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Abstract

A variety of both lithotrophic and organotrophic microorganisms are known to mediate the mobilization of various elements from solids mostly by the formation of inorganic and organic acids. Under appropriate environmental conditions, metals are solubilized and extracted from metal-rich materials in subsurface ecosystems by the action of bacteria and fungi. In mine tailings or landfills microbial metal leaching represents a potential environmental hazard. However, these microbial activities can be successfully applied in the industry for the recovery of metals from solid materials such as ores or incineration residues. Microbial leaching processes are currently used for the winning of gold and copper from low-grade ores (‘bioleaching’). Solid industrial waste materials such as fly ash, sludges, or dust might also be microbially treated to recover metals for the re-use in metal-manufacturing industries. Bioleaching allows the cycling of metals by a process close to natural biogeochemical cycles reducing the demand for resources such as ores, energy, or landfill space.

Bioleaching, Biohydrometallurgy, Heavy metal, Fly ash, Waste incineration residue, Renewable resource

1 Introduction

In the light of the expected shortage of non-renewable resources, increased efforts are absolutely necessary to open new sources of raw materials with the aid of new or improved technologies. A possibility to obtain metals from low-grade mineral resources is offered by the use of microbiological leaching processes [1, 2]. Bioleaching processes are based on the ability of microorganisms (bacteria, fungi) to transform solid compounds resulting in soluble and extractable elements which can be recovered. Applying bioleaching processes, it is possible to obtain metals from natural ores and industrial residues which cannot be handled with conventional techniques [2]. However, bioleaching processes have only recently gained importance in a variety of mineral industries, whereas, in contrast, chemical hydrometallurgical leaching under acidic conditions has been described in many publications [2].

Solids from waste incineration such as slag and ash are considered ‘artificial ores’ (Table 1). It might become possible to recycle the leached and recovered metals and to re-use them as raw materials by metal-manufacturing industries. In addition, the environmental quality of the residues is improved by the process with respect to a subsequent application of these materials for construction purposes. Bioleaching of waste materials allows the cycling of metals by a process close to natural biogeochemical cycles reducing the demand for resources such as ores, energy, or landfill space. Bioleaching represents a ‘clean technology’ process with a low cost and low energy level compared with conventional thermal solid waste treatment techniques. Government regulations and research policies that favor ‘green’ technologies are a key incentive for developing such processes. These find a wide acceptance with the public and in politics. It is a matter of innovative technologies showing a proved market gap.

Table 1

Concentration of selected elements in residues from municipal waste incineration compared to the elemental composition of the earth crust and ores suitable for economic metal recovery [3–5]

Element Earth crust (%) Slag (%) Fly ash (%) Ore (%)a 
Cd 0.00015 <0.001 0.04 0.2b 
Cr 0.02 0.04 0.06 30 
Cu 0.007 0.16 0.09 0.2 
Ni 0.008 0.014 0.014 1.5 
Pb 0.0016 0.06 0.8 4 
Sn 0.004 <0.05 0.6 1 
Ti 0.44 0.75 1.1 1 
Zn 0.008 0.19 2.7 4 
Element Earth crust (%) Slag (%) Fly ash (%) Ore (%)a 
Cd 0.00015 <0.001 0.04 0.2b 
Cr 0.02 0.04 0.06 30 
Cu 0.007 0.16 0.09 0.2 
Ni 0.008 0.014 0.014 1.5 
Pb 0.0016 0.06 0.8 4 
Sn 0.004 <0.05 0.6 1 
Ti 0.44 0.75 1.1 1 
Zn 0.008 0.19 2.7 4 

aThe percentage represents the elemental concentration in ores for economic metal recovery by conventional mining techniques.

bCd is usually associated with zinc ores (zinc sulfide, zinc carbonate). Within theses ores, Cd concentration is approximately 0.2%.

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Table 1

Concentration of selected elements in residues from municipal waste incineration compared to the elemental composition of the earth crust and ores suitable for economic metal recovery [3–5]

Element Earth crust (%) Slag (%) Fly ash (%) Ore (%)a 
Cd 0.00015 <0.001 0.04 0.2b 
Cr 0.02 0.04 0.06 30 
Cu 0.007 0.16 0.09 0.2 
Ni 0.008 0.014 0.014 1.5 
Pb 0.0016 0.06 0.8 4 
Sn 0.004 <0.05 0.6 1 
Ti 0.44 0.75 1.1 1 
Zn 0.008 0.19 2.7 4 
Element Earth crust (%) Slag (%) Fly ash (%) Ore (%)a 
Cd 0.00015 <0.001 0.04 0.2b 
Cr 0.02 0.04 0.06 30 
Cu 0.007 0.16 0.09 0.2 
Ni 0.008 0.014 0.014 1.5 
Pb 0.0016 0.06 0.8 4 
Sn 0.004 <0.05 0.6 1 
Ti 0.44 0.75 1.1 1 
Zn 0.008 0.19 2.7 4 

aThe percentage represents the elemental concentration in ores for economic metal recovery by conventional mining techniques.

bCd is usually associated with zinc ores (zinc sulfide, zinc carbonate). Within theses ores, Cd concentration is approximately 0.2%.

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2 Principles of bacterial metal leaching

Valuable metals have been obtained from ores by leaching for hundreds of years. This process was believed to be a chemical reaction mediated by water and oxygen until 1947, when bacterial catalyzation of iron oxidation and sulfuric acid formation in mine waters was demonstrated [6]. However, the microbial production of sulfuric acid in mine waters had already been suggested 15 years earlier, but attempts to isolate and characterize the strains responsible for the acidification were not successful [6].

A variety of microorganisms are known to catalyze leaching of metals mostly from ore deposits and mine tailings. Above all, autotrophic Thiobacillus species as well as heterotrophic Aspergillus and Penicillium species are described in the literature. Table 2 gives an overview of selected microorganisms known for their bioleaching potential. Excellent detailed reviews of microbial and chemical principles of bioleaching have been published elsewhere [2, 10, 18, 24].

Table 2

Selection of microorganisms known to mediate metal bioleaching reactions

Organism Type Nutrition Main leaching agent pH range pH optimum Temperature range Reference 
Acetobacter methanolicus bacteria heterotrophic gluconate acidiphilic   [7] 
Acidianus brierleyi bacteria facult. heterotrophic sulfuric acid acidophilic 1.5–3.0 45–75 [8, 9] 
Acidophillum cryptum bacteria heterotrophic organic acids 2.0–6.0  mesophilic [10] 
Actinomucor sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Alternaria sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Arthrobacter sp. bacteria heterotrophic     [12] 
Aspergillus amstelodami fungi heterotrophic     [11] 
Aspergillus clavatus fungi heterotrophic aspartate    [11] 
Aspergillus ficuum fungi heterotrophic oxalate    [13] 
Aspergillus fumigatus fungi heterotrophic     [11] 
Aspergillus niger fungi heterotrophic oxalate, citrate, gluconate, lactate    [5, 14] 
Aspergillus ochraceus fungi heterotrophic citrate, glutamate    [11] 
Bacillus megaterium bacteria heterotrophic citrate, amino acids    [15] 
Candida sp. fungi heterotrophic     [11] 
Cerostamella sp. fungi heterotrophic     [11] 
Chromobacterium violaceum bacteria heterotrophic cyanide    [9] 
Cladosporium resinae fungi heterotrophic     [11] 
Coriolus versicolor fungi heterotrophic     [11] 
Corynebacterium sp. bacteria heterotrophic     [16] 
Crenothrix sp. bacteria facult. autotrophic ferric iron 5.5–6.2  18–24 [10] 
Cunninghamiella sp. fungi heterotrophic     [11] 
Fusarium sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Gallionella sp. bacteria autotrophic ferric iron 6.4–6.8  6–25 [10] 
Gleophyllum trabeum fungi heterotrophic oxalate    [13] 
Leptospirillum ferrooxidans bacteria chemolithoautotrophic ferric iron  2.5–3.0 30 [9, 10] 
Leptospirillum thermoferrooxidans bacteria chemolithoautotrophic ferric iron  1.7–1.9 45–50 [8] 
Leptotrix sp. bacteria facult. autotrophic ferric iron, sulfuric acid 5.8–7.8  5–40 [10] 
Metallogenium sp. bacteria heterotrophic ferric iron 3.5–6.8 4.1  [10] 
Metallosphaera sedula bacteria chemolithoautotrophic ferric iron, sulfuric acid acidophilic  extr. thermophilic [8, 10] 
Mucor sp. fungi heterotrophic fumatate, gluconate    [11] 
Paecilomyces variotii fungi heterotrophic malate    [11] 
Penicillium brevicompactum fungi heterotrophic     [11] 
Penicillium cyclopium fungi heterotrophic     [11] 
Penicillium funiculosum fungi heterotrophic citrate, glutamate    [11] 
Penicillium notatum fungi heterotrophic     [11] 
Penicillium ochrochloron fungi heterotrophic oxalate    [11] 
Penicillium oxalicum fungi heterotrophic oxalate    [13] 
Penicillium simplicissimum fungi heterotrophic citrate, oxalate, gluconate    [13] 
Penicillium spinulosum fungi heterotrophic oxalate    [11, 14] 
Penicillium variotii fungi heterotrophic     [11] 
Phanerochaete chrysosporium fungi heterotrophic     [11] 
Pichia sp. fungi heterotrophic     [11] 
Pseudomonas putida bacteria heterotrophic citrate, gluconate    [15] 
Rhizopus sp. fungi heterophic lactate, fumarate, gluconate    [11] 
Schizophyllum commune fungi heterotrophic malate    [11] 
Sclerotium rolfsii fungi heterotrophic oxalate    [13] 
Siderocapsa sp. bacteria heterotrophic ferric iron    [10] 
Sulfobacillus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfobacillus thermosulfidooxidans sub. thermotolerans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  37–42 [8] 
Sulfobacillus thermosulfidooxidans sub. asporogenes archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfolobus acidocaldarius archaea chemolithoautotrophic ferric iron, sulfuric acid 0.9–5.8 2.0–3.0 55–85 [9, 10] 
Sulfolobus ambivalens archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus solfataricus archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus brierleyi archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [17] 
Sulfolobus yellowstonii archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8] 
Sulfurococcus sp. bacteria mixotrophic ferric iron, sulfuric acid acidophilic  extremely thermophilic [8] 
Thermothrix thiopara bacteria chemolithoautotrophic sulfuric acid neutral  60–75 [17] 
Thiobacillus acidophilus bacteria chemolithoautotrophic sulfuric acid 1.5–6.0 3.0 25–30 [10] 
Thiobacillus albertis bacteria chemolithoautotrophic sulfuric acid 2.0–4.5 3.5–4.0 28–30 [10] 
Thiobacillus capsulatus bacteria chemolithoautotrophic sulfuric acid    [18] 
Thiobacillus concretivorus bacteria chemolithoautotrophic sulfuric acid 0.5–6.0   [10] 
Thiobacillus cuprinus bacteria chemolithoautotrophic sulfuric acid    [19] 
Thiobacillus delicatus bacteria mixotrophic sulfuric acid  5.0–7.0 25–30 [10] 
Thiobacillus denitrificans bacteria chemolithoautotrophic sulfuric acid 5.0–7.0  30 [10] 
Thiobacillus ferrooxidans bacteria chemolithoautotrophic ferric iron, sulfuric acid 1.4–6.0 2.4 28–35 [7, 9, 10] 
Thiobacillus intermedius bacteria chemolithoautotrophic sulfuric acid 1.9–7.0 6.8 30 [10] 
Thiobacillus kabobis bacteria mixotrophic sulfuric acid 1.8–6.0 3.0 28 [10] 
Thiobacillus neapolitanus bacteria chemolithoautotrophic sulfuric acid 3.0–8.5 6.2–7.0 28 [10] 
Thiobacillus novellus bacteria chemolithoautotrophic sulfuric acid 5.0–9.0 7.8–9.0 30 [10] 
Thiobacillus organoparus bacteria mixotrophic sulfuric acid 1.5–5.0 2.5–3.0 27–30 [10] 
Thiobacillus perometabolis bacteria chemolithoheterotrophic sulfuric acid 2.6–6.8 6.9 30 [10] 
Thiobacillus prosperus bacteria chemolithoautotrophic sulfuric acid    [20] 
Thiobacillus rubellus bacteria chemolithoautotrophic sulfuric acid  5.0–7.0 25–30 [8, 10] 
Thiobacillus tepidarius bacteria chemolithoautotrophic sulfuric acid    [21] 
Thiobacillus thiocynoxidans bacteria chemolithoautotrophic sulfuric acid    [22] 
Thiobacillus thiooxidans bacteria chemolithoautotrophic sulfuric acid 0.5–6.0 2.0–3.5 10–37 [10] 
Thiobacillus thioparus bacteria chemolithoautotrophic sulfuric acid 4.5–10.0 6.6–7.2 11–25 [10] 
Thiobacillus versutus bacteria chemolithoautotrophic sulfuric acid  8.0–9.0  [10] 
Trametes versicolor fungi heterotrophic     [11] 
Trichoderma harzianum bacteria heterotrophic     [11] 
Trichoderma viride bacteria heterotrophic     [23] 
Yarrowia lipolytica fungi heterotrophic citrate    [11] 
Organism Type Nutrition Main leaching agent pH range pH optimum Temperature range Reference 
Acetobacter methanolicus bacteria heterotrophic gluconate acidiphilic   [7] 
Acidianus brierleyi bacteria facult. heterotrophic sulfuric acid acidophilic 1.5–3.0 45–75 [8, 9] 
Acidophillum cryptum bacteria heterotrophic organic acids 2.0–6.0  mesophilic [10] 
Actinomucor sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Alternaria sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Arthrobacter sp. bacteria heterotrophic     [12] 
Aspergillus amstelodami fungi heterotrophic     [11] 
Aspergillus clavatus fungi heterotrophic aspartate    [11] 
Aspergillus ficuum fungi heterotrophic oxalate    [13] 
Aspergillus fumigatus fungi heterotrophic     [11] 
Aspergillus niger fungi heterotrophic oxalate, citrate, gluconate, lactate    [5, 14] 
Aspergillus ochraceus fungi heterotrophic citrate, glutamate    [11] 
Bacillus megaterium bacteria heterotrophic citrate, amino acids    [15] 
Candida sp. fungi heterotrophic     [11] 
Cerostamella sp. fungi heterotrophic     [11] 
Chromobacterium violaceum bacteria heterotrophic cyanide    [9] 
Cladosporium resinae fungi heterotrophic     [11] 
Coriolus versicolor fungi heterotrophic     [11] 
Corynebacterium sp. bacteria heterotrophic     [16] 
Crenothrix sp. bacteria facult. autotrophic ferric iron 5.5–6.2  18–24 [10] 
Cunninghamiella sp. fungi heterotrophic     [11] 
Fusarium sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Gallionella sp. bacteria autotrophic ferric iron 6.4–6.8  6–25 [10] 
Gleophyllum trabeum fungi heterotrophic oxalate    [13] 
Leptospirillum ferrooxidans bacteria chemolithoautotrophic ferric iron  2.5–3.0 30 [9, 10] 
Leptospirillum thermoferrooxidans bacteria chemolithoautotrophic ferric iron  1.7–1.9 45–50 [8] 
Leptotrix sp. bacteria facult. autotrophic ferric iron, sulfuric acid 5.8–7.8  5–40 [10] 
Metallogenium sp. bacteria heterotrophic ferric iron 3.5–6.8 4.1  [10] 
Metallosphaera sedula bacteria chemolithoautotrophic ferric iron, sulfuric acid acidophilic  extr. thermophilic [8, 10] 
Mucor sp. fungi heterotrophic fumatate, gluconate    [11] 
Paecilomyces variotii fungi heterotrophic malate    [11] 
Penicillium brevicompactum fungi heterotrophic     [11] 
Penicillium cyclopium fungi heterotrophic     [11] 
Penicillium funiculosum fungi heterotrophic citrate, glutamate    [11] 
Penicillium notatum fungi heterotrophic     [11] 
Penicillium ochrochloron fungi heterotrophic oxalate    [11] 
Penicillium oxalicum fungi heterotrophic oxalate    [13] 
Penicillium simplicissimum fungi heterotrophic citrate, oxalate, gluconate    [13] 
Penicillium spinulosum fungi heterotrophic oxalate    [11, 14] 
Penicillium variotii fungi heterotrophic     [11] 
Phanerochaete chrysosporium fungi heterotrophic     [11] 
Pichia sp. fungi heterotrophic     [11] 
Pseudomonas putida bacteria heterotrophic citrate, gluconate    [15] 
Rhizopus sp. fungi heterophic lactate, fumarate, gluconate    [11] 
Schizophyllum commune fungi heterotrophic malate    [11] 
Sclerotium rolfsii fungi heterotrophic oxalate    [13] 
Siderocapsa sp. bacteria heterotrophic ferric iron    [10] 
Sulfobacillus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfobacillus thermosulfidooxidans sub. thermotolerans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  37–42 [8] 
Sulfobacillus thermosulfidooxidans sub. asporogenes archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfolobus acidocaldarius archaea chemolithoautotrophic ferric iron, sulfuric acid 0.9–5.8 2.0–3.0 55–85 [9, 10] 
Sulfolobus ambivalens archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus solfataricus archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus brierleyi archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [17] 
Sulfolobus yellowstonii archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8] 
Sulfurococcus sp. bacteria mixotrophic ferric iron, sulfuric acid acidophilic  extremely thermophilic [8] 
Thermothrix thiopara bacteria chemolithoautotrophic sulfuric acid neutral  60–75 [17] 
Thiobacillus acidophilus bacteria chemolithoautotrophic sulfuric acid 1.5–6.0 3.0 25–30 [10] 
Thiobacillus albertis bacteria chemolithoautotrophic sulfuric acid 2.0–4.5 3.5–4.0 28–30 [10] 
Thiobacillus capsulatus bacteria chemolithoautotrophic sulfuric acid    [18] 
Thiobacillus concretivorus bacteria chemolithoautotrophic sulfuric acid 0.5–6.0   [10] 
Thiobacillus cuprinus bacteria chemolithoautotrophic sulfuric acid    [19] 
Thiobacillus delicatus bacteria mixotrophic sulfuric acid  5.0–7.0 25–30 [10] 
Thiobacillus denitrificans bacteria chemolithoautotrophic sulfuric acid 5.0–7.0  30 [10] 
Thiobacillus ferrooxidans bacteria chemolithoautotrophic ferric iron, sulfuric acid 1.4–6.0 2.4 28–35 [7, 9, 10] 
Thiobacillus intermedius bacteria chemolithoautotrophic sulfuric acid 1.9–7.0 6.8 30 [10] 
Thiobacillus kabobis bacteria mixotrophic sulfuric acid 1.8–6.0 3.0 28 [10] 
Thiobacillus neapolitanus bacteria chemolithoautotrophic sulfuric acid 3.0–8.5 6.2–7.0 28 [10] 
Thiobacillus novellus bacteria chemolithoautotrophic sulfuric acid 5.0–9.0 7.8–9.0 30 [10] 
Thiobacillus organoparus bacteria mixotrophic sulfuric acid 1.5–5.0 2.5–3.0 27–30 [10] 
Thiobacillus perometabolis bacteria chemolithoheterotrophic sulfuric acid 2.6–6.8 6.9 30 [10] 
Thiobacillus prosperus bacteria chemolithoautotrophic sulfuric acid    [20] 
Thiobacillus rubellus bacteria chemolithoautotrophic sulfuric acid  5.0–7.0 25–30 [8, 10] 
Thiobacillus tepidarius bacteria chemolithoautotrophic sulfuric acid    [21] 
Thiobacillus thiocynoxidans bacteria chemolithoautotrophic sulfuric acid    [22] 
Thiobacillus thiooxidans bacteria chemolithoautotrophic sulfuric acid 0.5–6.0 2.0–3.5 10–37 [10] 
Thiobacillus thioparus bacteria chemolithoautotrophic sulfuric acid 4.5–10.0 6.6–7.2 11–25 [10] 
Thiobacillus versutus bacteria chemolithoautotrophic sulfuric acid  8.0–9.0  [10] 
Trametes versicolor fungi heterotrophic     [11] 
Trichoderma harzianum bacteria heterotrophic     [11] 
Trichoderma viride bacteria heterotrophic     [23] 
Yarrowia lipolytica fungi heterotrophic citrate    [11] 
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Table 2

Selection of microorganisms known to mediate metal bioleaching reactions

Organism Type Nutrition Main leaching agent pH range pH optimum Temperature range Reference 
Acetobacter methanolicus bacteria heterotrophic gluconate acidiphilic   [7] 
Acidianus brierleyi bacteria facult. heterotrophic sulfuric acid acidophilic 1.5–3.0 45–75 [8, 9] 
Acidophillum cryptum bacteria heterotrophic organic acids 2.0–6.0  mesophilic [10] 
Actinomucor sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Alternaria sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Arthrobacter sp. bacteria heterotrophic     [12] 
Aspergillus amstelodami fungi heterotrophic     [11] 
Aspergillus clavatus fungi heterotrophic aspartate    [11] 
Aspergillus ficuum fungi heterotrophic oxalate    [13] 
Aspergillus fumigatus fungi heterotrophic     [11] 
Aspergillus niger fungi heterotrophic oxalate, citrate, gluconate, lactate    [5, 14] 
Aspergillus ochraceus fungi heterotrophic citrate, glutamate    [11] 
Bacillus megaterium bacteria heterotrophic citrate, amino acids    [15] 
Candida sp. fungi heterotrophic     [11] 
Cerostamella sp. fungi heterotrophic     [11] 
Chromobacterium violaceum bacteria heterotrophic cyanide    [9] 
Cladosporium resinae fungi heterotrophic     [11] 
Coriolus versicolor fungi heterotrophic     [11] 
Corynebacterium sp. bacteria heterotrophic     [16] 
Crenothrix sp. bacteria facult. autotrophic ferric iron 5.5–6.2  18–24 [10] 
Cunninghamiella sp. fungi heterotrophic     [11] 
Fusarium sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Gallionella sp. bacteria autotrophic ferric iron 6.4–6.8  6–25 [10] 
Gleophyllum trabeum fungi heterotrophic oxalate    [13] 
Leptospirillum ferrooxidans bacteria chemolithoautotrophic ferric iron  2.5–3.0 30 [9, 10] 
Leptospirillum thermoferrooxidans bacteria chemolithoautotrophic ferric iron  1.7–1.9 45–50 [8] 
Leptotrix sp. bacteria facult. autotrophic ferric iron, sulfuric acid 5.8–7.8  5–40 [10] 
Metallogenium sp. bacteria heterotrophic ferric iron 3.5–6.8 4.1  [10] 
Metallosphaera sedula bacteria chemolithoautotrophic ferric iron, sulfuric acid acidophilic  extr. thermophilic [8, 10] 
Mucor sp. fungi heterotrophic fumatate, gluconate    [11] 
Paecilomyces variotii fungi heterotrophic malate    [11] 
Penicillium brevicompactum fungi heterotrophic     [11] 
Penicillium cyclopium fungi heterotrophic     [11] 
Penicillium funiculosum fungi heterotrophic citrate, glutamate    [11] 
Penicillium notatum fungi heterotrophic     [11] 
Penicillium ochrochloron fungi heterotrophic oxalate    [11] 
Penicillium oxalicum fungi heterotrophic oxalate    [13] 
Penicillium simplicissimum fungi heterotrophic citrate, oxalate, gluconate    [13] 
Penicillium spinulosum fungi heterotrophic oxalate    [11, 14] 
Penicillium variotii fungi heterotrophic     [11] 
Phanerochaete chrysosporium fungi heterotrophic     [11] 
Pichia sp. fungi heterotrophic     [11] 
Pseudomonas putida bacteria heterotrophic citrate, gluconate    [15] 
Rhizopus sp. fungi heterophic lactate, fumarate, gluconate    [11] 
Schizophyllum commune fungi heterotrophic malate    [11] 
Sclerotium rolfsii fungi heterotrophic oxalate    [13] 
Siderocapsa sp. bacteria heterotrophic ferric iron    [10] 
Sulfobacillus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfobacillus thermosulfidooxidans sub. thermotolerans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  37–42 [8] 
Sulfobacillus thermosulfidooxidans sub. asporogenes archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfolobus acidocaldarius archaea chemolithoautotrophic ferric iron, sulfuric acid 0.9–5.8 2.0–3.0 55–85 [9, 10] 
Sulfolobus ambivalens archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus solfataricus archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus brierleyi archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [17] 
Sulfolobus yellowstonii archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8] 
Sulfurococcus sp. bacteria mixotrophic ferric iron, sulfuric acid acidophilic  extremely thermophilic [8] 
Thermothrix thiopara bacteria chemolithoautotrophic sulfuric acid neutral  60–75 [17] 
Thiobacillus acidophilus bacteria chemolithoautotrophic sulfuric acid 1.5–6.0 3.0 25–30 [10] 
Thiobacillus albertis bacteria chemolithoautotrophic sulfuric acid 2.0–4.5 3.5–4.0 28–30 [10] 
Thiobacillus capsulatus bacteria chemolithoautotrophic sulfuric acid    [18] 
Thiobacillus concretivorus bacteria chemolithoautotrophic sulfuric acid 0.5–6.0   [10] 
Thiobacillus cuprinus bacteria chemolithoautotrophic sulfuric acid    [19] 
Thiobacillus delicatus bacteria mixotrophic sulfuric acid  5.0–7.0 25–30 [10] 
Thiobacillus denitrificans bacteria chemolithoautotrophic sulfuric acid 5.0–7.0  30 [10] 
Thiobacillus ferrooxidans bacteria chemolithoautotrophic ferric iron, sulfuric acid 1.4–6.0 2.4 28–35 [7, 9, 10] 
Thiobacillus intermedius bacteria chemolithoautotrophic sulfuric acid 1.9–7.0 6.8 30 [10] 
Thiobacillus kabobis bacteria mixotrophic sulfuric acid 1.8–6.0 3.0 28 [10] 
Thiobacillus neapolitanus bacteria chemolithoautotrophic sulfuric acid 3.0–8.5 6.2–7.0 28 [10] 
Thiobacillus novellus bacteria chemolithoautotrophic sulfuric acid 5.0–9.0 7.8–9.0 30 [10] 
Thiobacillus organoparus bacteria mixotrophic sulfuric acid 1.5–5.0 2.5–3.0 27–30 [10] 
Thiobacillus perometabolis bacteria chemolithoheterotrophic sulfuric acid 2.6–6.8 6.9 30 [10] 
Thiobacillus prosperus bacteria chemolithoautotrophic sulfuric acid    [20] 
Thiobacillus rubellus bacteria chemolithoautotrophic sulfuric acid  5.0–7.0 25–30 [8, 10] 
Thiobacillus tepidarius bacteria chemolithoautotrophic sulfuric acid    [21] 
Thiobacillus thiocynoxidans bacteria chemolithoautotrophic sulfuric acid    [22] 
Thiobacillus thiooxidans bacteria chemolithoautotrophic sulfuric acid 0.5–6.0 2.0–3.5 10–37 [10] 
Thiobacillus thioparus bacteria chemolithoautotrophic sulfuric acid 4.5–10.0 6.6–7.2 11–25 [10] 
Thiobacillus versutus bacteria chemolithoautotrophic sulfuric acid  8.0–9.0  [10] 
Trametes versicolor fungi heterotrophic     [11] 
Trichoderma harzianum bacteria heterotrophic     [11] 
Trichoderma viride bacteria heterotrophic     [23] 
Yarrowia lipolytica fungi heterotrophic citrate    [11] 
Organism Type Nutrition Main leaching agent pH range pH optimum Temperature range Reference 
Acetobacter methanolicus bacteria heterotrophic gluconate acidiphilic   [7] 
Acidianus brierleyi bacteria facult. heterotrophic sulfuric acid acidophilic 1.5–3.0 45–75 [8, 9] 
Acidophillum cryptum bacteria heterotrophic organic acids 2.0–6.0  mesophilic [10] 
Actinomucor sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Alternaria sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Arthrobacter sp. bacteria heterotrophic     [12] 
Aspergillus amstelodami fungi heterotrophic     [11] 
Aspergillus clavatus fungi heterotrophic aspartate    [11] 
Aspergillus ficuum fungi heterotrophic oxalate    [13] 
Aspergillus fumigatus fungi heterotrophic     [11] 
Aspergillus niger fungi heterotrophic oxalate, citrate, gluconate, lactate    [5, 14] 
Aspergillus ochraceus fungi heterotrophic citrate, glutamate    [11] 
Bacillus megaterium bacteria heterotrophic citrate, amino acids    [15] 
Candida sp. fungi heterotrophic     [11] 
Cerostamella sp. fungi heterotrophic     [11] 
Chromobacterium violaceum bacteria heterotrophic cyanide    [9] 
Cladosporium resinae fungi heterotrophic     [11] 
Coriolus versicolor fungi heterotrophic     [11] 
Corynebacterium sp. bacteria heterotrophic     [16] 
Crenothrix sp. bacteria facult. autotrophic ferric iron 5.5–6.2  18–24 [10] 
Cunninghamiella sp. fungi heterotrophic     [11] 
Fusarium sp. fungi heterotrophic oxalate, malate, pyruvate, oxalacetate    [11] 
Gallionella sp. bacteria autotrophic ferric iron 6.4–6.8  6–25 [10] 
Gleophyllum trabeum fungi heterotrophic oxalate    [13] 
Leptospirillum ferrooxidans bacteria chemolithoautotrophic ferric iron  2.5–3.0 30 [9, 10] 
Leptospirillum thermoferrooxidans bacteria chemolithoautotrophic ferric iron  1.7–1.9 45–50 [8] 
Leptotrix sp. bacteria facult. autotrophic ferric iron, sulfuric acid 5.8–7.8  5–40 [10] 
Metallogenium sp. bacteria heterotrophic ferric iron 3.5–6.8 4.1  [10] 
Metallosphaera sedula bacteria chemolithoautotrophic ferric iron, sulfuric acid acidophilic  extr. thermophilic [8, 10] 
Mucor sp. fungi heterotrophic fumatate, gluconate    [11] 
Paecilomyces variotii fungi heterotrophic malate    [11] 
Penicillium brevicompactum fungi heterotrophic     [11] 
Penicillium cyclopium fungi heterotrophic     [11] 
Penicillium funiculosum fungi heterotrophic citrate, glutamate    [11] 
Penicillium notatum fungi heterotrophic     [11] 
Penicillium ochrochloron fungi heterotrophic oxalate    [11] 
Penicillium oxalicum fungi heterotrophic oxalate    [13] 
Penicillium simplicissimum fungi heterotrophic citrate, oxalate, gluconate    [13] 
Penicillium spinulosum fungi heterotrophic oxalate    [11, 14] 
Penicillium variotii fungi heterotrophic     [11] 
Phanerochaete chrysosporium fungi heterotrophic     [11] 
Pichia sp. fungi heterotrophic     [11] 
Pseudomonas putida bacteria heterotrophic citrate, gluconate    [15] 
Rhizopus sp. fungi heterophic lactate, fumarate, gluconate    [11] 
Schizophyllum commune fungi heterotrophic malate    [11] 
Sclerotium rolfsii fungi heterotrophic oxalate    [13] 
Siderocapsa sp. bacteria heterotrophic ferric iron    [10] 
Sulfobacillus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfobacillus thermosulfidooxidans sub. thermotolerans archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  37–42 [8] 
Sulfobacillus thermosulfidooxidans sub. asporogenes archaea chemolithoautotrophic ferric iron, sulfuric acid extremely acidophilic  50 [8] 
Sulfolobus acidocaldarius archaea chemolithoautotrophic ferric iron, sulfuric acid 0.9–5.8 2.0–3.0 55–85 [9, 10] 
Sulfolobus ambivalens archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus solfataricus archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus thermosulfidooxidans archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8, 10] 
Sulfolobus brierleyi archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [17] 
Sulfolobus yellowstonii archaea chemolithoautotrophic ferric iron, sulfuric acid   extremely thermophilic [8] 
Sulfurococcus sp. bacteria mixotrophic ferric iron, sulfuric acid acidophilic  extremely thermophilic [8] 
Thermothrix thiopara bacteria chemolithoautotrophic sulfuric acid neutral  60–75 [17] 
Thiobacillus acidophilus bacteria chemolithoautotrophic sulfuric acid 1.5–6.0 3.0 25–30 [10] 
Thiobacillus albertis bacteria chemolithoautotrophic sulfuric acid 2.0–4.5 3.5–4.0 28–30 [10] 
Thiobacillus capsulatus bacteria chemolithoautotrophic sulfuric acid    [18] 
Thiobacillus concretivorus bacteria chemolithoautotrophic sulfuric acid 0.5–6.0   [10] 
Thiobacillus cuprinus bacteria chemolithoautotrophic sulfuric acid    [19] 
Thiobacillus delicatus bacteria mixotrophic sulfuric acid  5.0–7.0 25–30 [10] 
Thiobacillus denitrificans bacteria chemolithoautotrophic sulfuric acid 5.0–7.0  30 [10] 
Thiobacillus ferrooxidans bacteria chemolithoautotrophic ferric iron, sulfuric acid 1.4–6.0 2.4 28–35 [7, 9, 10] 
Thiobacillus intermedius bacteria chemolithoautotrophic sulfuric acid 1.9–7.0 6.8 30 [10] 
Thiobacillus kabobis bacteria mixotrophic sulfuric acid 1.8–6.0 3.0 28 [10] 
Thiobacillus neapolitanus bacteria chemolithoautotrophic sulfuric acid 3.0–8.5 6.2–7.0 28 [10] 
Thiobacillus novellus bacteria chemolithoautotrophic sulfuric acid 5.0–9.0 7.8–9.0 30 [10] 
Thiobacillus organoparus bacteria mixotrophic sulfuric acid 1.5–5.0 2.5–3.0 27–30 [10] 
Thiobacillus perometabolis bacteria chemolithoheterotrophic sulfuric acid 2.6–6.8 6.9 30 [10] 
Thiobacillus prosperus bacteria chemolithoautotrophic sulfuric acid    [20] 
Thiobacillus rubellus bacteria chemolithoautotrophic sulfuric acid  5.0–7.0 25–30 [8, 10] 
Thiobacillus tepidarius bacteria chemolithoautotrophic sulfuric acid    [21] 
Thiobacillus thiocynoxidans bacteria chemolithoautotrophic sulfuric acid    [22] 
Thiobacillus thiooxidans bacteria chemolithoautotrophic sulfuric acid 0.5–6.0 2.0–3.5 10–37 [10] 
Thiobacillus thioparus bacteria chemolithoautotrophic sulfuric acid 4.5–10.0 6.6–7.2 11–25 [10] 
Thiobacillus versutus bacteria chemolithoautotrophic sulfuric acid  8.0–9.0  [10] 
Trametes versicolor fungi heterotrophic     [11] 
Trichoderma harzianum bacteria heterotrophic     [11] 
Trichoderma viride bacteria heterotrophic     [23] 
Yarrowia lipolytica fungi heterotrophic citrate    [11] 
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The ability of microorganisms to leach and mobilize metals from solid materials comprises three principles, namely (i) redox reactions, (ii) the formation of organic or inorganic acids, and (iii) the excretion of complexing agents. The mediation by redox reactions is based either on electron transfer from minerals to microorganisms in the case of physical contact between organisms and solids or on bacterial oxidation of Fe2+ to Fe3+ where ferric iron subsequently catalyzes metal solubilization as an oxidizing agent [25].

3 Industrial applications and patents

Leaching processes have been investigated for the recovery of cadmium, cobalt, copper, gold, manganese, nickel, plutonium, silver, uranium, and zinc from ores and concentrates as well as for the removal of pyrite from coal [26–30]. Currently, these microbiological technologies are used on an industrial scale only for the recovery of copper, gold, or uranium from ores [9, 25, 30]. Subjecting refractory gold ore to microbial treatment prior to conventional chemical extraction can substantially increase recovery by promoting biological transformation of the minerals the gold is trapped in [32, 33]. The first bioleaching plant for copper in the United States was opened in 1989 [34].

Recent technical data on the operation (usage of water, energy, air, or chemicals) of bioleaching plants are rarely published. Usually, a 5–20% (w/w) ore suspension is used in reactors with capacities from 600 to 600 000 liters [10, 26, 31, 34]. In processes independent of reactors (‘heap leaching’) 80 000 liters of water was used per minute in a sprinkler system to leach metals from 1.5×106 tons of low-grade (0.3%) copper ore [1]. The copper content of the leachate was 0.5 g/l. The obtained copper represented 30% of the total copper obtained by conventional winning techniques from this mine.

Several leaching processes of metals from ores have been recently patented. A summary is given in Table 3. Most of the patents are filed for the winning of precious metals such as silver or gold and chemolithoautotrophic microorganisms such as Thiobacillus are applied for metal mobilization.

Table 3

Patents on biohydrometallurgical processing of ores

Type of ore Metals recovered Microorganisms Reference 
Iron ore Fe Pseudomonas sp. [35] 
Gold ore Au Chromobacterium violoceum, Chlorella vulgaris [36] 
Carbon containing gold ore Au Thiobacillus sp., heterotrophic fungal and bacterial strains [37] 
Sulfidic gold ore Au, Ag, Cu Thiobacillus ferrooxidans [38] 
Manganiferous silver ore Ag Bacillus sp., Bacillus polymyxa [39] 
Sulfidic ore Au, Ag, Cu Thiobacillus sp., Leptospirillum ferrooxidans [40] 
Sulfidic ore Au, Ag, Pt sulfate and hydrogen reducing bacteria [41] 
Type of ore Metals recovered Microorganisms Reference 
Iron ore Fe Pseudomonas sp. [35] 
Gold ore Au Chromobacterium violoceum, Chlorella vulgaris [36] 
Carbon containing gold ore Au Thiobacillus sp., heterotrophic fungal and bacterial strains [37] 
Sulfidic gold ore Au, Ag, Cu Thiobacillus ferrooxidans [38] 
Manganiferous silver ore Ag Bacillus sp., Bacillus polymyxa [39] 
Sulfidic ore Au, Ag, Cu Thiobacillus sp., Leptospirillum ferrooxidans [40] 
Sulfidic ore Au, Ag, Pt sulfate and hydrogen reducing bacteria [41] 
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Table 3

Patents on biohydrometallurgical processing of ores

Type of ore Metals recovered Microorganisms Reference 
Iron ore Fe Pseudomonas sp. [35] 
Gold ore Au Chromobacterium violoceum, Chlorella vulgaris [36] 
Carbon containing gold ore Au Thiobacillus sp., heterotrophic fungal and bacterial strains [37] 
Sulfidic gold ore Au, Ag, Cu Thiobacillus ferrooxidans [38] 
Manganiferous silver ore Ag Bacillus sp., Bacillus polymyxa [39] 
Sulfidic ore Au, Ag, Cu Thiobacillus sp., Leptospirillum ferrooxidans [40] 
Sulfidic ore Au, Ag, Pt sulfate and hydrogen reducing bacteria [41] 
Type of ore Metals recovered Microorganisms Reference 
Iron ore Fe Pseudomonas sp. [35] 
Gold ore Au Chromobacterium violoceum, Chlorella vulgaris [36] 
Carbon containing gold ore Au Thiobacillus sp., heterotrophic fungal and bacterial strains [37] 
Sulfidic gold ore Au, Ag, Cu Thiobacillus ferrooxidans [38] 
Manganiferous silver ore Ag Bacillus sp., Bacillus polymyxa [39] 
Sulfidic ore Au, Ag, Cu Thiobacillus sp., Leptospirillum ferrooxidans [40] 
Sulfidic ore Au, Ag, Pt sulfate and hydrogen reducing bacteria [41] 
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4 Solid wastes as metal resource

Industrial waste materials (e.g., slag, galvanic sludge, filter dust, fly ash) often represent valuable metal-containing concentrates. For these materials biological processing can be economically effective and is thought to be an important industrial process to recycle elements (Table 4). Mostly Thiobacillus strains are applied for metal solubilization. However, also heterotrophic microorganisms such as Aspergillus are used to remove metal from solid waste (Table 4). These industrial wastes serve as solid substrates for bioleaching processes and can be considered a ‘renewable resource’ decreasing the demand for metal supply by mining activities. So far, leaching processes have been applied to industrial solid waste materials mainly for the recovery of copper and zinc. They are extracted with efficiencies of close to 100%[55].

Table 4

Industrials wastes as solid substrates for bioleaching processes

Type of waste Metals recovered Microorganisms References 
Sewage sludge heavy metals Thiobacilli [22] 
Galvanic sludge Cu Thiobacilli [42, 43] 
 Cu, Cr, Zn Thiobacillus thiooxidans  
Red mud from alkaline Al extraction Al Thiobacilli, Aspergillus niger, Penicillium notatum, Penicillium simplicissimum, Trichoderma viride [23] 
Filter press residues Cu, Cr, V, Zn Thiobacillus thiooxidans [43] 
Filter dust Cu, Cr, Zn Thiobacillus thiooxidans [43] 
Various filter dusts Zn Thiobacillus thiooxidans [44] 
Coal fly ash Al Aspergillus niger [45, 48] 
 metals Thiobacillus thiooxidans [46] 
 metal oxides Rhodococcus sp. [47] 
Electro-filter dust from heavy oil combustion Ni, V Thiobacillus ferrooxidans, Aspergillus niger, Penicillium simpilicissimum [49] 
Municipal solid waste fly ash Zn Thiobacillus thiooxidans [43] 
 heavy metals Aspergillus niger [5] 
Oxidic fly ash from pyrite roasting Cu Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Sulfidic dust concentrates after flotations Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Filter dust of a copper works Cu, Pb, Zn Brettanomyces lambicus [51] 
 Zn Penicillium simplicissimum [52] 
 Zn Pseudomonas putida [16] 
Soda slag Zn Thiobacillus thiooxidans [43] 
Slag from lead melting process Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Nickel matte (lead smelting) Co Thiobacillus ferrooxidans [53] 
Solid waste of a tanning factory Cr Penicillium simplicissimum [11] 
Used catalyst from silane production Cu Thiobacillus ferrooxidans [54] 
 Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Residue from zinc electrolysis Zn Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Coprecipitated metals metals Clostridium sp. [56] 
Semi-conductors, electronic scrap Ga, As ‘Sulfolobus’ [57] 
Electronic waste Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Type of waste Metals recovered Microorganisms References 
Sewage sludge heavy metals Thiobacilli [22] 
Galvanic sludge Cu Thiobacilli [42, 43] 
 Cu, Cr, Zn Thiobacillus thiooxidans  
Red mud from alkaline Al extraction Al Thiobacilli, Aspergillus niger, Penicillium notatum, Penicillium simplicissimum, Trichoderma viride [23] 
Filter press residues Cu, Cr, V, Zn Thiobacillus thiooxidans [43] 
Filter dust Cu, Cr, Zn Thiobacillus thiooxidans [43] 
Various filter dusts Zn Thiobacillus thiooxidans [44] 
Coal fly ash Al Aspergillus niger [45, 48] 
 metals Thiobacillus thiooxidans [46] 
 metal oxides Rhodococcus sp. [47] 
Electro-filter dust from heavy oil combustion Ni, V Thiobacillus ferrooxidans, Aspergillus niger, Penicillium simpilicissimum [49] 
Municipal solid waste fly ash Zn Thiobacillus thiooxidans [43] 
 heavy metals Aspergillus niger [5] 
Oxidic fly ash from pyrite roasting Cu Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Sulfidic dust concentrates after flotations Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Filter dust of a copper works Cu, Pb, Zn Brettanomyces lambicus [51] 
 Zn Penicillium simplicissimum [52] 
 Zn Pseudomonas putida [16] 
Soda slag Zn Thiobacillus thiooxidans [43] 
Slag from lead melting process Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Nickel matte (lead smelting) Co Thiobacillus ferrooxidans [53] 
Solid waste of a tanning factory Cr Penicillium simplicissimum [11] 
Used catalyst from silane production Cu Thiobacillus ferrooxidans [54] 
 Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Residue from zinc electrolysis Zn Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Coprecipitated metals metals Clostridium sp. [56] 
Semi-conductors, electronic scrap Ga, As ‘Sulfolobus’ [57] 
Electronic waste Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
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Table 4

Industrials wastes as solid substrates for bioleaching processes

Type of waste Metals recovered Microorganisms References 
Sewage sludge heavy metals Thiobacilli [22] 
Galvanic sludge Cu Thiobacilli [42, 43] 
 Cu, Cr, Zn Thiobacillus thiooxidans  
Red mud from alkaline Al extraction Al Thiobacilli, Aspergillus niger, Penicillium notatum, Penicillium simplicissimum, Trichoderma viride [23] 
Filter press residues Cu, Cr, V, Zn Thiobacillus thiooxidans [43] 
Filter dust Cu, Cr, Zn Thiobacillus thiooxidans [43] 
Various filter dusts Zn Thiobacillus thiooxidans [44] 
Coal fly ash Al Aspergillus niger [45, 48] 
 metals Thiobacillus thiooxidans [46] 
 metal oxides Rhodococcus sp. [47] 
Electro-filter dust from heavy oil combustion Ni, V Thiobacillus ferrooxidans, Aspergillus niger, Penicillium simpilicissimum [49] 
Municipal solid waste fly ash Zn Thiobacillus thiooxidans [43] 
 heavy metals Aspergillus niger [5] 
Oxidic fly ash from pyrite roasting Cu Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Sulfidic dust concentrates after flotations Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Filter dust of a copper works Cu, Pb, Zn Brettanomyces lambicus [51] 
 Zn Penicillium simplicissimum [52] 
 Zn Pseudomonas putida [16] 
Soda slag Zn Thiobacillus thiooxidans [43] 
Slag from lead melting process Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Nickel matte (lead smelting) Co Thiobacillus ferrooxidans [53] 
Solid waste of a tanning factory Cr Penicillium simplicissimum [11] 
Used catalyst from silane production Cu Thiobacillus ferrooxidans [54] 
 Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Residue from zinc electrolysis Zn Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Coprecipitated metals metals Clostridium sp. [56] 
Semi-conductors, electronic scrap Ga, As ‘Sulfolobus’ [57] 
Electronic waste Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Type of waste Metals recovered Microorganisms References 
Sewage sludge heavy metals Thiobacilli [22] 
Galvanic sludge Cu Thiobacilli [42, 43] 
 Cu, Cr, Zn Thiobacillus thiooxidans  
Red mud from alkaline Al extraction Al Thiobacilli, Aspergillus niger, Penicillium notatum, Penicillium simplicissimum, Trichoderma viride [23] 
Filter press residues Cu, Cr, V, Zn Thiobacillus thiooxidans [43] 
Filter dust Cu, Cr, Zn Thiobacillus thiooxidans [43] 
Various filter dusts Zn Thiobacillus thiooxidans [44] 
Coal fly ash Al Aspergillus niger [45, 48] 
 metals Thiobacillus thiooxidans [46] 
 metal oxides Rhodococcus sp. [47] 
Electro-filter dust from heavy oil combustion Ni, V Thiobacillus ferrooxidans, Aspergillus niger, Penicillium simpilicissimum [49] 
Municipal solid waste fly ash Zn Thiobacillus thiooxidans [43] 
 heavy metals Aspergillus niger [5] 
Oxidic fly ash from pyrite roasting Cu Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Sulfidic dust concentrates after flotations Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Filter dust of a copper works Cu, Pb, Zn Brettanomyces lambicus [51] 
 Zn Penicillium simplicissimum [52] 
 Zn Pseudomonas putida [16] 
Soda slag Zn Thiobacillus thiooxidans [43] 
Slag from lead melting process Cu, Zn Thiobacillus ferrooxidans [50] 
  Thiobacillus thiooxidans [44] 
Nickel matte (lead smelting) Co Thiobacillus ferrooxidans [53] 
Solid waste of a tanning factory Cr Penicillium simplicissimum [11] 
Used catalyst from silane production Cu Thiobacillus ferrooxidans [54] 
 Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
Residue from zinc electrolysis Zn Thiobacillus ferrooxidans, Thiobacillus thiooxidans [50] 
Coprecipitated metals metals Clostridium sp. [56] 
Semi-conductors, electronic scrap Ga, As ‘Sulfolobus’ [57] 
Electronic waste Cu, Pb, Sn Bacillus sp., Saccharomyces cerevisiae, Yarrowia lipolytica [55] 
View Large

In addition, the use of microorganisms is also feasible for detoxification applications to reduce environmental pollution. Metal-contaminated soils and sediments have been microbiologically treated using various Thiobacillus species [58–60]. It has been shown for lead-, zinc-, copper-, and arsenic-containing soil that leaching efficiencies depend on the content of reduced sulfur compounds, on the content of organic carbon, and on the buffer capacity. Also, climatic conditions have to be considered when soils are treated in situ. Usually, at temperatures <15°C the leaching process not very effective [61].

5 Case study: Fly ash from municipal waste incineration

Slag and ash from municipal waste incineration represent concentrates of a wide variety of elements. These incineration residues can be considered ‘artificial ores’. Some of the elements (i.e., Al, Zn) are present in concentrations that allow economic recovery of the metal (Table 1). Other compounds (i.e., Ag, Ni, Zr) show relatively low concentrations (comparable to low-grade ores), which makes conventional technical recovery difficult. Especially in these cases, microbial processes are the technique of choice and basically the only possibility to obtain metal from these materials. In addition, the low toxicity of these residues to bacteria has been demonstrated [62]. Therefore, a biological metal recovery process is potentially feasible. In a recent study, Pseudomonas putida, Aspergillus niger, Thiobacillus thiooxidans and T. ferrooxidans were used as test organisms and incubated with fly ash obtained from municipal waste incineration.

When P. putida (DSM 548) was exposed to fly ash in batch cultures (baffled shake flasks, 110 rpm), citric acid – a product from the carbohydrate metabolism – acted with its complexing properties as leaching agent. The composition of the growth medium has been published elsewhere [63]. Glucose (24–42 g/l) was used as sole carbon source. Within a growth period of less than one week the pH dropped to about 4. Highest metal leaching efficiencies were in the range of 60–80% of the total content of a certain element present in the fly ash. For fly ash concentrations of >30 g/l, efficiencies were below 20% for all elements (Fig. 1). The reason was a limitation of the carbon source. Therefore, the pH did not decrease further and the ratio of citrate to fly ash was lower [64].

Figure 1
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Pseudomonas putida when grown in batch cultures (baffled shake flasks, 110 rpm) on glucose for 5 days at 30°C. The pH decreased constantly during growth on 1% fly ash from 8 to approximately 4. Microbially produced citric acid acted as leaching agent. A detailed description of the chemical composition of the fly ash has been published elsewhere [4, 5].
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Pseudomonas putida when grown in batch cultures (baffled shake flasks, 110 rpm) on glucose for 5 days at 30°C. The pH decreased constantly during growth on 1% fly ash from 8 to approximately 4. Microbially produced citric acid acted as leaching agent. A detailed description of the chemical composition of the fly ash has been published elsewhere [4, 5].

Figure 1
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Pseudomonas putida when grown in batch cultures (baffled shake flasks, 110 rpm) on glucose for 5 days at 30°C. The pH decreased constantly during growth on 1% fly ash from 8 to approximately 4. Microbially produced citric acid acted as leaching agent. A detailed description of the chemical composition of the fly ash has been published elsewhere [4, 5].
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Pseudomonas putida when grown in batch cultures (baffled shake flasks, 110 rpm) on glucose for 5 days at 30°C. The pH decreased constantly during growth on 1% fly ash from 8 to approximately 4. Microbially produced citric acid acted as leaching agent. A detailed description of the chemical composition of the fly ash has been published elsewhere [4, 5].

In the presence of fly ash, the heterotrophic fungus A. niger produced gluconic acid instead of citric acid due to the inhibition of enzymes in the TCA cycle by manganese. The chemical composition of the growth medium and the fly ash as well as culture conditions have been published elsewhere [5]. On sucrose (100 g/l), growth was completed after 2–3 weeks and the pH decreased within the growth period from approximately 10 to 4–5 depending on the amount of fly ash added. As a result, metal leaching efficiencies of >80% for certain elements were observed (Fig. 2). A. niger proved especially effective for the leaching of Pb [5].

Figure 2
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Aspergillus niger when grown in batch cultures (baffled shake flasks, 130 rpm) on sucrose at 30°C [5]. Microbially produced gluconic acid acted as leaching agent. Incubations were carried out until final pH was constant. Therefore, incubation times varied between 16 and 22 days depending on the amount of fly ash added. The chemical composition of the growth medium and the fly ash has been published elsewhere [5].
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Aspergillus niger when grown in batch cultures (baffled shake flasks, 130 rpm) on sucrose at 30°C [5]. Microbially produced gluconic acid acted as leaching agent. Incubations were carried out until final pH was constant. Therefore, incubation times varied between 16 and 22 days depending on the amount of fly ash added. The chemical composition of the growth medium and the fly ash has been published elsewhere [5].

Figure 2
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Aspergillus niger when grown in batch cultures (baffled shake flasks, 130 rpm) on sucrose at 30°C [5]. Microbially produced gluconic acid acted as leaching agent. Incubations were carried out until final pH was constant. Therefore, incubation times varied between 16 and 22 days depending on the amount of fly ash added. The chemical composition of the growth medium and the fly ash has been published elsewhere [5].
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Aspergillus niger when grown in batch cultures (baffled shake flasks, 130 rpm) on sucrose at 30°C [5]. Microbially produced gluconic acid acted as leaching agent. Incubations were carried out until final pH was constant. Therefore, incubation times varied between 16 and 22 days depending on the amount of fly ash added. The chemical composition of the growth medium and the fly ash has been published elsewhere [5].

Sulfuric acid produced by the autotrophic organism T. thiooxidans (DSM 504) during oxidation of elemental sulfur acted as leaching agent as well (Fig. 3). The growth medium consisted of tap water, 1% (w/v) elemental sulfur, and 4% (v/v) anoxic sewage sludge as inoculum to enrich Thiobacilli. In addition, a pure culture of T. thiooxidans was added after 3 days to the enrichments to enhance metal leaching. Cultivation was performed in batch cultures (baffled shake flasks, 110 rpm). Growth and pH decrease depended on the amount of fly ash added and generally lasted 1–3 months. At the end of the growth phase, the pH had dropped to a value of approximately 1. Elements such as cadmium, copper, or zinc were mobilized by >80%, whereas others (e.g., Pb) were solubilized only by a small percentage [64].

Figure 3
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by an enrichment of Thiobacilli from anoxic sewage sludge. Growth was performed chemolithoautotrophically in batch cultures (baffled shake flasks, 110 rpm) for approximately 60 days at 30°C. The chemical composition of the fly ash has been published elsewhere [5]. Microbially produced sulfuric acid acted as leaching agent. pH decreased during the growth period from approximately 10 to about 1.
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by an enrichment of Thiobacilli from anoxic sewage sludge. Growth was performed chemolithoautotrophically in batch cultures (baffled shake flasks, 110 rpm) for approximately 60 days at 30°C. The chemical composition of the fly ash has been published elsewhere [5]. Microbially produced sulfuric acid acted as leaching agent. pH decreased during the growth period from approximately 10 to about 1.

Figure 3
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by an enrichment of Thiobacilli from anoxic sewage sludge. Growth was performed chemolithoautotrophically in batch cultures (baffled shake flasks, 110 rpm) for approximately 60 days at 30°C. The chemical composition of the fly ash has been published elsewhere [5]. Microbially produced sulfuric acid acted as leaching agent. pH decreased during the growth period from approximately 10 to about 1.
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by an enrichment of Thiobacilli from anoxic sewage sludge. Growth was performed chemolithoautotrophically in batch cultures (baffled shake flasks, 110 rpm) for approximately 60 days at 30°C. The chemical composition of the fly ash has been published elsewhere [5]. Microbially produced sulfuric acid acted as leaching agent. pH decreased during the growth period from approximately 10 to about 1.

Biohydrometallurgical processing of fly ash poses serious problems especially at higher pulp densities, because of the high content of toxic metals and the saline and strongly alkaline (pH>10) environment. For examining the biological leaching of fly ash at high pulp densities, pulp (80 g/l) from a storage vessel was mixed with a culture of T. ferrooxidans and T. thiooxidans in such a way that three stirred reaction vessels (vessels A, B, and C; each of them 1 dm3) ran serially in a semi-continuous process at pulp densities of 48 g/l [65]. The overflow of vessel A was fed to vessel B, and the overflow of vessel B was fed to vessel C in order to decrease the pH stepwise from bioreactor to bioreactor. The results show that leaching efficiencies were of the same order as in experiments where T. thiooxidans was grown in batch cultures (Fig. 4). However, by employing a semi-continuous process higher pulp densities can be applied resulting in increased overall loads of elements in a shorter time period as compared to batch cultures. This experimental installation seems to be a promising first step on the way to a pilot plant with high capacities to detoxify fly ash and to recover metals from this material [65].

Figure 4
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Thiobacillus thiooxidans and T. ferrooxidans at pulp densities of 4% (w/v) [65]. Metal leaching was performed semi-continuously at room temperature (22°C) in a series of three connected reaction vessels (A, B, C) with retention times of 2 days in each vessel. pH values in vessel A, B and C were approximately 3, 2 and 1.5, respectively, and were constant throughout the experiment. The growth medium consisted of (grams per liter of distilled water) K2HPO4 (0.1), MgSO4·7H2O (0.25), (NH4)2SO4 (2.0), KCl (0.1), FeSO4·7H2O (8), powdered sulfur (10) and H2SO4 (1 ml). pH was 2.5–2.7.
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Thiobacillus thiooxidans and T. ferrooxidans at pulp densities of 4% (w/v) [65]. Metal leaching was performed semi-continuously at room temperature (22°C) in a series of three connected reaction vessels (A, B, C) with retention times of 2 days in each vessel. pH values in vessel A, B and C were approximately 3, 2 and 1.5, respectively, and were constant throughout the experiment. The growth medium consisted of (grams per liter of distilled water) K2HPO4 (0.1), MgSO4·7H2O (0.25), (NH4)2SO4 (2.0), KCl (0.1), FeSO4·7H2O (8), powdered sulfur (10) and H2SO4 (1 ml). pH was 2.5–2.7.

Figure 4
Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Thiobacillus thiooxidans and T. ferrooxidans at pulp densities of 4% (w/v) [65]. Metal leaching was performed semi-continuously at room temperature (22°C) in a series of three connected reaction vessels (A, B, C) with retention times of 2 days in each vessel. pH values in vessel A, B and C were approximately 3, 2 and 1.5, respectively, and were constant throughout the experiment. The growth medium consisted of (grams per liter of distilled water) K2HPO4 (0.1), MgSO4·7H2O (0.25), (NH4)2SO4 (2.0), KCl (0.1), FeSO4·7H2O (8), powdered sulfur (10) and H2SO4 (1 ml). pH was 2.5–2.7.
View largeDownload slide

Efficiency of heavy metal removal from various amounts (w/v) of municipal waste incineration fly ash by Thiobacillus thiooxidans and T. ferrooxidans at pulp densities of 4% (w/v) [65]. Metal leaching was performed semi-continuously at room temperature (22°C) in a series of three connected reaction vessels (A, B, C) with retention times of 2 days in each vessel. pH values in vessel A, B and C were approximately 3, 2 and 1.5, respectively, and were constant throughout the experiment. The growth medium consisted of (grams per liter of distilled water) K2HPO4 (0.1), MgSO4·7H2O (0.25), (NH4)2SO4 (2.0), KCl (0.1), FeSO4·7H2O (8), powdered sulfur (10) and H2SO4 (1 ml). pH was 2.5–2.7.

The results show the potential of different microorganisms to leach substantial quantities of toxic metals from fly ash. Depending on the point of view, the mobilization or bioleaching of these metals could be either a hazard for the environment (leachates from landfills or ore deposits) or a chance to reduce toxic elements (to fulfil the regulations for landfilling or even better for a re-use of the fly ash, e.g., for construction purposes) and to recover valuable metals (e.g., zinc) by a low cost and low energy level technology compared with thermal treatment (e.g., vitrification or evaporation).

6 Perspectives for bioleaching processes

According to the Agenda 21 established at the Earth Summit in Rio de Janeiro (1992), it is a strong requirement that in the field of biotechnology progress must be made towards a more environmentally friendly winning of mineral resources [66]. The application of biological metal leaching processes is a step in this direction. Bioleaching technologies described must be seen in the context of a future in which industrial technologies have to be more in harmony with global material cycles within the biosphere [67]. There are several advantages of bioleaching techniques compared to chemical leaching (Table 5).

Table 5

Biological leaching of metals from waste incineration residues compared with thermal treatment or chemical leaching

Advantages Disadvantages 
– leaching agents are produced in situ (no need for transportation) – long reaction times 
– formation of a micro-climate around particles with elevated concentrations of leaching agents – dependence on climate (when residues are treated in the field) 
– microbial selectivity depending on strain used and leaching conditions – heavy metal toxicity to microorganisms 
– increase in leaching efficiency – potential for acid leaks 
– excretion of surfactants  
– low energy demand  
– no emission of gaseous pollutants  
Advantages Disadvantages 
– leaching agents are produced in situ (no need for transportation) – long reaction times 
– formation of a micro-climate around particles with elevated concentrations of leaching agents – dependence on climate (when residues are treated in the field) 
– microbial selectivity depending on strain used and leaching conditions – heavy metal toxicity to microorganisms 
– increase in leaching efficiency – potential for acid leaks 
– excretion of surfactants  
– low energy demand  
– no emission of gaseous pollutants  
View Large
Table 5

Biological leaching of metals from waste incineration residues compared with thermal treatment or chemical leaching

Advantages Disadvantages 
– leaching agents are produced in situ (no need for transportation) – long reaction times 
– formation of a micro-climate around particles with elevated concentrations of leaching agents – dependence on climate (when residues are treated in the field) 
– microbial selectivity depending on strain used and leaching conditions – heavy metal toxicity to microorganisms 
– increase in leaching efficiency – potential for acid leaks 
– excretion of surfactants  
– low energy demand  
– no emission of gaseous pollutants  
Advantages Disadvantages 
– leaching agents are produced in situ (no need for transportation) – long reaction times 
– formation of a micro-climate around particles with elevated concentrations of leaching agents – dependence on climate (when residues are treated in the field) 
– microbial selectivity depending on strain used and leaching conditions – heavy metal toxicity to microorganisms 
– increase in leaching efficiency – potential for acid leaks 
– excretion of surfactants  
– low energy demand  
– no emission of gaseous pollutants  
View Large

Industrial technologies of the future must be friendly to humans and the environment. They are based on four key characteristics, namely (i) they should be based on renewable resources, (ii) they should use ‘mild’ production processes, (iii) resulting products and services should be environmentally compatible, and (iv) any waste they generate should be recyclable [66]. Whereas classical bioprocesses have been applied for decades (i.e., food processing) often on a large scale, process-integrated industrial biological technology (‘clean technology’) is still in its infancy. Industry views this as a very promising technology for sustainable development [67]. Especially metal recovery by biological means should be improved.

Acknowledgements

This work was supported by the Swiss National Science Foundation within the Priority Program Environment. Information on the program can be obtained from http://www.IP-Waste.unibe.ch

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