SEM/TEM-EDS), secondary ion mass spectrometry (SIMS) or laser ablation inductively-coupled plasma mass spectrometry (LA-ICP-MS). The use of histochemical dyes combined with light microscopy further aids in the identification of anatomical and structural features of the studied plant tissues.

Ultramafic outcrops represent less than 1% of the terrestrial surface but their unusual geochemistry makes them a global hotspot for biodiversity. Ultramafic soils are a peculiarity for soil scientists in all climatic zones of the world. These soils lack essential pedogenetic elements: Al, Ca, K, and P. Whereas serpentinites will most likely give birth to Eutric Cambisols with little influence by climate, peridotites will induce an acceleration of weathering processes; this over-expressed weathering is due to their deficiency in Si and Al and lack of secondary clay formation. Soils evolve towards Ferralsols in tropical conditions. Results from isotopic dilution techniques show that Ni borne by primary minerals is unavailable. Secondary 2:1 clay minerals (e.g. Fe-rich smectite) and amorphous Fe oxyhydroxides are the most important phases that bear available Ni. Therefore, smectite-rich soils developed on serpentinite and poorly weathered Cambisols on peridotite (only in temperate conditions) are the soils with highest availability of Ni. Although soil pH conditions are a major factor in controlling available Ni, the chemical bounds of Ni to containing phases are even more important to consider. Plants take up significant amounts of Ni, and its biogeochemical recycling seems an essential factor that explains Ni availability in the surface horizons of ultramafic soils.

Phytomining can be limited by low biomass productivity by plants or limited availability of soil metals. Ongoing research attempts to overcome these potential constraints and to make phytomining a successful commercial technique in the recovery of metals from polluted or naturally metal-rich soil by (hyper)accumulating plants. Recently, the benefits of combining phytoremediation with bioremediation, which consists in the use of beneficial microorganisms such as endophytes or rhizosphere bacteria and fungi, for metal removal from soils have been demonstrated. Metal-resistant microorganisms play an important role in enhancing plant survival and growth in these soils by alleviating metal toxicity and supplying nutrients. Furthermore, these beneficial microorganisms are able to enhance the metal bioavailability in the rhizosphere of plants. An increase in plant growth and metal uptake increases the effectiveness of phytoremediation processes coupled with bioremediation. Herein, we highlight the specificity of the rhizosphere and the critical roles in soil nutrient cycling and provision of ecosystem services that can be brought by rhizosphere microorganisms. We discuss how abiotic factors, such as the presence of metals in polluted sites or in naturally rich (ultramafic) soils modulate activities of soil microbial communities. Then we introduce the concept of microbe-assisted phytomining, and underline the role of plant-associated microorganisms in metal bioavailability and uptake by host plants that has attracted a growing interest over the last decade. Finally, we present various techniques, including phenotypic, genotypic, and metagenomic approaches, which allow for characterising soil microbial community structure and diversity in polluted or naturally metal-rich soils.

The identification and use of hyperaccumulator plants in mining projects has been recognised as an important component part of mine planning at several sites around the world. Indeed, mine planning that includes hyperaccumulator plants requires operators to maximize the biological resources of a site by discovering and utilizing these unusual plant species at the early planning stages. These locally adapted hyperaccumulator species can then be used for rehabilitation in and around the mine area, or be utilized for their potential to extract ecocatalysts and metals. Such opportunities should be more widely explored so that these unique plants can become an integrated and valuable part of the mining process. This chapter concentrates on the experiences of integrating hyperaccumulating plants into mine rehabilitation projects in Indonesia and New Caledonia, in order to highlight some of the opportunities and challenges encountered when attempting to incorporate these species into the mining cycle.

Cadmium is one of the most threatening soil contaminants because of its high toxicity and widespread anthropogenic distribution. Therefore, remediation of Cd-polluted soils is urgently required. Cropping Cd-accumulating plants appears to be the most relevant approach for removing this pollutant from large soil surfaces. Several field studies have shown the potential of phytoextraction to clean-up moderately Cd-contaminated sites, but this process still has important limitations. Hyperaccumulating plants such as Noccaea caerulescens and Sedum plumbizincicola show considerable Cd removal rates due to their extraordinary accumulation capacities, but commonly suffer from strongly limited biomass production, especially N. caerulescens. Interesting results were also found for other plants, e.g. some cultivars of ‘indica’ rice Oryza sativa or Solanum nigrum, but in these cases, further studies are required for confirmation. Some fast-growing willow clones, cultivated in short rotation coppice, offer a possibility to produce energy biomass on contaminated soils more than by decontaminating them, because of their low Cd extraction rate. Relatively little is known about the use of harvested biomass produced through phytoextraction. A few studies showed that combustion is a feasible option, because Cd is retained mainly in the fly ash, whereas the bottom ash contains relatively low amounts of Cd and could even be used as a fertilizer. Further investment is required to evaluate the possibility of producing high-performance cultivars of the best Cd hyperaccumulators. If this approach yields positive results, the complete process chain will need to be tested on a large scale, including the valorisation of biomass.

Initial experiments using Mediterranean Ni-hyperaccumulator plants for the purpose of phytomining were carried out in the 1990s. In order to meet commercial phytoextraction requirements, a technology has been developed using hyperaccumulator species with adapted intensive agronomic practices on natural Ni-rich soils. Ultramafic soils in the Balkans display a great variability in Ni concentrations and available Ni levels, both in Albania and the Pindus Mountains of Greece. In Albania, Vertisols are currently being used for low-productivity agriculture (pasture or arable land) on which phytomining could be included in cropping practices. Alyssum murale occurs widely on these ultramafic Vertisols and is a spontaneous weed that grows among other crops. This review chapter presents the different steps that were investigated during the study of soil suitability, and selection of plants up to optimization of agronomic practices, at field scale, as recently developed to reach the implementation stage of Ni agromining in Albania. During a 7-year study we addressed the following questions: (i) what are the optimal soils for Ni agromining in terms of fertility and Ni availability? (ii) what is the phytoextraction potential of local populations of Ni hyperaccumulator species? (iii) what should be the agronomical practices used to optimize the cropping of A. murale for extensive phytomining adapted to a Balkan agricultural setting?

Cobalt is economically considered a critical metal for a variety of technologies. Globally, the most important Co ore deposits occur in the Katangan Copperbelt (Democratic Republic of Congo) where a richness of Cu-Co-tolerant and accumulator plants have developed naturally. Cobalt mining there has resulted in the dissemination of large quantities of waste in the environment and is a major environmental issue. Reduction of environmental risks and Co dispersion can be performed by phytoremediation and/or agromining, using trace-element-tolerant and putative hyperaccumulator plants that originated from the biodiversity of natural Co and Cu-rich habitats. Accumulation of foliar Co to >300 μg g⁻¹ is exceptionally rare globally, being known principally from the Copperbelt of Central Africa. This chapter highlights advances in our knowledge of Co accumulation in plants, examines potential for use of a Co-accumulator in agromining, and defines perspectives for Co agromining by designing multi-functions and services of agroecosystems.

Selenium hyperaccumulator plants such as Stanleya pinnata, Astragalus bisulcatus, and the newly discovered Cardamine hupingshanensis may play an important role in the Se cycle from soil to plant to human, especially in China. Se-hyperaccumulators can be used for agromining or for phytoremediation of Se, as well as for applications to Se-deficient soils in Se-biofortification strategies.

Thallium is a highly toxic and valuable element for which there are known fast-growing hyperaccumulator plants that have some of the greatest bioaccumulation coefficients (plant/soil concentration quotients) of any non-essential element. As with other elements, many hyperaccumulators discovered to date are in the Brassicaceae family. In contrast, hyperaccumulation of the precious metals Au, Pd, and Pt is not recorded for any plant species. To achieve uptake of these precious (noble) metals, chemicals must be added to the soil in order to induce metal solubilisation; and for these particular metals, cyanide has proven time and again to be the most effective agent to promote uptake. However, cyanide does not specifically target the noble metals. Increased solubility and uptake of more toxic Cu and Ag can limit the uptake efficiency of a phytomining or agromining crop (a co-metallic effect). Worldwide, numerous soils are known that have a high Tl burden (>1.5 μg g⁻¹) and hence are unsuitable for safe food production, of low value, thus being ideal for agromining. Among all elements that could potentially be agromined, Tl has perhaps the greatest potential to be economically successful. Despite this promising technique, Tl has received relatively little attention. In contrast, the geographical scope for noble metal uptake is much more limited. Research is warranted for discovering new hyperaccumulators, the economics of recovering Tl and noble metals from biomass, and quantification of areas where agromining for valuable metals may be feasible.

Manganese (Mn), one of the important trace element in different concentrations in living tissues, is also widely used in the metal industry. It is an essential micronutrient for plants, taken up under the +2 oxidation state, which is crucial in the reactions of some enzymes (malic dehydrogenase, oxalosuccinate decarboxylase, superoxide dismutase), and is an activator of those involved in the tricarboxylic acid cycle. In soils, Mn is commonly in the form of +4 and +3 valency states oxides, which could be reduced to the +2 form by some of the ways, such as acidizing soil solution, waterlogging soil, heating and drying, and by the activity of anaerobic and aerobic micro-organisms. Mn can be taken up by plants growing in base-rich soils in high concentrations. Mn hyperaccumulation plants have been defined by a threshold foliar concentration of over 10,000 μg g⁻¹ dry weight (DW). Mn toxicity could cause stunting, chlorosis, curled leaves, brown lesions, as well as inhibition of photosynthesis and respiration in plants. Several elements such as P and Ca are reported to have important impacts on the uptake and accumulation of Mn in plants. Mn can be stored in vacuoles, cell walls, golgi apparatus, chloroplast lamellae structure, and to form black agglomerations in plant cells.

Arsenic contaminated soil is a major issue in PR China. The discovery of an As hyperaccumulator fern, Pteris vittata opens a door for phytoextraction of As-contaminated soils. In situ phytoextraction projects using P. vittata have been established that achieved high removal rates of As. The first phytoextraction project in the world was established in Chenzhou, Hunan Province. Subsequently, more phytoextraction projects were established in Guangxi Zhuang Autonomous Region, Yunnan Province, Henan Province and Beijing. During these field-based projects, the safe disposal and re-utilization of P. vittata biomass were considered essential processes. Incineration technologies for P. vittata biomass are well developed. Safe landfilling has been applied for the disposal of the burned ash of P. vittata when the amount of that ash is small. When the ash amount is large, a recycling method has to be applied. Agromining of Ni has been successfully achieved, but agromining of As is at present only an idea, owing to the low commercial value of As. Nevertheless, production of a biofuel resulting from the incineration process, together with the recycling of As, could be a potential opportunity for agromining of this metalloid.

Sedum plumbizincicola (Crassulaceae), a new Sedum species, was originally discovered in 2005 in Zhejiang Province, eastern PR China. It was identified as a Cd-Zn hyperaccumulator in 2007. During the past decade, great efforts have been made to understand its metal-accumulating capacities, physiological mechanisms for metal hypertolerance and hyperaccumulation, enhancing measures of phytoextraction, field application phytoremediation practice, and disposal of harvested biomass. This chapter provides a brief review of the progress on phytoremediation of Cd- and Zn-contaminated soils using this species. Agronomic measures to enhance Cd and Zn phytoextraction efficiency by S. plumbizincicola were studied, including cultivation management, intercropping with other plant species, and nutrient management. Changes in soil and plant metal uptake were investigated during long-term and repeated phytoextraction of Cd- and Zn-contaminated soils using S. plumbizincicola. Field assessment results confirm that phytoextraction using S. plumbizincicola is a promising technique for the remediation of slightly Cd-polluted soils without the need to halt normal agricultural production.

The growing demand of strategic resources, e.g. rare earth elements (REEs), for development of modern technologies has spurred an increase in mining activities and consequently a release of REEs into the environment, posing a potential threat to human health. Phytoremediation, regarded as an in situ and low-cost means to remediate polluted soils, uses the growth and harvest of hyperaccumulator plants that take up high concentrations of metals in their shoots, allowing metal removal from contaminated soil (phytoextraction) or commercial production of high-value metals (phytomining). In this chapter, we review the discovery of REE hyperaccumulators worldwide, particularly focusing on the fern species Dicranopteris dichotoma that preferentially takes up light REEs. Though less understood, mechanisms of REE uptake, translocation, and distribution in hyperaccumulator plants are also discussed. Finally, taking D. dichotoma as an example, we estimate the phytomining potential for REEs using this species, based on its biomass production, REE concentrations in the ash, and current market prices of REEs.

The technology of agromining has created a new era in the recovery of strategic metals from natural or secondary resources, including industrial wastes. During the last decades, hyperaccumulator plants have changed recognition from merely a botanical curiosity to a prospect having tangible socio-economic and environmental applications. The knowledge base for this group of plant species, with unique properties capable of surviving and thriving in toxic and stressful environments, has increased greatly during the last 20 years, thanks to thorough investigations at various scales involving several disciplines, including botany, ecology, ecophysiology, microbiology, soil science and agronomy. The processes and mechanisms that preside over the hyperaccumulation of toxic metals and metalloids in plants are now better understood. For example, the fate and biopathways of elements in plants is actively being investigated using powerful new explanatory techniques, such as synchrotron and microprobe analysis. In addition, new species having exceptional ability to accumulate metals have been discovered, thereby considerably increasing the number of known hyperaccumulators. In parallel, work conducted by agronomists and soil scientists has allowed the domestication of selected hyperaccumulator species and hence an enabling large-scale implementation of agromining. This approach promotes a new form of agriculture, which could generate income for peoples in developing countries that live on agriculturally mediocre lands, such as those derived from ultramafic bedrock. Finally, the implication of scientific knowledge in the chain, such as chemistry and chemical engineering, and the stimulation of pluri-disciplinary research programs, bring hope to the feasibility of manufacturing specialist products of high industrial interest from agromined bio-ore.