Bioleaching Techniques for Sustainable Recovery

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1. Introduction

The global market size of metals and their manufactured products was valued at $11.2 trillion in 2020, and it is projected to reach $18.5 trillion by 2030 [1]. This significant growth is driven by the rising demand from diverse end-use industries, such as healthcare, aviation, energy and power, electricity, and electronics [2]. Additionally, metals play a crucial role in the construction of buildings, structures, transportation networks (including bridges and railways), as well as industries like mechanical engineering, transportation, cosmetics, catalysis, and environmental cleanup [3].

An assured supply of metals is critical to economic abundance of countries and national defense. Currently, the United States and other developed nations must import metals, causing tensions between countries partly because supply chains are diminished due to the impact of the COVID-19 pandemic [4].

The market demands metals as sustainable raw materials with high recycled content to reduce the carbon footprint of the final product [5]. Countries such as the United States, Japan, Australia, and Canada support initiatives to secure material supply through diversification, development, and recycling. The agricultural, industrial, and domestic sectors are economically interested in recovering valuable minerals, processing them, and converting them into marketable products [3].

Metal recovery through recycling refers to reprocessing waste into new metal products to reduce greenhouse gas emission levels, conserve natural resources, and manage energy consumption. In Europe, metal recycling in household solid waste is integral to sustainable waste management [6]. Countries such as Canada, the United States, and the United Kingdom, among others, promote the recycling industry with waste collection systems, separation processes, and sorting [7]. Waste management is one of the critical steps to achieving sustainable development and a circular economy [8]. Governments are tightening restrictions on waste generation and opening new landfills, putting pressure on companies to produce more environmentally friendly and sustainable goods [9].

Several metal product manufacturing companies use recyclable and recycled materials to manufacture new metal products [7]. Studies by Moreau et al. show that metals used in renewable energy technologies retain their properties and can, in principle, be recycled. This fact offers more significant potential for a circular economy [10].

It is believed that there will be the availability of material to be recycled, as the recycling market was 217.0 billion dollars in 2020 with a projection of 368.7 billion dollars by 2030 [7], added to the global generation of waste such as electronic waste with values of 42 million tons in 2014 [11], 53.6 million tons in 2019 and an estimated 74.7 million tons by 2030 [12].

Studies show that the amount of metallic fraction in unsorted mixed household waste is 5.4 kg/capita/year, which represents approximately 1.6% by weight of the total solid household waste produced. The metallic fraction of unsorted mixed household waste contains about 0.78 kg/capita/year of aluminum packaging, 2.08 kg/capita/year of metallic packaging, and 2.55 kg/capita/year of other metals. The estimated metal fraction collected from solid household waste is 1.1 kg/capita/year [6].

Recoverable material profit in e-waste was estimated at USD 57 billion in 2019 [12]. For the same year, 70.9% of steel cans were recycled along with other steel packaging types, including strapping and drums, with a 3.6% increase in steel scrap used by country and region [13].

Mixed waste is incinerated, and some metals are recovered before or after the municipal solid waste incineration process. However, the recoverability is limited since a large part of the aluminum is melted and oxidized in these, and the quality of the steel scrap is reduced [6]. In addition, when pyrometallurgical processes are used for metal recovery, organic materials, carbon, and other materials such as graphite anodes are lost after burning in the smelting furnace and cannot be recycled [14].

According to studies by Inman et al., leaching is the most common method for recovering metals from e-waste at different concentrations [4]. Leaching uses inorganic acids, including hydrochloric acid, nitric acid, sulfuric acid, sulfuric acid, phosphoric acid, and organic acids, including oxalic acid, formic acid, citric acid, tartaric acid, maleic acid, ascorbic acid, malic acid. Inorganic acids have advantages such as low cost and high leaching efficiency, although they cause equipment corrosion and secondary contamination. Leaching with organic acids can achieve the same efficiency in a milder environment, although their price is higher than that of inorganic acids, which restricts their large-scale industrial application [15].

Hydrometallurgy provides advantages for the recycling of materials, such as higher efficiency, excellent metal selectivity, lower energy consumption, and reduced emissions of hazardous gases; it faces challenges such as the production of wastewater [16] and costs due to its multiple stages in the process [14], which provides a strong motivation to study more sustainable chemistries [16].

In contrast, biohydrometallurgy brings added value to these processes, as they can recover quantities of metals using aqueous solutions and biological metabolites produced by certain microorganisms [17]; bioleaching, for example, is considered one of the green technologies for metal recovery, offering low cost in terms of installation and operation, low energy consumption, no toxic waste generation and low capital investment [1,18,19,20].

In the bioleaching process, metals are solubilized from insoluble solid substrates [1], either directly by the metabolism of microorganisms or indirectly by the products of their metabolism, such as the production of organic acids, chelating agents, amino acids, and complexing agents obtained from heterotrophic bacteria or fungi [21].

Bioleaching has received attention in a variety of industrial areas, especially in mineral and solid industrial waste materials (e.g., galvanic sludge, sewage sludge, fly ash, electronic waste, spent petrochemical catalysts, medical waste, spent batteries, residual slag), where the concentration of metals is low, where the presence of certain elements would result in smelter damage, or where environmental considerations favor biological treatment options. This process also allows the recovery of metals from low-grade sulfide ores and concentrates that cannot be economically processed by conventional techniques, as well as the production of concentrated solutions of metal salts, which could be recycled [18].

This work is a review of the bioleaching process as a sustainable alternative for the recovery of metals from solid matrices such as agricultural, municipal, and industrial waste such as animal feces, peel, and vegetable waste, crop residues, municipal solid waste, mining waste, especially of low grade, ash from combustion processes, electronic waste, used batteries, metallurgical slag, among others. The bio-extraction of metals from these matrices contributes to cycle closures and, in turn, to sustainable processes.

2. Recovery of Metals of Interest from Solid Matrices

The concept of solid matrices refers to a diverse range of waste materials generated from various sources, including agricultural, municipal, and industrial activities. These solid matrices often contain a significant amount of valuable metals, but their recovery can be challenging due to their complex composition and low metal concentration.

Biotechnology is a promising alternative to current industrially available technologies. One of the emerging technologies is the bioprocessing of waste materials to recover metals [11].

The recovery processes of metals of interest by biological methods involve three stages: the first is the extraction of the solute from the solvent using bioleaching, the second is the concentration process using biosorption/desorption, and the third is the deposition of the metal as a species in concentrated solution as a precipitated solid phase. Figure 1 shows a block diagram summarizing the process.

Bioleaching is the first stage where the metals of interest, such as Au, Ag, As, Co, Cu, Mn, Mo, Ni, U, V and W, and Zn, among others, are extracted from primary ores and solid matrices in general. The growing academic and commercial interest in the bioprocess is attributed to its better environmental profile, ease, and practicality of operation, better profitability, the potential for future development, and excellent selectivity with metals. Metals are extracted from solid matrices even in low concentrations [11]. In this bioprocess, solid matrices with metal content (SMMC) such as mining waste (tailings—low-grade ore), consumer waste such as electronic scrap, used batteries, municipal solid waste, and agricultural waste are used as raw materials, moving towards a circular economy, which is considered a green alternative with lower energy costs and environmental impacts compared to traditional metallurgical processes [12].

The second phase is the concentration of metals in the solution, where the biosorption/desorption process is employed. Biosorption is carried out in continuous systems in packed bed columns with microorganisms immobilized in porous matrices, as shown in the study by Ramírez et al. [22]. The use of residual yeast or fungi from the [23] industry is recommended, especially from the brewing industry, due to their volume of generation, easy acquisition, and low cost.

After the adsorption process, desorption is carried out; in this process, the aim is to separate and recover the metals retained in the packed bed column so that a concentrated solution of these metals is generated. For the desorption process, various extracting solutions or eluting agents are used, such as chelating agents (EDTA), acidic solutions (HCl, H₂SO₄, HNO₃), inorganic and organic salts (NaNO₃, Ca(NO₃)₂, sodium citrate), among others [24,25]. This process protonates the active sites of the microorganisms immobilized in the column, activating them again [25,26], which makes the development of the following adsorption process more efficient and allows the reuse of the packed column [24,27].

In the third phase, the metal as a concentrated solution species is deposited as a stable solid phase using conventional chemical methods such as precipitation and electrodeposition or reduction processes [12], which employ reducing agents that lower the redox potential such as SnCl₂, FeSO₄, SO₂. Recently, organic reducing agents such as thiourea, glucose, sucrose, lactose [28], and even cellulose, hemicellulose, and lignin present in different biomasses are being explored, which are “greener” due to their low toxicity and produce less harmful gas emissions compared to inorganic reductants [29,30].

3. Solid Matrices as a Metal Source

Metal supply depends on specific geological, physical, and industrial conditions, so one supply metric does not fit all metals [10]. With waste production, a growing pool of metals is created, a pool of renewable resources that can replace limited metals from enrichment deposits in the geosphere [5].

Waste is defined as an object or substance that is discarded after its initial use. The broadest category of waste is solid waste, which can be divided into different types, agricultural waste, municipal solid waste, and industrial waste [31].

More than 12 billion tons of solid waste are produced annually worldwide [31], including approximately 1.55 billion tons of agricultural waste [32] and about 2 billion tons of municipal solid waste [31]. The generation of industrial waste is almost 18 times greater than that of municipal solid waste [33].

The wastes mentioned above contain metals in various concentrations [3,6,33,34,35,36,37,38,39,40], which have the potential as matrices to be subjected to the process of extraction of metals in the form of dissolution using the bioleaching process.

Figure 2 shows the different solid matrices with metal contents (SMMC) with the potential to be recovered by bioleaching.

3.1. Agricultural Residues

Crop residues are relevant raw materials for metal extraction. Residues such as peanut shells, cow horn, corn cob ash, sugar cane bagasse, and rice husk are rich in silicon, calcium, magnesium [3,41], and other trace elements such as Fe, Al, P, Mg, Zn, and Mn [42].

Meanwhile, based on the FAO’s State of Food and Agriculture (2019) report, approximately 14 percent of global food (estimated to be worth USD 400 billion annually) still becomes lost post-harvest and before it reaches the market. Furthermore, as per the UNEP’s Food Waste Index Report, an additional 17 percent of our food is wasted in retail and by consumers, primarily in households. According to FAO’s calculations, the combined amount of lost and wasted food could provide sustenance for 1.26 billion undernourished individuals each year [43].

At a regional level, Sub-Saharan Africa has the highest losses at 21.4 percent. Least Developed Countries (LDCs) and Small Island Developing States (SIDS) also experience significant losses, with 18.9 percent and 17.3 percent, respectively. Structural deficiencies in these regions result in substantial food losses between the farm and retail levels. East and Southeast Asia also report significant food losses at 15.1 percent, mainly due to significant losses in the fruit and vegetable value chains. The lowest losses occur in Latin America and the Caribbean (12.3 percent) and Europe and North America (9.9 percent). All regions, except for Central and Southern Asia, record an increase in estimated losses in 2020 compared to 2016, with the highest increases observed in SIDS (an additional 1 percent), Oceania (an additional 1.2 percent), and North Africa and Western Asia (an additional 1.7 percent) [43].

It is estimated that the global percentage of food lost after harvest in farming, transportation, storage, wholesale, and processing was 13% in 2016 and 13.3% in 2020. These percentages correspond to a food loss index of 98.7 in 2016 and 101.2 in 2020 [44].

Even some typical wastes, such as ashes from sugarcane bagasse, rice husk, corn cob, bamboo leaf, corn stalk, and palm kernel husk, are regularly employed as metal matrices to reinforce materials [41].

On the other hand, the chemical composition of coconut shell contains mainly calcium oxide, followed by silica, along with traces of Al, K, Fe, and P, in the form of oxides or chlorides [3]. Corn leaves and cacao plants contain Cd [39], cattle manure constitutes an essential source of metallic elements such as Zn and Cu [35], and pig manure contains Cu, Zn, and Mn [36].

Studies by Ramírez-Carmona et al. resulted in a map of agricultural biomass residues in Antioquia, Colombia, showing the metal concentrations of 92 species and the Tm/ha produced per crop. For example, metals are found in papaya residues, 1993 mg/kg of P and 6800 mg/kg Mg; branch onion residues, 1060 mg/kg of P and 10,807 mg/kg of Fe; paprika residues, 680 mg/kg of P; and citron residues, 104,000 mg/kg of Ca, among others [42].

3.2. Municipal Solid Waste

Over 2 billion tons of solid urban waste is generated annually, with approximately 33% being improperly managed. This mismanagement poses significant health and environmental risks, including water, soil, and air contamination. Improper disposal methods such as open burning of hazardous waste not only harm waste workers and neighboring communities but also increase the vulnerability of children to adverse health outcomes [45,46].

Thirty-seven percent of municipal solid waste is disposed of in landfills, 33% in open spaces; 19% is recycled, and 11% is incinerated. These wastes contain metals due to industrial and anthropic activities [47], involving metals such as Zn, Pb, Cu, Cr, Hg [37,48,49,50], Cd [37,48,49], Ni [49], Co and As [37]. In addition, household wastes such as eggshells are rich in Ca [33]. In the study by Kuusiola et al., the compositions of the metal fractions of 54% tinned steel, 15% stainless steel, 24% aluminum, and 8% other metals are shown [6]; likewise, in landfills, the concentrations of leached metals are 108.5 g/Mg of Pb, 90 g/Mg of Cu, 560 g/Mg of Zn, 101.5 g/Mg of Cr and 2.24 g/Mg of Cd [48].

In municipal solid waste incineration processes, metals such as Zn, Cu, Cr, Pb, Ni, Cd, and Hg are found [49,50]. Zhang et al. reported that after 15 days of bioleaching, 80.7–82.1% of Cd, 72.5–74.1% of Zn, 42.8–43.9% of Cu, and 24.1–25.2% of Cr and 12.4–13.0% of Pb were removed [49].

Similarly, studies in Poland showed that metal concentrations in the soil near the municipal solid waste landfill were similar to geochemical reference levels in forest and agricultural soils [48].

3.3. Industrial Wastes

Industrial waste is produced by industrial activity, including any material rendered useless during manufacturing, such as from factories, industries, mills, and mining operations. Industrial waste includes soil and gravel, masonry and concrete, and electronic waste, among others [8].

Every year, American industrial facilities generate and dispose of around 7.6 billion tons of industrial solid waste. Additionally, approximately 54 million tons of e-waste, including electronic devices like TVs, computers, and phones, are produced annually, with a projected increase to 75 million tons by 2030. However, in 2019, only 17% of e-waste was documented as being adequately collected and recycled. Improper management of e-waste and its components poses significant risks, leading to adverse health and developmental effects, particularly in young children [46,51].

Metallurgical slag is among the most abundant by-products generated by such industries [3,9]. The production of this waste is used to recover iron [52]. On the other hand, titanium is concentrated in the blast furnace titanium slag as vanadium titanomagnetite, which contains SiO₂, Al₂O₃, CaO, and MgO [53], and the solid residues from silica sand purification contain metals such as Ba and Cd [3].

Raw materials for vanadium products include the vanadium–titanium magnetite, vanadium slag, coal, petroleum coke, fly ash, and spent catalysts [54].

The WEEE, commonly called e-waste, contains up to 60 different elements in various concentrations, comprising base metals, critical metals, and platinum group metals mixed in a complex matrix of metallic and non-metallic materials [11,55]. For example, Au, Ag and Pd, Cu, and Ni are recovered from used cell phone printed circuit boards, with 540–880 mg/kg Ag, 168 mg/kg Au and 110 mg/kg Pd [33,34].

Industrial wastes such as fly ash, gypsum, and red mud are alumina, silica, and zeolite sources. Likewise, sewage sludge ashes contain metals such as Cu, Cr, Cd, Ni, Pb, Zn, and Co [39,40,56].

Finally, depleted mines, although they increase the percentage of waste generated [9], contain a diversity of metals in low concentrations [57] that can be extracted by biological rather than chemical methods, as mentioned above.

4. Bioleaching

Leaching is a chemical method for extracting metals of interest [58]. Leaching, peroration, or solid/liquid extraction all involve an operation that consists of extracting with the help of a potentially soluble component a solute that is in solid form accompanied by other undesirable solids [59].

In general, in a leaching process, there are three components:

A: solid solute that goes into the solution;
B: inert solid (insoluble in S);
S: extracting solvent.

In bioleaching, the function of the solvent is performed by microorganisms, by the action of either bacteria or fungi, as they participate in the biogeochemical cycle of minerals in direct ways by the metabolism of the microorganisms or indirectly by the products of their metabolism [21,60].

Therefore, bioleaching is defined as the solubilization of metals from insoluble solid substrates [21]. In the case of employing bacteria, they use the mineral as a substrate, capturing electrons for their metabolic processes and releasing heat and metals without needing any external energy to carry out the process [61]. In the case of fungi, they produce organic acids, which leach metals from solid matrices. Microorganisms can also excrete ligands that stabilize the metal by forming metal-rich complexes [62].

Metal solubilization can be facilitated by biologically produced amino acids, cyanide, and thiosulfate [62]. In addition, microorganisms can participate in the redox cycling of iodine [63], which is a potential alternative leachant for obtaining the metal and decreasing metal solubility by consuming ligands that are bound to the metal or by biosorption, enzymatic reduction, and precipitation, and by employing the metal as a micronutrient, as shown in Figure 3.

As mentioned above, SMMC metal bioleaching processes can be carried out using bacteria or fungi; the decision-making for the selection depends on the objectives to be achieved in the bioprocess. Table 1 shows the general features for selecting the bacterial or fungal bioleaching application route.

Bacterial bioleaching is applied when the recovery of a metal of interest is required, and it is not necessary to preserve the properties of the solid matrix. On the other hand, fungal bioleaching is applied when it is necessary to preserve the properties of the solid matrix, especially the crystalline properties, in case it is a mineral SMMC. Furthermore, sterilization and sanitization processes are required in fungal but not bacterial bioleaching due to their resistance to contamination, and because the process is usually performed in one step, which limits the exposure to external contaminants. In contrast, fungal bioleaching is performed in two steps, either by a direct or indirect method.

The operational times differ between the two methods, with bacterial bioleaching being prolonged due to the bacteria acting directly in the process. In contrast, fungal bioleaching has variable times depending on the SMMC/bacteria system and the method used. The indirect method of fungal bioleaching has a longer production time for the leaching solvents (fermented broth) but has a shorter bioleaching process time. The information provided in this table can assist researchers and industry professionals in selecting the appropriate bioleaching method according to their specific metal recovery requirements and constraints.

4.1. Bacterial Bioleaching

Bacterial leaching, also known as bioleaching, biohydro-metallurgy, or bio-oxidation of sulfides, can be defined as a natural dissolution process resulting from the action of a group of bacteria, mainly of the genus Thiobacillus, with the ability to oxidize sulfide SMMC, allowing the release of the metals contained in them [18,64].

Bacterial bioleaching is based on the ability of microorganisms to transform solid compounds into soluble and extractable elements [65] or expose metals contained in ores and concentrates by direct oxidation or indirect chemical oxidation caused by corrosive metabolic by-products generated by electrochemistry, or a combination of both [18].

The attack and solubilization of an SMMC through microorganisms are performed by different mechanisms, which depend on the matrix’s sulfur matrix [66,67].

Similarly, the bioleaching process occurs by the catalysis that microorganisms exert during the dissolution of certain SMMC; for example, microorganisms such as bacteria convert metal compounds into their water-soluble forms and are biocatalysts of these leaching processes [68,69]. The microorganism uses SMMC as fuel, electron transfer for its survival purposes, and releasing metals, without the need for external application of energy. In this type of process, high activation energies are not necessary; proof of this is that the reactions take place at low pressure and some at low temperature, depending on the type of microorganism, whereas other ways need extreme conditions for their development and performance [68].

According to Rodríguez et al. (2001), bacterial bioleaching or leaching is understood as the attack and solubilization of an SMMC through the direct or indirect action of different microorganisms [70].

Microorganisms adapted to bioleaching processes are of two categories:

Autotrophic: These microorganisms obtain nutrients and energy for their life cycles from the inorganic matter surrounding them.
Heterotrophic: They require the availability of organic matter to complete their life cycles.

In both groups or categories of bacteria, some species operate predominantly in the presence of oxygen. These are the aerobic bacteria that carry out, in the first place, the oxidation reactions and have the property of oxidizing metal sulfides to soluble sulfates. Similarly, anaerobic bacteria can function and carry out their life cycles without oxygen; these batteries first conduct reduction reactions [71]. The respective classification is shown in Figure 4.

According to Figure 4, regardless of the bacterial classification, the main characteristic of the microorganisms used in metal recovery is their capacity to evolve in environments with very aggressive or extreme temperatures, pH, and living conditions [68,70].

Some of the bacteria involved are acidophilic microorganisms capable of surviving at low pH levels, high temperatures, and high concentrations of metallic elements, and whose energy source is the oxidation of Fe²⁺ to Fe³⁺ and reduced sulfur compounds [70].

The most significant area within the biotechnological process of metals is focused on the microbial oxidation of sulfide SMMC. Low pH, high metal concentrations, and sometimes high temperatures characterize the aqueous environments associated with SMMC discharges. However, some microorganisms can live, develop and reproduce under these conditions and in these environments. In these environments, microorganisms use reduced sulfur species and certain metals in solution as a primary energy source, resulting in the solubilization of valuable metals [68,72].

According to Rodriguez et al. (2001), in recovery by bioleaching, the main action of microorganisms is direct oxidation through an enzymatic attack or indirect through regeneration of the leaching agent Fe³⁺ of SMMC [70].

In some cases, the bacteria contribute to the weathering of the gangue by liberating the valuable mineral and facilitating its subsequent attack since the sulfuric acid generated by the bacteria produces a rupture of the Si-O and Al-O bonds in the alumino-silicates of the mineral gangue [70].

The microorganisms used in the leaching of metals from ores and concentrates are presented in Table 2. These microorganisms are capable of oxidizing sulfides and sulfur or ferrous iron species. An oxidant (ferric sulfate) is formed when the latter is oxidized.

The bioleaching of A. thiooxidans and A. ferrooxidans contributes via both “contact” and “non-contact” mechanisms. The “contact” mechanism considers that most cells adhere to the surface of the bioleaching substrates. The “non-contact” mechanism is related to redox reactions, such as iron (III) reduction and sulfur oxidation [72,80].

In this sense, there are many and varied definitions of bioleaching. However, what should be made clear is that this leaching can be determined because the raw material studied can be under the direct or indirect action of microorganisms [81].

According to Table 2, a direct mechanism is understood as that which is mediated by bacterial action and where the chemical reactions are catalyzed enzymatically; this option also supposes the physical contact of the microorganisms with the solid matrix [81].

On the other hand, an indirect mechanism involves chemical reactions, enzymatic or non-enzymatic, with no physical contact between the microorganisms and the solid matrix. However, the microorganisms are relevant in forming chemical reagents that can participate in the process [81,82].

The first attempt to explain the mechanism of bioleaching was made by Silverman and Ehrlich in 1964 when they proposed two possible mechanisms [83], as shown in Figure 5.

According to the first possible mechanism, the bacteria attack the metal sulfide directly by adhering to the mineral surface and then enzymatically oxidize it by transporting electrons from the reduced part of the mineral, usually a sulfide, to dissolved oxygen. The general reaction is presented in Equations (1) and (2) [60,65,69].

(1) $M S + 2 O_{2} \to M^{2 +} + {S O}_{4}^{2 -} .$

In the case of pyrite, the above reaction would look like this:

(2) ${F e S}_{2} + \frac{7}{2} O_{2} + H_{2} O \overset{B a c t e r i a}{\to} {F e}^{2 +} + 2 {S O}_{4}^{2 -} + 2 H^{+} .$

The first mechanism proposed (Equation (1)) states that the oxidation of the mineral is carried out by direct enzymatic action, in which the role of the microorganisms is to catalyze the metal sulfide dissolution reaction. The iron-oxidizing bacteria can leach metal sulfides directly without the participation of biologically produced ferric sulfate. The M represents a bivalent metal. The second mechanism, called indirect (Equation (2)), is based on microorganisms oxidizing the minerals by generating ferric ion. In the case of pyrite, the direct transformation of sulfide to sulfate occurs through enzymatic oxidation, where the ferrous sulfate formed is oxidized to ferric sulfate in a later stage by the bacteria [74].

This theory of direct mechanism has been supported by several experimental studies that confirm the adherence of bioleaching bacteria to the surface of minerals. The work presented by Berry and Murr evidence that Acidithiobacillius spp. secrete some substances that can help the attack, although their nature is unknown [84].

Similarly, pyrite crystals exposed to the action of A. ferrooxidans were observed under the scanning electron microscope, detecting traces of corrosion in the crystals and suggesting that the bacteria caused these through a metabolite that could act in three different ways: oxidation of the ferrous ion to ferric, solubilization of the sulfur on the surface of the mineral or by direct attack. In addition, it was found that A. ferrooxidans could discern the most favorable regions of the mineral surface to obtain its energy source and select the site of attack according to the best availability of nutrients. However, the authors, far from using these results in favor of the direct mechanism, have used them to explain the indirect mechanism known as contact leaching [85].

Studies carried out by different authors also detected by electron microscopy the formation of holes on the surface of dissolved sphalerite in the presence of bacteria, and it was concluded that they occurred due to the direct attack of the bacteria on the surface of the mineral [86]. Tributsch studied by SEM the surface of lead sulfide after bacterial attack, showing depressions where the bacteria had been located. This author concluded that the bacteria produced a chemical carrier that promoted the attack at the point of adhesion of the microorganisms [87].

Studies by some authors mention that bacteria breathe using minerals, which provides a new vision of the problem, although, in this case, not related to sulfide minerals [88,89].

In contrast to the direct mechanism, the indirect mechanism considers the action of ferric ions on the sulfide ore dissolving it. Through this chemical leaching reaction, ferrous ions and elemental sulfur are produced. Finally, these chemical species are biologically oxidized to ferric iron and sulfate ions. This mechanism, in principle, does not require the adherence of cells to the sulfide mineral [81,89].

Some of the bacteria mentioned in Table 3 show extraction efficiencies in laboratory experiments with SMMC, such as minerals, sediments contaminated with metals after wastewater treatment, and printed circuit boards, among other materials that can be returned to the production chain once they fulfill their useful life and become waste.

4.2. Fungal Bioleaching

Leaching by fungal action is called fungal bioleaching. It occurs mainly by the action of organic acids produced in the fermentative process [2] when metals are mobilized from solid materials through ligand-induced metal solubilization [121].

The fungi used in producing organic acids, such as citric, oxalic, gluconic, and others, are shown in Table 4. They can be quickly grown using unsophisticated fermentation techniques and inexpensive growth media [122].

In the context of fungal bioleaching processes, it is important to note that while fungi can produce mycotoxins that pose risks in food matrices, these concerns are not typically relevant in industrial processes such as bioleaching. Fungal mycotoxins have been known to cause issues ranging from crop yield reductions and negative impacts on farm animal health to alterations in food quality, organoleptic characteristics, and nutritional value. The associated costs include prevention and decontamination measures [123].

Human exposure to mycotoxins primarily occurs through food consumption, although isolated cases of respiratory-related ailments have been reported. Since food represents the main source of risk for humans, it justifies the inclusion of mycotoxins as one of the molecule groups considered in the Food Safety program. However, in the context of industrial processes like bioleaching, the focus is primarily on harnessing the beneficial capabilities of fungi without significant concern for mycotoxin-related issues, as these processes involve different considerations and control measures [123,124,125].

Fungal cells have a specific structure or organization in the material, where various components are distinguished, such as cell wall, plasma membrane, cytoplasm, mitochondria, endoplasmic reticulum and the Golgi apparatus. Along with its structure appears the function of the cell, which is basically to remain viable, develop and multiply. This function of the cell is mediated by the various components that constitute it [122].

Studies by different authors reveal that the filamentous fungus Penicillium simplicissimum (same as Penicillium janthinellum) is one of the most versatile microorganisms for the biotechnological production of organic acids due to its adaptability to different culture media and its selectivity at a metabolic level to generate multiple organic acids.

Other filamentous fungi such as Aspergillus spp., Fusarium graminearum, Aspergillus fumigatus, and Trichoderma harzianum also produce organic acids [122,126,127,128], mainly by submerged fermentation using different carbon sources (substrates) such as cellulosic waste hydrolysates, cane molasses, glycerol, and even primary alcohols.

There are also solid-state fermentation processes that simultaneously obtain citric and gluconic acid using agro-industrial residues as substrates [129]. However, submerged fermentation systems are preferred to produce the different acids since they allow better control of the process and, therefore, greater productivity of these acids [129,130].

The fungal bioleaching process is carried out by direct or indirect methods, as shown in Figure 6.

Direct method: this method is carried out in one stage where the fermentation occurs: SMMC/culture medium/inoculum (fungus) simultaneously. In the process, the fungus produces the leaching substances, mainly organic acids, and simultaneously extracts the metal contained in the SMMC. The process can take 3 to 10 days depending on the objective, and the pH value of the fermentation usually starts between 6 and 7. As the bioprocess progresses, it reaches pH values between 3.5 and 4, which leads to a decrease in the efficiency of the process because the fungus is inhibited by the presence of SMMC residues [122].

Indirect method: this approach is carried out in two stages [122].

Stage 1: Production of the solvent extractor or fermented broth. Fermentation: culture medium/inoculum (fungus) for 8–10 days. Subsequently, a separation process is carried out, where the biomass is discarded, and the focus is on the fermented broth. This stage generally presents pH values below 3.0.

Stage 2: The fermented broth is in contact with the SMMC, a process that can take 4 to 8 h depending on the SMMC. Subsequently, a separation process is carried out, where the metal-free solid residues are discarded and the focus is on the fermented broth containing the extracted metals (leachates).

Acids are excellent metal leachants from SMMC. Heterotrophic metabolism can also achieve leaching due to the excretion of siderophores and organic acids. These provide protons and metal complexing anions, as citrate and oxalate anions can form stable complexes with many metals [122], including chelates which are relevant in metal dissolution by acidolysis and complex formation mechanisms. In conclusion, the main mechanisms through which organic acids interact with metals (bioleaching reactions) are acidolysis (acid-base reaction), redoxolysis, bioaccumulation, chelates, and complex formation mechanisms [21].

The efficiency of the process depends on the acids produced and their acidity depending on their functional group (e.g., carboxylic or sulfonic). Considering that these acids are not equal in the number of carboxylic groups, hydroxyl groups, and carbon–carbon double bonds in their molecules, they are classified according to their typical characteristics of the carbon chain, saturation, substitution, and functional groups. Table S1 shows the main groups of organic acids, their formula, dissociation reactions, pKa, and corresponding structures [2,131,132].

Based on the Lewis acid-base theory, the ability to release protons is shown by the strength of the acid. The stronger the acidity, the stronger the ability to release protons. For example, oxalic acid (pKa 1.23) shows higher acidic capacity than formic acid (pKa 3.75), implying that the former has higher leaching power provided that the conjugate base of the oxalate anion does not interact strongly with the metal of interest, causing the precipitation of metal complexes [15].

Studies show that oxalic acid (pKa 1.23) leached more iron ions than lactic acid (pKa 3.86). The pKa values of each carboxylic acid indicate that oxalic acid is stronger than lactic acid, which leaches metals more efficiently. In addition, the complexation reaction and the formation of iron oxalates may play a relevant role in increasing the leaching of iron ions, which is confirmed in the leaching of iron contained in kaolin using oxalic acid, which is more effective than when organic acids such as citric, malonic, or acetic acid are used [133]. Oxalates are known for chelating metals, and this can be exploited for the dissolution and separation of metals. The increase in the solubility of simple oxalate compounds in the presence of excess oxalate provides the basis for formation of the oxalate complex [134].

Metallic oxalates display a diverse range of solubilities which are influenced by the particular metal cation and solution conditions. Insoluble oxalates include calcium oxalate (CaC₂O₄), silver oxalate (Ag₂C₂O₄), and lead oxalate (PbC₂O₄). Conversely, sodium oxalate (Na₂C₂O₄) and potassium oxalate (K₂C₂O₄) exhibit high solubility, while barium oxalate (BaC₂O₄) is generally soluble. Transition metal oxalates like iron oxalate (FeC₂O₄) and nickel oxalate (NiC₂O₄) can display variable solubility depending on conditions. Factors such as pH, temperature, presence of other ions, and ligand complexation influence the solubility behavior of metallic oxalates [134].

In bioleaching processes, the binding behavior of oxalic acid is influenced by adsorption of oxalic acid onto metal surface which leads to the formation of an upright mono-oxalate species, with the carboxylate group binding to the surface. This upright orientation enables interactions between the carboxylic acid group and the surrounding environment, resulting in the creation of a chemically functionalized surface. The presence or absence of intramolecular hydrogen bonding determines the various surface species of mono-oxalate. The tilting of the molecules is influenced by surface coverage and temperature, leading to the observation of both unidentate and bridging species [135].

L-aspartic acid can release a total of three protons: two protons from its carboxyl groups and one proton from its amino group. On the other hand, L-tartaric acid does not possess an amino group, and therefore, two acidity constants are reported specifically for its carboxyl groups. In the case of L-glutamic acid, two protons are released from its carboxyl groups, while an additional proton is released from its amino group. Glutamate and aspartate chelate metal ions weakly via the amino nitrogen and carbonyl oxygen bind. A stronger chelation occurs upon amide-nitrogen-bound hydrogen by some metal ions such as Cu²⁺. This reaction occurs in neutral pH conditions (pH ≈ 7) with Cu²⁺ [136].

Several reports have documented the leaching of metals with fungi. Fungi of the genera Aspergillus and Penicillium are among the most effective and relevant for biological leaching due to filamentous fungi’s robust adaptability and ability to tolerate metal contamination stress [21].

Laboratory studies have been carried out using fungi, where only the leaching action is specified according to the type and species of microorganism. For example, A. niger, P. simplicissimum, and P. purpurogenum are related to the production of low-molecular-weight metabolites, mainly organic acids such as gluconic acid, pyruvic acid, citric acid, oxalic acid, malic acid, and succinic acid, different from the mechanism reported for R. rubra, A. thiooxidans and A. ferrooxidans [122].

Some of the most common organisms for fungal bioleaching are the genera Acidithiobacillus, Aspergillus, and Penicillium. For example, Penicillium simplicissimum is used to extract elemental Zn from ZnO. Fungi are also particularly suitable for phosphorus bioleaching, where organic acids such as citric and oxalic acid solubilize P from Fe and Al phosphates. In this process, carboxylic anions compete with binding sites that chelate Al³⁺ and Fe³⁺ [121].

Many microorganisms are reported to solubilize metals in soils, including Aspergillus niger, Penicillium purpurogenum, Rhodotorula rubra, Acidithiobacillus thiooxidans, and Acidithiobacillus ferrooxidans. The mechanism of metal solubilization during the process is related to a chemical process where the binding of microorganisms to the mineral can enhance dissolution [19,69].

Despite successful records of fungal tolerance to metals at the laboratory scale, no documentation of their use at the industrial scale is available [21,137].

In Table 5, fungal bioleaching experiments are presented: operating conditions and metal extraction efficiencies of different SMMC.

According to Table 5, the most important and significant area within the biotechnological process of metals is focused on the microbial oxidation of sulfide minerals. The aqueous environments associated with mine discharges and mining sites are typically characterized by low pH, high concentrations of heavy metals, and, in some cases, elevated temperatures. Despite these conditions and environments, certain microorganisms not only survive but also thrive and reproduce. In these environments, microorganisms utilize reduced sulfur species and certain metals in solution as their primary energy source, resulting in the solubilization of valuable metals [68,72].

Fungal species such as A. niger, P. simplicissimum, and P. purpurogenum are among the most used species in bioleaching and offer advantages over bacterial bioleaching, including the ability to thrive at high pH values and a faster leaching rate [19]. In these studies, pH is a control variable that indirectly indicates the presence or absence of organic acid production during the fermentation processes. pH influences the growth and excretion of organic acids in filamentous fungi. When grown in an unbuffered medium, filamentous fungi often rapidly acidify their environment to very low, and sometimes detrimental, pH values [155,156].

The production of organic acids and other metabolites in the fermentation process is also influenced by the agitation rate. Agitation at low to intermediate levels, ranging from 100 to 300 rpm, increases with agitation speed, whereas agitation speeds between 500 and 800 rpm further enhance it. Citrate synthase activity decreases with increasing agitation speed, while aconitase and isocitrate dehydrogenase activities increase with agitation speed, favoring the transformation of citrate into oxoglutarate [129].

Amino acids such as glycine, histidine, and alanine have been used to test their effect on gold solutions, revealing that the initial dissolution of gold in histidine solution is faster than in glycine and alanine solutions. However, upon extended leaching, it was found that glycine dissolves gold more rapidly and to a greater extent than histidine and alanine [157].

Pulp density plays a crucial role in determining the feasibility of applying bioleaching on a commercial scale. Increasing the pulp density from 1% to 2% (w/v) leads to a significant reduction of 50% in both the volume of leaching media required and the size of the bioreactor. This reduction in size and resource consumption directly translates into a substantial decrease in bioleaching costs. In the bio-hydrometallurgical treatment of low-grade ores, it is common to utilize pulp densities of 10% or higher to maximize efficiency and productivity [158].

5. Future Prospects

The recovery of metals from solid matrices using bioleaching is a promising alternative to traditional metallurgical processes due to its better environmental profile, effectiveness, and high selectivity with metals.

Solid matrices with metal content, such as mining waste, electronic scrap, used batteries, municipal solid waste, and agricultural waste, are potential raw materials moving toward a circular economy. This approach is considered a green alternative with lower energy costs and environmental impacts than traditional metallurgical processes and industrially available technologies for metal recovery.

Additionally, the biomasses produced by these biotechnological processes can be used as soil improvers and can even be used in the biosorption/desorption processes for the concentration of metals in the recovery of metals [23], where these processes are relevant due to the formation of non-soluble compounds between metals and metabolites generated by certain microorganisms.

The use of bioleaching avoids the depletion of non-renewable resources and reduces raw material acquisition costs.

6. Conclusions

Bacterial bioleaching is applied when the aim is to recover a metal of interest without preserving the properties of the solid matrix. In contrast, fungal bioleaching is preferred when it is necessary to preserve the properties of the solid matrix, especially its crystalline properties.

Fungal bioleaching involves a two-step process (direct or indirect), whereas bacterial bioleaching is a single-step process.

Optimal pH for fungal bioleaching varies depending on the microorganism and metal source, ranging from pH 2.5 to pH 10–12.

Temperature and agitation–aeration conditions significantly affect the efficiency of bioleaching, with temperatures ranging from 25 °C to 95 °C and agitation–aeration ranging from 0 to 400 rpm and 100–400 mL/min, respectively.

The pulp density used in bioleaching, ranging from 1% to 10% (w/v), influences the extraction efficiency of metals.

Author Contributions

Conceptualization, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; methodology, C.O.-L.; software, C.O.-L. and L.G.-A.; validation, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; formal analysis, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; investigation, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; resources, C.O.-L. and L.G.-A.; data curation, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; writing—original draft preparation, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; writing—review and editing, C.O.-L., L.G.-A., M.R.-C. and L.R.-C.; visualization, C.O.-L. and L.R.-C.; supervision, C.O.-L.; project administration, C.O.-L.; funding acquisition, C.O.-L., L.G.-A. and M.R.-C. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

g/Mg	Concentration unit equivalent to gram per megagram, or Ton
SMMC	Solid Matrices with Metal Contents
SEM	Scanning Electron Microscopy
WEEE	Waste Electrical and Electronic Equipment
FCC	Fluid Catalytic Cracking

Footnotes

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Figures and Tables

Figure 1. Recovery processes of metals of interest. Source: Authors.

Figure 2. SMMC with the potential to be recovered by bioleaching. Source: Authors.

View Image - Figure 3. Possible roles of microorganisms in mineral processing and recovery. Source: Adapted with permission from Ref. [62]. 2007, Springer Nature.

Figure 3. Possible roles of microorganisms in mineral processing and recovery. Source: Adapted with permission from Ref. [62]. 2007, Springer Nature.

Figure 4. The bacterial classification used in the bioleaching process.

Figure 5. Direct and indirect mechanisms of bioleaching. Adapted from [83].

Figure 6. Fungal bioleaching process. Source: the authors.

Table 1

General features for the application of bacterial or fungal bioleaching. Source: Authors.

Feature	Bacterial Bioleaching	Fungal Bioleaching
Application	Applied when it is required to recover a metal of interest, and it is not necessary to preserve the properties of the solid matrix	Applied when it is necessary to preserve the properties of the solid matrix, especially the crystalline properties, in case it is a mineral SMMC.
		Applied if the final color of the solid matrix is not of interest.
		Applied if not required to separate the fungus from the solid matrix.
Sterilization and Sanitization	Not required	Required
Stages	Performed in one step	Performed in two steps: Direct method (See Section 4.2).
Stages	Performed in one step	Performed in two steps: Indirect method (See Section 4.2).
Operational times	Prolonged due to bacteria acting directly in the process	Direct method: Simultaneous fermentation with leaching can take 3 to 10 days, depending on the target.
Operational times	Process times depend on the SMMC/bacteria system	Indirect method: Production of the leaching solvents (fermented broth): can have a production time of 8 to 10 days, with possible constant production and storage for consumption, without this being the limiting stage. The bioleaching process takes approximately 4 to 6 h, depending on the solid matrix and the metal to be extracted.

Table 2

Bacteria used in bioleaching and their optimum conditions.

Microorganism	Energy Source	pH	T (°C)	References
Acidithiobacillus ferrooxidans	Ferrous iron, sulfide minerals, sulfur, thiosulfate	1.7–3.5	28–30	[73]
Leptospirillum ferrooxidans	Ferrous iron	3.0	30	[74]
Acidithiobacillus thiooxidans	Elemental sulfur, thiosulfate	1.0–3.5	28–30	[75]
Thiobacillus thioparus	Elemental sulfur, thiosulfate	7.0–8.5	28–30	[76]
Sulfobacillus thermosulfidoxidans	Ferrous iron, elemental sulfur, sulfide minerals	2.1–2.5	50–55	[77]
Sulfolobus acidocaldarius	Elemental sulfur, yeast extract	2.0–3.0	70–75	[78]
Sulfolobus brierly	Elemental sulfur, ferrous iron, yeast extract	2.0–3.0	60	[79]
Acidiphilium acidophilum	Elemental sulfur, thiosulfate, yeast extract, salts, sugars, amino acids	2.0–3.0	28–30	[79]

Table 3

Bacterial bioleaching: operating conditions and metal extraction efficiencies of different SMMCs.

Microorganism	SMMC	Metal	pH	T (°C)	Agitation	Pulp Density	Efficiencies	References
A. ferrooxidans, Desulfotomaculum geothermicum	Crushed and screened graphitic schist with a diameter of 8 mm	Iron, zinc, nickel, copper, and cobalt	1.7–2.0	40–50	-	-	In 500 days, the recoveries were Ni 92%, Zn 82%, Co 14%, and Cu 2%.	[90]
A. ferrooxidans	Pyrrhotite, chalcopyrite and arsenopyrite	Iron, copper	2.8–3.2	–	-	-	In 41 days, recoveries were 47.4 mg/L at a pH of 3.2.	[91]
A. ferrooxidans	Dried and crushed sludge at different particle sizes	Gold, copper, zinc, lead	1.8–2.2	30	100 rpm	6.0% (w/v)	In 14 days, the extractions were 4.71%, 9.01% Pb, 12.98% Cu, and 31.88% Zn.	[80]
A. ferrooxidans	Quartz, chlorite, chalcopyrite, albite, pyrite	Aluminum, iron, copper	1.8	30	150 rpm	-	In 5 weeks, metal recoveries were 47.29% Al, 54.41% Fe, and 28.08% Cu.	[92]
A. ferrooxidans FT-22, A. ferrooxidans FT-23, A. ferrooxidans BF, and A. ferrivorans	Albite, quartz, clinochlore, muscovite, illite	Silver, copper	10.5–11.0	25	20–30 rpm	40% (w/v)	In 48 h, the recovery of metals was 51% Ag and 70% Cu.	[93]
Sulfobacillus thermosulfidooxidans, A. thiooxidans, Acidiphilum multivorum, and Leptospirillum Ferriphilum.	Chalcopyrite	Iron, copper	2.0	30	-	1–6% (w/v)	In 11 days, the metal recovery was 28.57% Fe and 39.55% Cu.	[94]
S. Thermosulfidooxidans, A. thiooxidans/A. ferrooxidans, S. thermotolerans, and A. albertensis.	Clay, sand, silt	Zinc, copper, nickel, chromium	1.5–3.1	30	200 rpm	10% (w/v)	In 20 days of operation, metal recovery was 49% Zn, 50% Cu, 65% Ni and 27% Cr.	[95]
Sulfobacillus thermophidus oxidans	Printed circuit board (PCB)	Aluminum, lead, zinc, and tin	-	45	120–145 rpm	0.33% (w/v)	Recovery of 83% Zn, 89% Cu, and 81% Ni in 18 days.	[96]
A. thiooxidans and A. ferrooxidans	Soil contaminated with metals and metalloids	Cadmium, copper, lead, zinc, zinc, chromium, iron	5.6	30	150 rpm	10% (w/v)	In 42 days, metal recovery was 36% Fe and 70% Zn.	[97]
Burkholderia spp. Z-90	Soil contaminated with metals and metalloids	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	3.0	35	180 rpm	5% (w/v)	In 5 days, the maximum metal recovery achieved was 31.6% As, 37.7% Cd, 24.1% Cu, 52.2% Mn, 32.5% Pb, and 44% Zn.	[98]
Shewanella putrefaciens	Soil contaminated with metals and metalloids	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	2.2	30	100 rpm	3% (w/v)	Arsenic recovery was 57.5% in 40 days.	[99]
Acidithiobacillus, Acetobacter, Acidophilum, Acidophilum, Arthrobacter spp., and Pseudomonas spp.	Panchakavya (soil mixture)	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	2.6	30	120–180 rpm	0.2–1% (w/v)	Metal recovery in 5 days was 64% Pb and 49% Cu.	[100]
Massilia spp., Alicyclobacillus spp., and Micromonospora spp.	Soil contaminated with metals and metalloids	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	3.5	30	180 rpm	1% (w/v)	The metal extraction in 10 min was 32.09% Cd	[101]
Myxotrophic acidophiles	Soil contaminated with metals and metalloids	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	2.0	25	175 rpm	4% (w/v)	In 14 days, the two-step bioleaching achieved the extraction of 34% Cd	[102]
Indigenous bacteria	Agricultural land	Zinc, copper, nickel	8.0	28	180 rpm	1% (w/v)	In 9 days, the maximum metal extraction achieved was 74.72% Cu, 35.35% Ni, and 69.92% Zn.	[103]
A. ferrooxidans, A. thiooxidans, and L. ferriphilum	Pyrite and sulfosalts	Aluminum, manganese, iron, copper, zinc, mercury, zinc, mercury	4.0	30	180 rpm	5% (w/v)	In 31 days, the maximum metal recovery was 93.3% Cu, 92.13% Mn, and 96.1% Zn.	[104]
Sulfobacillus thermosulfidooxides and A. caldus	Pyrite and sulfosalts	Aluminum, manganese, iron, copper, zinc, mercury, zinc, mercury	7.5	45	180 rpm	5% (w/v)	Fermentation was carried out for 31 days, and the metal recovery efficiency was 45% As, 89% Cd, 94% Cu, 34% Hg, 95% Mn, and 98% Zn.	[104]
Indigenous bacteria	Port sediments	Copper, chromium, cadmium, lead, zinc	6.0	30	100 rpm	1% (w/v)	During 30 days of processing, the recovery of metals was 29% Cu, 8% Ni, 5% Pb, and 39% Zn.	[105]
Bacteria from exogenous soil	Port sediments	Copper, chromium, cadmium, lead, zinc	8.0	30	100 rpm	4% (w/v)	During 30 days of processing, the recovery of metals was 100% Cu, 95% Cr, 100% Ni, 100% Pb, 100% Zn, 100% Cu, 95% Cr, 100% Ni, 100% Ni, 100% Pb, 100% Pb and 100% Zn.	[105]
A. ferrooxidans and A. thiooxidans	Anaerobic sediment from urban wastewater	Copper, chromium, cadmium, lead, zinc	5.0	25	120 rpm	15% (w/v)	Metal recovery during 57 days was 43% Cu and 80% Zn.	[106]
A. ferrooxidans, A. thiooxidans, and Leptospirillum ferriphilum	Sediment from sewage outfall	Copper, chromium, cadmium, lead, zinc	4.0	30	180 rpm	5% (w/v)	Metal recovery was 90.9% Cu and 94.74% Zn; elements such as Cd, Hg, Mn, and Pb were below 30%.	[107]
A. ferrooxidans	Mining tailings	Copper, iron, cadmium, antimony, zinc, nickel, chromium, nickel, chromium	3.0	30	200 rpm	5% (w/v)	In 20 days, the maximum efficiency achieved was 36.2% Cu, 65.95% Cr, 97.4% Ni, 2.2% Sb, and 34.8% Zn.	[108]
A. ferrooxidans and A. thiooxidans	Mining tailings	Arsenic, zinc, copper, lead	2.5	30	200 rpm	5% (w/v)	Metal recovery in 25 days was 72.2% As, 47.1% Cu, 99.5% Mn, and 78.9% Zn.	[108]
A. ferrooxidans	Mining tailings	Arsenic, zinc, copper, lead	2.0	30	200 rpm	20% (w/v)	The maximum metal recovery achieved in 50 days was 71.37% Fe, 0.82% Pb, and 97.38% Zn.	[109,110]
A. thiooxidans	Tailings from an abandoned and inactive mine	Arsenic, zinc, copper, lead	1.8	40	150 rpm	0.5% (w/v)	Arsenic recovery in 25 days was 47%.	[108,111,112]
A. ferrooxidans	Mine and metallurgical wastes	Lead, iron, copper, zinc	1.5	40	160 rpm	20% (w/v)	In 50 days of fermentation, the metal recovery achieved was 85.45% Fe, 4.12% Pb, and 97.85% Zn.	[109,110]
A. ferrooxidans and A. thiooxidans	Mine tailings deposits	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	6.0	30	200 rpm	5%(w/v)	In 20.8 days, 42.4% As, 45% Cu, 47.7% Fe, 92% Mn, and 67.2% Zn were extracted.	[108,111]
A. ferrooxidans and A. thiooxidans	Mine waste	Arsenic, manganese	2.5	30	200 rpm	5% (w/v)	In 35 days, metal recovery was 96.7% As and 100% Mn.	[75]
Leptospirillum ferriphilum, A. caldus, Sulfobacillus thermosulfidooxidan, A. sulfuroxidans, Ferroplasma acidiphilum, Acidiplasma sp., Sulfobacillus acidophilus, Acidithiobacillus spp., and Acidiphilum cryptum.	Mining waste materials	Silver, lead mercury, zinc, arsenic, manganese, indium, gallium, germanium, and cobalt.	1.7	45	150 rpm	5% (w/v)	Bioleaching was carried out for 50 days, and the efficiency of recovered metals was 90% Cu and 99% Zn.	[113]
Leptospirillum ferriphilum, A. caldus, Sulfobacillus sp. and Ferroplasma sp.	Mine tailings deposits	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	1.8	45	150 rpm	5% (w/v)	In 30 days, the metal recovery was 59.5% Co, 55% Cu, and 98.2% Ni.	[114]
Leptospirillum ferriphilum, A. caldus, Sulfobacillus sp. and Ferroplasma sp.	Mine tailings deposits	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	1.2	45	150 rpm	5% (w/v)	In 30 days, the metal recovery was 36.5% Co, 72% Cu, and 61.2% Ni.	[114]
A. caldus, Leptospirillum ferriphilum, Methylophaga spp. and Sphingomonas spp.	Tailing material in mining areas in Germany	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	1.5	40	550 rpm Aeration: 5 L/min	15% (w/v)	Fermentation was carried out for seven days, and the metal extraction achieved was 105,000 mg/kg.	[73]
A. caldus and Leptospirillum ferriphilum	Scorodite	Arsenic, copper, iron, sulfur	1.2	45	Aeration: 200 mL/min	1% (w/v)	The maximum recovery achieved during 88 days was 97% As.	[115]
Acidophilic ferrous, iron-oxidizing, and sulfur-oxidizing species	Tailing material in mining areas in Germany	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	1.6	30	100 rpm	4% (w/v)	During 22 days, the extraction efficiencies reported were 100% As, 85% Cd, 40% Cu, 85.4% Ln, 100% Mn, 5% Pb, and 100% Zn.	[116]
Acidophilic ferrous iron-oxidizing and sulfur-oxidizing species	Tailing material in mining areas in Germany	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium, gallium, germanium, cobalt	1.8	30	100 rpm	4% (w/v)	During 22 days, the reported extraction efficiencies were 79.9% In and 94.6% Zn.	[116]
Acidophilic ferrous iron-oxidizing and sulfur-oxidizing species	Tailing material in mining areas in Germany	Silver, lead, mercury, zinc, zinc, arsenic, manganese, indium gallium, germanium, cobalt	1.8	30	100 rpm	10% (w/v)	During 22 days, the reported extraction efficiencies were 72% As, 88% Cd, 87% In, and 81% Zn.	[116]
A. thiooxidans Ram 8, A. ferrooxidans Ram 6F, Leptospirillum ferrooxidans, and Ferroplasma acidiphilum BRGM 4	Tailing and mining residues (pyrite, quartz, etc.)	Iron, zinc, silica, cobalt, cobalt, nickel, aluminum, manganese, arsenic	2.0	30	150 rpm	10% (w/v)	The recovery achieved in the fermentative process was 91% Co, 57% Cu.	[117]
Marinobacter sp., Acidithiobacillus spp., Leptospirillum sp., Cuniculiplasma sp., Nitrosotenius sp. and Ferroplasma sp.	Tailing and mining residues (pyrite, quartz, etc.)	Iron, zinc, silica, cobalt, cobalt, nickel, aluminum, manganese, arsenic	1.5	30	300 rpm	10% (w/v)	In 10 days of retention, the amount of metal recovered was 87% Co, 43% Cu, 67% Ni, and 100% Zn.	[118]
Leptospirillum ferriphilum YSK, Ferroplasma thermophilum L1, A. caldus S1, and A. thiooxidans A01.	Metallurgical industry waste	Copper, cobalt, nickel, zinc	1.8	40	175 rpm	5% (w/v)	In 16 days, the maximum copper recovery was 58.7%.	[119]
Indigenous bacterial and fungal strains	Mining waste	Silver, manganese	2.0	30	200 rpm	6% (w/v)	67% Ag, 745 Mn.	[120]

Table 4

Organic acids produced by selected fungus in fermentative processes.

Fungi	Organic Acids
Yarrowia lipolytica	Citric acid
Mucor spp.	Fumaric and gluconic acid
Rhizopus spp.	Lactic, fumaric and gluconic acid
Aspergillus niger	Citric, oxalic and gluconic acids
Aspergillus spp.	Citric, malic, tartaric, ketoglutaric, itaconic and aconitic acid
Penicillium spp.	Citric, malic, tartaric, ketoglutaric, ketoglutaric and gluconic acids
Schizophyllum commune	Malic acid
Paecilomyces variotii	Malic acid

Table 5

Fungal bioleaching: operating conditions and metal extraction efficiencies of different SMMCs.

Microorganism	SMMC	Metal	pH	T (°C)	Agitation-Aeration	Pulp Density	Result	References
Aspergillus niger	Spent FCC catalyst (zeolites), crushed and screened	Nickel, vanadium, aluminum, aluminum, antimony, molybdenum, cobalt, tungsten	6.0	30	-	1% (w/v)	In 60 days, the recovery was 9% Ni, 23% Fe, 30% Al, 36% V, and 64% Sb.	[138]
Penicillium simplicissimum	Spent FCC catalyst (zeolites), crushed and screened	Nickel, vanadium, aluminum, aluminum, antimony, molybdenum, cobalt, tungsten	4–7	30	-	3% (w/v)	In two-step bioleaching, 32% Al, 67% Co, 65% Mo, and 38% Ni were recovered in 30 days.	[139]
Purpureocillium lilacinum y Aspergillus niger (7:3)	Printed circuit boards, crushed with d < 40mm	Aluminum, lead, zinc, and tin	5.0	30	150 rpm	3 to 8% (w/v)	In 27 days, 15.7 ± 0.87% Al, 20.5 ± 0.78% Pb, 49.5 ± 0.38% Zn and 8.1 ± 0.34% Sn were extracted.	[140]
Aspergillus niger	Printed circuit boards, shredded and screened	Aluminum, lead, zinc, copper	5.08	25	120 rpm	3.9% (w/v)	In 21 days, the maximum recovery of metals was 98.57% Zn, 43.95% Ni, and 64.03% Cu.	[141]
P. simplicissimum	Printed circuit boards	Aluminum, lead, zinc, copper	6.0	30	100–400 mL/min	1–10% (w/v)	The maximum recovery achieved for Cu and Ni was 40% in 7 days.	[142]
Aspergillus niger	Saprolite	Iron, silica, nickel, manganese	5.0	95	400 rpm	10% (w/v)	The maximum recovery achieved in 24h was 65% Ni and 58% Fe.	[143]
Aspergillus niger	Limonite	Iron, aluminum, silica, manganese	5.0	95	400 rpm	10% (w/v)	Maximum recovery achieved in 24h was 78% Ni and 60% Fe.	[143]
Penicillium simplicissimum	Waste ash from power plant	Vanadium, iron, nickel	4.5	30	130 rpm	1% (w/v)	The maximum extraction achieved was 48.3% Fe, 19% V, and 12% Ni in 15 days.	[144]
Aspergillus niger NCIM 548	Chromite	Nickel, cobalt	2.5	30	150 rpm	2% (w/v)	In 21 days of fermentation, the metal recovery was 70.49% Ni and 66.93% Co.	[145]
Aspergillus niger	Fly ash from municipal solid waste incinerators	Aluminum, lead, zinc, copper	10–12	30	120 rpm	1–8% (w/v)	After 30 days, the recovery of Cu, Pb, and Fe metals was between 60 to 70%, 55 to 70%, and 30 to 40%, respectively.	[146]
Aspergillus niger y Aspergillus tubingensis	Electronic waste (e-waste)	Copper, lead, tin, silver, gold, platinum, platinum, aluminum, manganese, and palladium	5.0	30	140 rpm	1%(w/v)	The achieved metal recovery was 80% Al, 50% Co, 90% Mn, 80% Li and 67% Ni in 27 days.	[147]
Aspergillus niger	Bauxite (d < 180 µm)	Aluminum, iron, silica	6.5	30	130 rpm	1% (w/v)	Metal recovery in 10 days was 82.80% Al.	[148]
Aspergillus niger adaptado	Lithium-ion batteries (LIBs)	Cobalt, lithium, nickel, manganese, copper, aluminum, graphite, and other materials	5.4	30	120–170 rpm	0.3–1% (w/v)	The obtained recovery efficiency from spent LIBs was 100%, 94%, 72%, 62%, 45%, and 38% for Li, Cu, Mn, Al, Ni, and Co, respectively, in 27 days.	[149]
Penicillium chrysogenum strain F1	Soil contaminated with metals and metalloids	Cadmium, copper, lead, zinc	-	25	120 rpm	5% (w/v)	In 15 days, the recovery of metals was 50% Cd, 35% Cu, 9% Pb, and 40% Zn.	[19]
Phanerochaete chrysosporium	Waste of electrical and electronic equipment	Copper, lead, tin, silver, gold, platinum, platinum, aluminum, manganese, and palladium	5.0	30	150 rpm	1% (w/v)	In 14 days, the copper recovery achieved was 54%.	[15]
Aspergillus fumigatus(M3Ai)	Soil contaminated with metals and metalloids	Cadmium, copper, lead, lead, zinc, chromium	6.5	30	130 rpm	5% (w/v)	In 3 days, the metal recovery in two-step bioleaching was 79% Cd and 69% Cr.	[150]
Aspergillus flavus	Soil contaminated with metals and metalloids	Cadmium, copper, lead, lead, zinc, chromium	-	30	130 rpm	5%(w/v)	In 15 days, the maximum metal recovery was 39.77% Cd, 18.16% Pb, and 58.22% Zn.	[105]
Fibroporia vaillantii	Wood preservative: Chromated copper arsenate	Chromium, copper, arsenic	3.1	30	150 rpm	-	In 28 days of fermentation, the maximum metal recovery efficiency was 87% Cu, 80% Cr, and 100% As.	[151]
Geotrichum sp. G1 y Bacillus sp. B2	Soil contaminated with metals and metalloids	Cadmium, copper, lead, lead, zinc, chromium	2.0–10	-	-	2%	Chromium extraction at 28 days was 94.8%.	[152]
Aspergillus niger(M1DGR)	Soil contaminated with metals and metalloids	Cadmium, copper, lead, lead, zinc, chromium	6.5	30	130 rpm	5% (w/v)	The 3-day two-step bioleaching metal recovery was 98% Cd and 43% Cr.	[150]
Penicillium rubens(M2Aiii)	Soil contaminated with metals and metalloids	Cadmium, copper, lead, lead, zinc, chromium	6.5	30	130 rpm	5% (w/v)	The 3-day metal recovery in two-step bioleaching was 79% Cd and 69% Cr.	[150]
Penicillium, Aspergillus, y Fusarium	Panchakavya (soil mixture)	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	2.6	30	120–180 rpm	0.2–1% (w/v)	The 5-day metal recovery was 64% Pb and 49% Cu.	[100]
Aspergillus niger strain SY1	Contaminated sediment	Cadmium, arsenic, copper, lead, lead, zinc, chromium, iron	6.5	30	220 rpm	10% (w/v)	Metal recovery in 7 days was 93.5% Cd, 62.3% Cu, 11.5% Pb, and 68% Zn.	[153]
Aspergillus niger strain SY1	Contaminated sediment	Cadmium, copper, lead, lead, zinc, chromium	6.5	30	220 rpm	2.5% (w/v)	In 15 days of fermentation, the recovery efficiency achieved was 90% Cd, 20% Pb, 60% Cu, and 60% Zn.	[153]
Penicillium chrysogenum strain KBS3	Mine tailings	Cobalt, zinc, copper, nickel, manganese, lead	2.5	30	120 rpm	10% (w/v)	In 25 days, the maximum metal recovery achieved was 60% Co, 67% Cu, 69% Mg, 55% Ni, and 65% Zn.	[120]
Aspergillus fumigatus	Mine tailings	Arsenic, iron, manganese, lead, zinc, zinc	5.0	30	150 rpm	8% (w/v)	In 40 days, the one-step bioleaching recovered 62.1% As, 58.4% Fe, 100% Mn, 56.1 Pb, and 54.43% Zn.	[154]
Aspergillus fumigatus	Mine tailings	Arsenic, iron, manganese, lead, zinc, zinc	5.0	30	150 rpm	8% (w/v)	The two-step bioleaching showed that the maximum metal recovery would be 32% As, 45.20% Fe, 58.4% Mn, 88.4% Pb, and 31.3% Zn.	[154]

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su151310222/s1, Table S1: Leading groups of organic acids, formula, dissociation reactions, and corresponding pKa [2,131,132].

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This review paper explores the potential of bioleaching as a sustainable alternative for recovering metals from solid matrices. With over 12 billion tons of solid waste annually worldwide, bioleaching provides a promising opportunity to extract metals from solid waste, avoiding harmful chemical processes. It explains bacterial and fungal bioleaching techniques that extract copper, gold, zinc, and other metals from solid matrices. Fungal bioleaching effectively extracts a wide range of valuable metals, including nickel, vanadium, aluminium, molybdenum, cobalt, iron, manganese, silver, platinum, and palladium. The review highlights different solid matrices with metal contents that have the potential to be recovered by bioleaching, presenting promising bioprocess alternatives to current industrially available technologies for metal recovery. The optimal conditions for bioleaching, including pH, temperature, agitation–aeration, and pulp density are also discussed. The review shows that bioleaching has the potential to play a crucial role in the transition to a more sustainable and circular economy by providing an efficient, cost-effective, and environmentally friendly method for metal recovery from solid matrices.

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Title

Bioleaching Techniques for Sustainable Recovery of Metals from Solid Matrices

Author

Rendón-Castrillón, Leidy¹; Ramírez-Carmona, Margarita¹

; Ocampo-López, Carlos¹

; Gómez-Arroyave, Luis²

¹ Centro de Estudios y de Investigación en Biotecnología (CIBIOT), Chemical Engineering Faculty, Universidad Pontificia Bolivariana, Medellín 050031, Colombia; [email protected] (L.R.-C.); [email protected] (M.R.-C.)
² Bioexplora S.A.S., Medellín 050031, Colombia; [email protected]

First page

10222

Publication year

2023

Publication date

2023

Publisher

MDPI AG

e-ISSN

20711050

Source type

Scholarly Journal

Language of publication

English

DOI

https://doi.org/10.3390/su151310222

ProQuest document ID

2836506225

Bioleaching Techniques for Sustainable Recovery of Metals from Solid Matrices

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