Agromining in Brazil: search for tropical hyperaccumulators, management strategies, and ecosystem risks from exposure to ultramafic soil
Heavy metal. Hyperaccumulation. Metalliferous soils. Nickel. Phytomining
Ultramafic soils are anomalous environments in terms of heavy metal content (mainly Ni, Co, and Cr) and can generate economic returns through mineral extraction. However, conventional extraction techniques are responsible for strong environmental impacts. In this scenario, hyperaccumulator plants can remove high amounts of metals from enriched substrates in an economical, ecological, and profitable way through agromining. Although promising, this approach requires species prospecting, soil management strategies, and risk assessment to ensure environmental sustainability. Thus, this work aimed to develop a method to monitor Ni levels in plants by portable X-ray fluorescence (XRFp) and to evaluate the natural and induced accumulation of the metal in five tropical hyperaccumulators and their respective potentials for agromining in Brazil. Additionally, to investigate the environmental, ecological, and human health risks by exposure to soil particles and consumption of vegetables grown in this setting. To this end, 14 species with different Ni accumulation patterns were used for calibration using FRXp. Brazilian (Pfaffia sarcophylla, Lippia lupulina and Justicia lanstyakii), Mexican (Blepharidium guatemalense) and African (Berkheya coddii) species grown on ultramafic soils were evaluated for Ni contents and spatial distribution of metals in leaves by synchrotron light-based X-ray microfluorescence (μFRX-SR). Petrographic analyses were performed on the source materials and the ultramafic soils were characterized chemically, physically and mineralogically. The available, pseudo-total, total, sequential and bioaccessible Ni, Co and Cr contents were determined. The carcinogenic and non-carcinogenic risks to human health, the bacterial community of the soils, and the effect of citric acid doses on metal availability were also evaluated. Our results showed that calibration model for FRXp was efficient in predicting Ni in plants (R² = 0.94). Brazilian hyperaccumulators showed low potential for commercial agromining However, the high Ni accumulation of B. guatemalense and B. coddii (> 1.0 %) makes these species candidates for tropical agromining. Furthermore, the application of citric acid (40.0 mmol kg-1) to ultramafic soil increased by 25.0 % the foliar Ni accumulation by B. guatemalense and by 60.0 % the metal content in the bio-ore. The species evaluated showed a similar pattern of spatial distribution of metals, and preferential accumulation of Ni in the phloem and epidermis, suggesting defense mechanisms against herbivory. In the soil, the total metal contents (mg kg-1) for the districts of Niquelândia and Buenos Aires, respectively, were Co (373.5 and 349.2), Cr (1844.5 and 2485.5) and Ni (9597.5 and 1428.5). Environmental and human health risks were estimated and considered acceptable due to higher retention of metals in Fe oxides and in the residual fraction. However, high ecological risks were described for both soils and unacceptable cancer risk from consumption of vegetables grown in these environments. The highest metal tolerance was observed in the phyla Proteobacteria, Bacteroidota and Firmicutes. Therefore, our results indicate efficient Ni monitoring by FRXp and high potential for natural and induced Ni agromining in Brazil. Furthermore, management that intensifies erosion and mobility of metals and food crops on these soils should be avoided to ensure food security and environmental sustainability.