Aerobic release of arsenic and antimony from mine soils by biostimulation of indigenous microbial activity and bioaugmentation with Cupriavidus genera of bacteria

Vol.: (0123456789) 1 3 Plant Soil (2024) 497:175–197 https://doi.org/10.1007/s11104-023-06372-1 RESEARCH ARTICLE Aerobic release ofarsenic andantimony frommine soils bybiostimulation ofindigenous microbial activity andbioaugmentation withCupriavidus genera ofbacteria HanaHorváthová · KatarínaSchwarzkopfová· HanaVojtková · ĽubomírJurkovič · TomášFaragó · KateřinaBoturová· EdgarHiller · MartinUrík · MartinaVítková Received: 15 June 2023 / Accepted: 24 October 2023 / Published online: 21 November 2023 © The Author(s) 2023 Abstract Background and Aims Bioremediation of soils contaminated with metal(loid)s is an attractive research area due to its sustainability and economic benefits. In the Slovak Republic, there are several abandoned mines containing high concentrations of arsenic (As) and antimony (Sb). This calls for new options for removing these hazardous metalloids from contaminated substrates. Studies on bioleaching of soils cocontaminated with both metalloids are very rare. This study aimed to test the effectiveness of bioleaching of soils heavily co-contaminated with As and Sb (up to 1463 mg.kg–1 and 5825 mg.kg–1, respectively) at a former stibnite mining site (Poproč, eastern Slovakia) through biostimulation and bioaugmentation. Methods Bioleaching of As and Sb from four soils was induced by biostimulation of autochthonous microflora with Sabouraud medium (SAB) and SAB+glucose, and bioaugmentation of the soil with bacterial strains Cupriavidus oxalaticus and Cupriavidus metallidurans. Soil samples were subjected to determination of physicochemical properties, microbiological parameters, and additional mineralogical analysis. Results An inverse relationship between the total metalloid concentration and the microbial diversity was confirmed. In experiments with Cupriavidus metallidurans and Cupriavidus oxalaticus, mean bioleached As fractions were 37.6% and 41.3%, while Sb bioleaching was significantly lower, Responsible Editor: Fayuan Wang. Supplementary Information The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s1110402306372-1. H.Horváthová(*)· K.Schwarzkopfová· Ľ.Jurkovič· T.Faragó· E.Hiller Department ofGeochemistry, Faculty ofNatural Sciences, Comenius University inBratislava, Ilkovičova 6, 84215Bratislava, SlovakRepublic e-mail: hana.horvathov[email protected] H.Horváthová The Centre ofEnvironmental Services, Ltd., Kutlíkova 17, 85052Bratislava, SlovakRepublic H.Vojtková· K.Boturová Faculty ofMining andGeology, Department ofEnvironmental Engineering, VŠB – Technical University ofOstrava, 17. listopadu 15/2172, 70800Ostrava-Poruba, CzechRepublic M.Urík Institute ofLaboratory Research onGeomaterials, Faculty ofNatural Sciences, Comenius University inBratislava, Ilkovičova 6, 84215Bratislava, SlovakRepublic M.Vítková Department ofEnvironmental Geosciences, Faculty ofEnvironmental Sciences, Czech University ofLife Sciences Prague, Kamýcká 129, 165 00, Praha-Suchdol, CzechRepublic 176 Plant Soil (2024) 497:175–197 1 3 Vol:. (1234567890) ranging between 17.0–26.2%. The mean bioleached fraction of As and Sb using SAB was 40.7% and 14.4%, respectively. The addition of glucose to SAB increased As bioleaching (50.7%) but not that of Sb. Conclusion Collectively, the results highlighted a role of microorganisms in the mobility of metalloids in soils with their prospective applications in remediation of contaminated sites. Keywords Bioleaching· Contamination· Metalloid· Soil· Tailings Introduction The geochemistry of As and Sb in near-surface environments is studied in detail due to their indiscriminate toxicity to living organisms, including humans. Both metalloids were shown to negatively affect microbial diversity in soils/sediments and plant growth, are probable human carcinogens and exhibit other negative human health outcomes (Bolan etal. 2022; Diquattro etal. 2020; Fatoki and Badmus 2022; Nabi etal. 2021; Xu etal. 2020). Historically, As and Sb were thought to have identical geochemical behaviour in oxidised environments. However, it is now well-known that there are differences in mobility, redox kinetics, affinity for solid components and speciation between As and Sb (Drahota etal. 2023; Ettler etal. 2010; Fu etal. 2016; Radková etal. 2023; Wilson etal. 2010). The prevalent species of As and Sb in aquatic and soil environments with a high value of redox potential and in a wide range of pH are negatively charged species of arsenic (H3AsO4) and antimonic (HSbO3) acids, i.e., in the form of oxyanions (Bolan etal. 2022; Wang etal. 2023). There is no doubt that in oxidised environments rich in Fe, the guest solid phases of As and Sb are mainly Fe(III) oxides as shown by many studies using different approaches (Drahota etal. 2018, 2023; Fazle Bari etal. 2020; Hiller etal. 2021; Kreidie etal. 2011; Radková etal. 2023; Ružičić etal. 2023; Tapia etal. 2022). High concentrations of As and Sb in the environment are usually related to mining and smelting areas, in which, in addition to direct emissions, produced wastes also contribute to environmental contamination (Radková etal. 2023). Despite its small area, the Slovak Republic has countless abandoned mining and processing areas with unsecured or technically outdated mine waste dumps and tailings ponds left after the mining of stibnite and other metal(loid) ores that contaminate waters, soils, sediments and biota (Hiller et al. 2012, 2013, 2016). This calls for removal of contamination of solid matrices with As and Sb to reduce their source reservoir to natural waters. A large body of recent excellent studies has been published focusing on the release, mobility and bioavailability of As and Sb in soils, sediments and mine wastes co-contaminated with metalloids (Álvarez-Ayuso 2022; Chang etal. 2022; Drahota etal. 2023; Hiller etal. 2021; Johnston etal. 2020a; Yang etal. 2015). However, these studies omit the significance of metabolic activity of the autochthonous microbial consortia that may support the mobilisation of As and Sb via extrusion of acidic or redox active extracellular metabolites (e.g., organic acids), process known as bioleaching (Dusengemungu et al. 2021; Gao et al. 2021). Bioleaching was successfully applied to the removal of metal(loid) s from low-grade ores, mine wastes, metal-containing secondary raw materials and sewage sludge (Kremser etal. 2022; Nguyen etal. 2015; Sikander etal. 2022). Among various soil microorganisms, facultative chemolithoautotrophic β-proteobacteria belonging to the genus of Cupriavidus received attention since they were shown to have a dominant position within a natural microflora in metal(loid) contaminated environment (Goris et al. 2001; Ryan and Adley 2011) and abundance of the transition metal efflux systems and other metal resistance determinants (Mazhar etal. 2020; Ridene etal. 2023; Yang etal. 2020). Several dozen representatives of this genus were included in a number of interesting biotechnological applications, especially in a field of mineralprocessing and agricultural biotechnology or as plant growth promoters in metal(loid)- containing environments (Cuadrado etal. 2010; Cheng etal. 2023; Reith et al. 2009; Yan et al. 2021). Within the above-mentioned applications, the species of Cupriavidus genus were used as individual strains or consortia (Akkurt etal. 2023; Alvi-Gazitua etal. 2022; Ridene etal. 2023). The incorporation of specialised microbial culture to enhance the removal of contaminants is known as bioaugmentation (Lopes etal. 2022). The ability of microbial populations to remove contaminants in a certain type of the environment can be increased by adding the specific nutrients, electron acceptors (Jablonovská etal. 2010) or adjustments of the physicochemical conditions in the contaminated 177 Plant Soil (2024) 497:175–197 1 3 Vol.: (0123456789) area (Lopes etal. 2022). This strategy usually refers to biostimulation (Mrozik and Piotrowska-Seget 2010). The addition of nutrients and carbon sources for stimulation of microbial growth promoting As bioleaching from soils was reported in several studies (Chen etal. 2024; McLean etal. 2006; Park etal. 2006; Stucker etal. 2013). However, reports on Sb bioleaching after biostimulation of autochthonous microbial consortia are still sparse. These approaches inspired us to evaluate the release As and Sb from mine soils collected at the abandoned Sb deposit in Poproč (eastern Slovakia) using the biostimulation and bioaugmentation with the strains Cupriavidus metallidurans and Cupriavidus oxalaticus under aerobic conditions. The strains were selected because of their broad genetic toolbox for dealing with several organic and inorganic contaminants (Bedade and Singhal 2018; Xiang et al. 2020; Yan etal. 2021) and their resistance to a wide range of metal(loid)s (Jiang etal. 2017; Van Houdt etal. 2009). The present research brings the unique application of bioleaching to native co-contaminated mine soils with As and Sb. Studies on the bioleaching of soils co-contaminated with As and Sb are sparse, and to our best knowledge, the bacteria of Cupriavidus genus on this type of solid matrices have not been used so far. The high concentration of metal(loid)s in the environment due to mining activities in combination with insufficient monitoring and control over the fate of contamination might be inscrutable. Over time, the physico-chemical changes can lead to the release of metalloids, therefore, looking for the possibilities of their removal from mine soils and wastes is of a high priority. Moreover, the selected approach – bioleaching is referred to as cost-effective, environmentally friendly, and does not require hazardous chemicals (Pathak etal. 2009; Sarkodie etal. 2022). Material andmethods Brief description of the area The abandoned stibnite mines of Poproč are located in the SE part of the Spišsko-Gemerský rudohorie Mts. near the village of Poproč (Fig.1). Mining began in the 17th century and ended in 1965. Between 1931 and 1965, production at the deposit reached a peak (10,000 metric tons of Sb and 80 kg of gold) (Grecula etal. 1995). The main minerals of the deposit were quartz, stibnite and carbonates with accompanying arsenopyrite, galena, pyrite, sphalerite, tetrahedrite and gold (Chovan and Andráš 1994). During the operation of the mines, voluminous mine wastes were produced, mainly tailings, which were disposed of three ponds and along the stream of Olšava, draining the mine area. No measures were taken to isolate the mine tailings. Direct contact of accumulated Asand Sb-rich waste with atmospheric precipitation caused massive contamination of soils, sediments, and surface and groundwater (Hiller etal. 2012). The area is dominated by mixed beech-oak forests and the tailings ponds are covered with vegetation, small shrubs, and trees. Soil sampling Soil samples were taken from four selected sites (Fig. 1). The sampling sites were selected to best Fig. 1 Location of abandoned stibnite mines in Poproč and selected soil sampling sites 178 Plant Soil (2024) 497:175–197 1 3 Vol:. (1234567890) represent the territory of the former stibnite mines, especially from the point of view of total As and Sb concentrations and pH. At each site, mine soil was taken from the corners and centre of a 1 m2 square area (5 subsamples) from a depth of 0-20 cm using a stainless steel soil auger. Five subsamples were thoroughly mixed to obtain a composite soil sample kept until analytical and experimental work in re-sealable PE bags. Soil samples were air-dried in the dark at room temperature, carefully disintegrated if necessary and passed through a 2 mm sieve. Sample POP 1 is soil from a forest where mine waste heaps occur, and sample POP 2 is poorly developed soil on a tailings pond near the ruins of former mining buildings. Samples POP 3 and POP 4 are also mine soils from tailings ponds taken downstream the stream of Olšava. Samples POP 2–POP 4 from tailings ponds represent mineral, significantly oxidised mine material of yellow, orange to red colours without vertical division. In the following text, for unification and simplification, the samples are referred to as “mine soils” because they are affected by mining activities. Mineralogical analyses Soil samples from the same sampling sites were mineralogically characterised in detail in previous works (Hiller etal. 2021; Jurkovič etal. 2019) and in a recent study of Zarzsevszkij et al. (2023). In this study, all soil samples were subjected to optical microscopy (Carl Zeiss Jenapol, type 30-G0060). Scanning electron microscopy (SEM; TESCAN VEGA3XMU) equipped with an energy dispersive X-ray spectrometer (EDS; Bruker QUANTAX200) was used only with sample POP 2 to visualise grain morphology and semi-quantitative determination of chemical composition. Iron oxides identified by optical microscopy were refined by Raman spectrometry. The Raman spectra of the samples were measured using Thermo Scientific DXR3xi Raman Imaging Microscope (Thermo Fisher Scientific, USA). Excitation laser wavelengths of 780 nm and 532 nm, 50 × objective, a 25 μm confocal pinhole, and an EMCCD detector were used in the study. Microbiological characterisation of soils The basic microbial parameters were determined according to the criteria of Nielsen and Winding (2002): measurement of abundance and biodiversity of soil microorganisms, measurement of total organic carbon, microbial biomass carbon and identification of key species of autochthonous microorganisms. Isolation, cultivation, and identification of the microbial strains Bacteria were isolated using the dilution plate method (Jones etal. 1948) on Tryptone Soya Agar (HiMedia Laboratories Ltd, Mumbai, India) and cultivated at 30 °C for 24–48 h. All colonies displaying any morphological variety were selected and inoculated into the original nutrient medium to acquire pure bacterial strains. The biodiversity of microorganisms was determined with the BIOLOGTM system (Biolog Inc., USA), specifically with identification assays GEN III MicroPlate TM and FF MicroPlate TM. Microbial biomass carbon The microbial biomass carbon was determined with the chloroform fumigation extraction method performed according to ISO norm 14240-2:1997. The method is based on the cell lysis induced with chloroform vapour, which causes the protoplasm released into the soil solution. Subsequently, the protoplasm is extracted with potassium sulphate. The content of the carbon bound in the microbial biomass (Cmic) is then determined from the extract by titration with Mohr salt (Vance etal. 1987). Microbial activity Soil respiration (CO2B) was daily monitored through the measurement of CO2 released under aerobic incubation of 50 g of soil at 25 °C for 7 d (Alef and Nannipieri 1995). Carbon dioxide was measured by titration with NaOH after precipitating the trapped CO2 with barium chloride. While determining the potential respiration (CO2P), the soil sample was supplemented with 10 g of glucose. The metabolic quotient (qCO2) was calculated as the ratio of CO2B to Cmic, expressed as mg CO2.kg–1Cmic.h–1. Microbial quotient (qMIC) was calculated as the ratio of Cmic to TOC, expressed as the percentage (%) (de Cassia Lima Mazzuchelli etal. 2020). Single extractions with distilled water (H2O) and ammonium nitrate (NH4NO3) The extractions using H2O and 1 M NH4NO3 solution were performed according to the norms EN-124572:2002 (EN 12457-2 2002) and DIN ISO 19730:200907, respectively. Distilled water extracts the easily 179 Plant Soil (2024) 497:175–197 1 3 Vol.: (0123456789) mobile fraction of metal(loid)s, while the 1 M NH4NO3 solution targets the plant-available fraction (Rao etal. 2008). A 10 g of dried sample was weighted into a 100 mL polyethylene centrifuge tube and mixed with H2O (pH = 5.77, EC = 15.8 μS.cm–1) or unbuffered 1 M NH4NO3 solution at ratios of 1:10 or 1:2.5 (w/v), respectively. The tubes were sealed and shaken at 30 cycles.min–1 for 24 h (distilled water) and at 180 cycles. min–1 for 2 h (NH4NO3) on end-over-end shaker (MultiRS-60, Biosan), centrifuged at 3000 rpm for 10 min (Universal 320 R, Hettich) and finally filtered through a 0.45 μm filter. The filtrates were acidified with ultrapure HNO3 and stored at 4 °C until chemical analysis. Bacterial strains used for bioleaching Strain Cupriavidus metallidurans CCM 7663T (Taxonomy ID: 266264) (Fig.S1) was first isolated from the decanting tank in the process of galvanising when its excellent resistance properties to zinc ions were identified (Makkar and Casida 1987; Mergeay etal. 1985). In subsequent studies, significant resistant abilities of this strain to other metals were confirmed (Vojtková etal. 2012). Bacterial strain Cupriavidus oxalaticus CCM 7669T (Taxonomy ID: 96344) (Fig.S2) was first isolated from the digestive tract of earthworms as oxalate-degrading bacteria (Khambata and Bhat 1953) and it shows an excellent ability to adapt to high concentrations of metals because of its genetic variability (Collard etal. 1994). Bacterial strains, both obtained from the Czech Collection of Microorganisms in Brno, were stored on gelatin discs, and revived by CCM methodology for reviving of cultures on gelatin discs. Tryptone Soya Broth (casein enzymic hydrolysate 17.0 g.L–1, soya peptone 3.0 g.L–1, NaCl 5.0 g.L–1, K2HPO4 2.5 g.L–1, dextrose 2.5 g.L–1, pH = 7.3±0.2; HiMedia Laboratories) and Tryptone Soya Agar (casein enzymic hydrolysate 15.0 g.L–1, papaic digest of soya-bean meal 5.0 g.L–1, sodium chloride 5.0 g.L–1, agar 15.0 g.L–1, pH = 7.3±0.2; HiMedia Laboratories) were used as medium for reviving the culture. Biostimulation and bioaugmentation of indigenous microorganisms The two types of media were tested to enhance the activity of autochthonous microorganisms to intensify their As and Sb bioleaching performance. The first type of medium was liquid non-modified Sabouraud Dextrose Broth (SAB) medium (special peptone 10.0 g.L–1, dextrose 20.0 g.L–1; HiMedia Laboratories). The bioleaching was performed in Erlenmeyer flasks containing 1 g of soil sample and 100 mL of liquid SAB medium. In the second type, a 1 g sample was weighed into the Erlenmeyer flasks and 100 mL liquid SAB medium enriched with 20.0 g.L–1 glucose (D-(+)-Glucose, anhydrous) was added. Beside the evaluation of bioleaching through stimulated indigenous microbiota, the bioaugmentation using the inoculum of bacterial strains of genus Cupriavidus was also performed to stimulate the bioleaching. One g of soil with 90 mL of liquid SAB medium in Erlenmeyer flasks was inoculated with 10 mL of Cupriavidus metallidurans or Cupriavidus oxalaticus in exponential growth phase. The biotic controls without addition of bacterial inoculum contained 1 g of soil sample poured with 100 mL of distilled water. All treatments were incubated under static laboratory conditions for 28 d at 25 °C in the dark. After cultivation, the obtained leachates were filtered through 20 μm filter paper and analytically measured for total dissolved As and Sb concentrations. All leaching tests were performed in triplicates and data were expressed as arithmetic mean±standard deviation (SD). Chemical analyses Active ( pHH2O ), exchangeable (pHKCl) soil reactions and electrical conductivity ( ECH2O ) were measured in soil-water suspensions and 1 M KCl solution at a ratio of 1:2.5 (wt:wt) according to the methods described in the official methodology for soil analysis (Fiala 1999) using a WTW Multi 350i instrument equipped with SenTixR41 and TetraConR325 electrodes until reproducible values were obtained. The values of pH and EC were also obtained in a saturated soil paste (pHpaste and ECpaste) prepared by adding distilled water to the soil sample until a slurry was obtained. Total, organic and inorganic carbon contents (TC, TOC and TIC, respectively) were determined with a Ströhlein TOC Analyzer C-mat 5500. The TC was measured by combustion of 0.05 g of sample (ground to analytical fineness and dried at 110 °C) in an oxygen atmosphere at 50 °C to 1000 °C. Inorganic carbon was removed using hot HCl and TOC was determined in the insoluble residue. The TIC was calculated as the difference between TC and TOC. The 180 Plant Soil (2024) 497:175–197 1 3 Vol:. (1234567890) accuracy of the measurements was checked by world standards and comparative samples. The carbonate content (CaCO3%) was obtained by decomposing the samples in 7 M HCl and measuring the released volume of CO2, and the grain size distribution using the hydrometer method (Gee and Bauder 1986). Trace metalloids (As, Sb) were analysed by inductively coupled plasma-optical emission spectroscopy ICP-OES after microwave-assisted total digestion in an acid mixture of HNO3/HCl/HF, evaporated and then dissolved in diluted aqua regia. The target metalloids measured in the standard reference material 2711a (Montana II soil) were within the certified values with relative difference (RD) values between 5–12%. Arsenic and Sb concentrations in the leachates from all types of extractions were determined by atomic absorption spectrometry (AAS; Varian Spectr AA 220) equipped with a hydride generation system (HG; VGA 76). The detection limit was 1.0 μg.L–1 for both As and Sb. All determinations of metalloid concentrations were performed by laboratories EL, Ltd., Spišská Nová Ves, Slovak Republic, fulfilling the accreditation requirements of ISO/IEC 17025:2017. Results Physico-chemical and mineralogical properties The solid samples showed variable pHH2O and pHpaste values (3.85–7.45 and 3.38–7.54, respectively) as well as CaCO3 content (<0.08–7.67%), which was positively related to pH H 2O /pHpaste and total inorganic carbon (TIC), respectively (Table 1). The sample POP 2 near the mine buildings had the highest pH H 2O , probably due to neutralisation by weathering construction materials. The total organic carbon content (TOC) in sample POP 1 (2.62%) was higher than in soil samples POP 2–POP 4, which had TOC in the range of 0.10–0.91% (Table1). The grain-size distribution among the soils was very similar; sand significantly predominated over silt and clay (sandy loam), and only sample POP 4 contained more silt than sand (silt loam). The total concentrations of As and Sb in mine soils ranged from 15.0 mg.kg–1 to 1463 mg.kg–1 and from 1022 mg.kg–1 to 5825 mg.kg–1, respectively. The higher concentration range of Sb compared to that of As was due to the fact that the main ore mineral in the Table 1 Physico-chemical properties of mine soils taken from the forested area (POP 1) and sites covered with tailings (POP 2–POP 4) a EC – electrical conductivity, TC – total carbon, TOC – total organic carbon, TIC – total inorganic carbon; b BDL <0.08 % Samples POP 1 POP 2 POP 3 POP 4 pHH2O 4.52 7.45 3.85 6.05 pHKCl 3.71 7.17 3.34 5.92 pHpaste 4.48 7.54 3.38 6.47 EC H 2 O a (mS.cm–1) 213 156 146 51 ECpaste (mS.cm–1) 177 120 55 49 TCa (%) 3.25 1.83 0.21 0.16 TOCa (%) 2.62 0.91 0.10 0.14 TICa (%) 0.63 0.92 0.11 BDLb CO2 (%) 2.31 3.37 0.40 BDL CaCO3 (%) 5.25 7.67 0.92 BDL Grain size distribution (%) Clay 8 8 6 8 Silt 27 32 24 52 Sand 65 60 70 40 Texture Sandy loam Sandy loam Sandy loam Silt loam Total concentrations (mg.kg-1) As 15.3 740 1463 804 Sb 1022 2200 5825 2099 181 Plant Soil (2024) 497:175–197 1 3 Vol.: (0123456789) mined hydrothermal veins was stibnite (Sb2S3). These concentrations significantly exceeded the maximum permissible concentrations of As and Sb in receiving soils recommended by the World Health Organization (As = 8 mg.kg–1 and Sb = 36 mg.kg–1) (Nunes etal. 2021). Indication criteria (ID) and intervention criteria (IT) for industrial soils defined in the national legislation are 65 mg.kg–1 and 140 mg.kg–1 for As, and 25 mg.kg–1 and 80 mg.kg–1 for Sb, respectively. Exceeding the ID limit requires the monitoring of the contaminated area, while when exceeding the IT limit, a detailed geological survey with risk assessments is necessary (Anon 2015). It is obvious that Sb in all soils and As in three soils, excluding POP 1, exceeded several times the respective IT values. The sorption and redox capabilities of soils are key factors determining the behaviour and speciation dynamics of released contaminants. In particular, redox transitions in iron minerals significantly affect the mobility of chemical elements such as As and other trace metal(loid)s as highlighted by Rinklebe etal. (2016). Since biologically induced phase transformations and contaminant release are intricately mediated by processes such as mineral redox changes, precipitation, dissolution and (de)sorption, mineralogical studies were performed to identify the main constituents that may contribute to these complex interplays. In addition, soil mineralogy affects the growth and structure of the microbial community (Finley etal. 2022). According to X-ray diffraction results of mine soils POP 1 to POP 4 published in Hiller et al. (2021) and Jurkovič etal. (2019), the main minerals were quartz, micas (i.e., muscovite and biotite), carbonates (calcite and dolomite) and clay minerals such as illite, chlorite and kaolinite. Previous studies also demonstrated the abundance of trivalent Fe secondary minerals with varying crystallinity and mass concentration of As, Fe, and Sb. There is a strong evidence that As in the initial soils of tailings ponds does not form its own minerals, being always associated with Fe oxides, while Sb occurs commonly as tripuhyite (FeSbO4) and more rarely as oxides, e.g., valentinite/senarmontite (Sb2O3) and cervantite (Sb2O4) (Jurkovič et al. 2019). As shown in Figs.2 A-L, quartz was the most common mineral of the soils, with its grains frequently covered by Fe oxides and carbonates (Figs.2 G, I, J). The most typical carbonate mineral was dolomite (CaMg(CO3)2) (Fig.2 H), and Fe oxides were dominated by goethite (α-Fe3+O(OH)) and ferrihydrite (Fe3+10O14(OH)2) (Figs.2 K, L). This aspect holds particular significance as the presence of Fe oxides affects the behaviour of metalloids that could be released through bioleaching processes. Entrapment and adsorption of metalloids in the lattice and on Fig. 2 Images of the studied mine soils obtained by optical microscopy in polarised light: A to F – fragments of quartz-sericite phyllites and metabasic rocks (m. rock) with a rim of Fe oxides (Fe-oxides) in sample POP 1; G – quartz grains (qtz), Fe oxides and carbonates (sample POP 2); H – fragment of dolomite (dol) in sample POP 3; I to J – quartz grains (qtz) covered with Fe oxides and K to L – Fe oxides are represented by goethite (goe) and ferrihydrite (fer) as identified by Raman spectroscopy (samples POP 3 and POP 4) 182 Plant Soil (2024) 497:175–197 1 3 Vol:. (1234567890) the surface of Fe oxides, respectively, are regarded as the primary mechanisms governing their mobility in soil (Zhou etal. 2022). As confirmed by SEM with EDS analyses (Figs. 3 A-D and Table S1), these Fe oxides are important reservoirs of the two metalloids with prevalence of Sb over As. Only sample POP 2 was subjected to SEM, however, it is believed to be representative of the qualitative mineralogical characteristics of other mine soils developed on tailings in the area. The predominant association of As and Sb with amorphous and crystalline Fe oxides in soil from the area of Poproč using Wenzel sequential extraction (more than 90% of total As and Sb bound to Fe oxides) was confirmed in the most recent accompanying study of Zarzsevszkij etal. (2023). Microbiological properties The highest abundance of microorganisms (bacteria and fungi) was found in sample POP 1 that was collected from a forested mine waste heaps above the Agnes adit (Fig.1). Among the samples, POP 1 was the least mine-impacted and had rather the properties of forest soil, which was indirectly confirmed by its highest TOC content (Table1). The diversity of microorganisms isolated from the samples POP 1–POP 3 was analysed by the BIOLOGTM system and is presented in Tables S2 and S3. The results showed that Bacillus genus participated in the highest confirmed abundance in all three soils. Based on the detailed taxonomic analysis, isolated bacteria belonged mainly to four phyla: Firmicutes (40.0%), Actinobacteria (18.2%), α, β and γ-Proteobacteria (38.2%) and Bacterioidetes (3.64%). Among the abundant cultivable bacteria were those belonging to the genera Paenibacillus, Arthrobacter, Micrococcus, Rhodococcus, Cupriavidus and Pseudomonas. The bacterial diversity in the soils suggested their capability to adapt and prosper in their own ecological niche. In addition, four species of Cupriavidus genus were isolated among β-Proteobacteria. Their cultivability and tolerance to high metalloid concentrations indicate an adaptability of Cupriavidus genus, and Fig. 3 Selected SEM images of mine soil sample POP 2 acquired in backscattered electrons and representative EDS spectra (see also TableS1 for EDS results of individual analytical points in wt.%). A) Overview image of metal(loid)-containing grains and their spatial distribution in the contaminated soil, fragments of the mine tailing material; B) Silicate particle with a possible formation of iron oxide rim containing high concentrations of hazardous metal(loid)s (As 3.7 wt.%, Sb 23 wt.%, Pb 1.1 wt.%); C) Iron oxide cluster with increased concentrations of As, Sb, and Pb; D) Iron oxide particle with up to 5 wt.% of As and up to 5 wt.% of Sb, tiny monazite fragment Table 2 Microbiological properties of mine soil samples a Cmic – microbial biomass carbon content, CO2B – basal respiration rate, CO2P – potential respiration rate, SAI – substrate availability index (ratio of CO2P to CO2B), qMIC – microbial quotient (ratio of Cmic to TOC), qCO2 – metabolic quotient (ratio of CO2B to Cmic) Property Unit POP 1 POP 2 POP 3 TOC % 2.62 0.91 0.10 Cmic amg.g–1. 1.218 1.099 0.654 CO2Bamg.g–1.h–1 0.024 0.020 0.011 CO2Pamg.g–1.h–1 0.094 0.076 0.042 SAIa3.96 3.80 3.86 qMICa% 60.9 73.3 36.3 qCO2 amg.mg–1Cmic.h–1 0.020 0.018 0.017 Number of different isolated bacterial species 42 35 31 Number of different isolated fungal species 16 9 6 183 Plant Soil (2024) 497:175–197 1 3 Vol.: (0123456789) therefore, potential for bioextraction of metalloids. Among the microscopic fungi, three phyla were isolated: Ascomycota (68.2%) Basidiomycota (9.52%) and Zygomycota (23.8%) (TableS3). The most abundant genus in the soils was Aspergillus (28.6%), followed by Cladosporium, Neosartorya, Paecilomyces, Penicillium, Bjerkandera, Irpex, Absidia, Mucor and Rhizopus. Finally, it was shown that the soil microbiocenosis survived in the environment with high concentrations of metal(loid)s. The microbial properties of mine soils are summarised in Table 2. The highest value of microbial biomass (Cmic) exhibited sample POP 1 (1.218 mg.g–1), followed by POP 2 (1.099 mg.g–1) and POP 3 (0.654 mg.g–1). The mean value of the basal respiration rate (CO2B) varied from POP 3 (0.011 mg.g–1.h–1) to POP 2 (0.020 mg.g–1.h–1) and POP 1 (0.024 mg.g–1.h–1). The presence of glucose showed the expected increase in respiration with potential respiration (CO2P) values of 0.042, 0.076 and 0.094 mg.g–1.h–1 in POP 3, POP 2 and POP 1, respectively. According to the CO2P/CO2B ratio (substrate availability index (SAI)), the highest microbial activity was in sample POP 2 due to the presence of easily usable organic substances. The microbial quotient (qMIC) reflects how efficiently soil organic matter is used by microorganisms (Pankhurst etal. 2002). The highest value, 73.3% was calculated for sample POP 2. The metabolic quotient (qCO2) as the rate of microbial respiration referred to Cmic, indicates the ability of soil microbes to utilise soil organic matter. It is an indicator of eco-physiological properties and community changes. Only small differences in qCO2 were observed. Table 3 Extracted concentrations (mg.L–1) and fractions of the total As and Sb concentration (%) using short-term batch extractions with distilled water and 1 M NH4NO3 solution. The final pH values of the suspensions are also indicated. Arithmetic mean (standard deviation; n =3) Extraction with distilled water Extraction with 1 M NH4NO3 solution Concentration (mg.L–1) Extractability (%) Concentration (mg.L–1) Extractability (%) pH As Sb As Sb pH As Sb As Sb POP 1 6.91 (0.52) 0.03 (0.00) 0.42 (0.08) 1.96 (0.09) 0.41 (0.08) 4.23 (0.01) 0.01 (0.00) 0.14 (0.00) 0.19 (0.01) 0.03 (0.00) POP 2 7.36 (0.18) 0.33 (0.00) 0.49 (0.02) 0.45 (0.00) 0.22 (0.01) 7.25 (0.08) 0.25 (0.11) 0.71 (0.07) 0.09 (0.04) 0.08 (0.01) POP 3 4.30 (0.08) 0.04 (0.00) 5.55 (0.32) 0.03 (0.00)) 0.95 (0.05) 3.61 (0.06) 1.41 (0.04) 0.73 (0.03) 0.24 (0.01) 0.03 (0.00) POP 4 6.00 (0.40) 0.37 (0.10) 2.25 (0.65) 0.46 (0.12) 1.07 (0.31) 5.76 (0.00) 0.04 (0.00) 0.69 (0.05) 0.01 (0.00) 0.08 (0.01) Table 4 Leached concentrations of As and Sb from mine soils after biostimulation of autochthonous microflora with SAB liquid medium (SAB) and SAB liquid medium plus glucose (SAB+GL) and the respective extractabilities expressed as the percentage of the total concentration in soil. The BC treatment is a biotic control without biostimulation. Arithmetic mean±standard deviation (in parentheses; n = 3) Leached concentration (mg.L–1) Extractability (%) Soil sample Treatment pH As Sb As Sb POP 1 SAB 5.83 (2.56) 0.15 (0.01) 1.49 (0.15) 98.6 (0.92) 14.6 (2.93) SAB+GL 3.85 (0.02) 0.12 (0.03) 0.68 (0.28) 81.0 (3.69) 6.69 (5.42) BC 0.04 (0.00) 0.01 (0.00) 25.0 (16.9) 0.06 (0.00) POP 2 SAB 4.19 (0.09) 1.41 (1.92) 3.35 (0.36) 19.1 (5.20) 15.2 (3.27) SAB+GL 4.14 (0.16) 2.73 (0.29) 4.07 (0.90) 36.9 (0.78) 18.5 (8.14) BC 2.19 (0.00) 1.82 (0.00) 29.5 (0.00) 8.25 (0.00) POP 3 SAB 5.98 (3.03) 5.30 (0.27) 5.28 (0.48) 36.3 (3.62) 9.06 (1.64) SAB+GL 3.49 (0.41) 6.98 (0.73) 2.80 (0.91) 47.7 (9.96) 4.80 (3.12) BC 3.21 (0.00) 2.23 (0.00) 22.0 (0.00) 3.82 (0.00) POP 4 SAB 8.09 (0.16) 0.73 (0.06) 3.86 (0.40) 9.04 (1.42) 18.4 (3.76) SAB+GL 4.26 (0.43) 2.98 (0.29) 5.92 (0.24) 37.1 (7.28) 28.2 (2.29) BC 1.29 (0.00) 2.40 (0.00) 16.0 (0.00) 11.4 (0.00) 190 Plant Soil (2024) 497:175–197 1 3 Vol:. (1234567890) catalytic agents, biosurfactants and ultrasound, (ii) application of weak magnetic field or external voltage via electrodes, (iii) illumination of bioleaching systems and (iv) mutation of bioleaching bacteria by UV irradiation. Several strategies enhanced the metal(loid) removal efficiency but many of them failed due to the low resistance of bioleaching bacteria to stress induced by an external agent. To select the appropriate bioleaching approach, it is recommended to conduct a life-cycle assessment in order to compare all possible options (Nguyen etal. 2021). In addition, the bioleaching process will be fully completed when combined with other processes to recover the released metal(loid)s (Nguyen etal. 2021). Biosorption, bioelectrochemical systems (BES) (Liapun and Motola 2023), selective chemical precipitation of the dissolved metals from the biolixiviant using sodium hydroxide (Kremser etal. 2022), sulphide precipitation (Kaksonen etal. 2011) or immobilisation into crystals (Contreras etal. 2013) are just a few of the promising technologies for metal(loid) recovery and their return to the industrial cycles. However, such metal(loid) recovery as the post-bioleaching step is still a technological challenge (Sikander et al. 2022). The combination of bioleaching with the appropriate recovery method represents a biotechnological approach utilising seemingly unprospective waste. Conclusions Mine soils, three samples from tailings ponds and one sample from an old mine heap, co-contaminated with As and Sb (up to 1463 mg.kg–1 As and 5825 mg.kg–1 Sb) were subjected to short-term leaching tests using distilled water and 1 M NH4NO3 solution, and approximately one month long leaching test through biostimulation of autochthonous microbiota and bioaugmentation with two strains of the genus Cupriavidus in aerobic conditions. Both approaches biostimulation and bioaugmentation significantly increased the bioleaching of As and Sb compared to short-term tests as well as non-sterile biotic control. These percentages corresponded to a maximum of 0.74 g of leached As and 1.10 g of leached Sb per 1 kg of the soil at a soil-liquid phase ratio of 1:100. This result suggests the possibility of using biostimulation and bioaugmentation in the simultaneous removal of As and Sb from contaminated solid matrices. However, significantly lower bioleached fractions of Sb than those of As pointed to a difference in behaviour between the two metalloids that could be partially explained by a different solid-phase speciation of Sb compared to that of As. There are still open questions that could explain the observed difference in bioleaching between As and Sb, probably related to the speciation of metalloids in the liquid phase and the degree of their complexation with dissolved organic matter and metabolites secreted by microorganisms. Therefore, to shed more light on the release mechanism of these metalloids mediated by microorganisms, further research focused on speciation behaviour and the role of complexing agents in the mobilisation of As and Sb is necessary. Acknowledgments We would like to thank three anonymous reviewers for their criticism and valuable comments that contributed to the improvement of the original version of the manuscript. The authors would like to thank Noemi Mészárosová (CAS) for her analytical work. Author Contributions Experimental setup, material preparation, data collection and analysis concerning the bioleaching experiment were performed by K. Schwarzkopfová, Ľ. Jurkovič, T. Faragó and M. Urík. The microbiological characterisation of soil samples was performed by K. Boturová, H. Vojtková and H. Horváthová. Mineralogy was studied by T. Faragó, Ľ. Jurkovič and M. Vítková. The original manuscript was written by K. Schwarzkopfová and E. Hiller and it was finalised by H. Horváthová and M. Urík. The manuscript was edited and revised by H. Horváthová and E. Hiller. All authors read and approved the final manuscript. Funding Open access funding provided by The Ministry of Education, Science, Research and Sport of the Slovak Republic in cooperation with Centre for Scientific and Technical Information of the Slovak Republic This research was supported by the Slovak Research and Development Agency under the contract No. APVV-17-0317, APVV-21-0212 (E. Hiller, as the main investigator) and by Project for Specific University Research (SGS) No. SP2023/004 from the Faculty of Mining and Geology of VŠB – Technical University of Ostrava (H. Vojtková, as the co-investigator). This study was supported also by the Operation Program of Integrated Infrastructure for the project, UpScale of Comenius University Capacities and Competence in Research, Development and Innovation, ITMS2014+: 313021BUZ3, co-financed by the European Regional Development Fund (Comenius University in Bratislava, as the fund recipient). Declarations Conflict of interest The authors declare no conflict of interest Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the 191 Plant Soil (2024) 497:175–197 1 3 Vol.: (0123456789) original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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