Exploring the potential of acidithiobacillus in bioleaching: keys to sustainable metal extraction

Document Type : Review Paper

Authors

1 Carrera de Ingeniería Ambiental, Facultad de Ciencias Químicas, Universidad de Cuenca, Ecuador

2 Escuela de Posgrado, Universidad San Ignacio de Loyola, Peru

3 Facultad de Ingeniería Industrial, Universidad Tecnológica del Perú, Lima, Perú

10.22059/ijmge.2026.396449.595266

Abstract

The Acidithiobacillus genus is a set of acidophilic bacteria that has a crucial participation in the bioleaching process, because they can oxidize iron and sulfur and contribute to the sulfide mineral dissolution, releasing metals such as: copper, gold, and other valuable items. This systematic review compiled the environmental factors and optimal conditions for the use of the Acidithiobacillus proteobacteria in the bioleaching process in the Scopus database since January 2014 until December 2024. PRISMA’s guidelines were used for the identification, selection, and analysis of relevant primary studies. The results and discussions of each article were examined, synthesizing the answers to the questions posed and highlighting the most relevant findings along with their implications for the field of biomining. In conclusion, it is evident that biomining with Acidithiobacillus emerges as an innovative and sustainable alternative for the metal extraction, offering environmental, economic and technical advantages compared to traditional methods. Despite it, the associated technical challenges are recognized, such as the control of leaching conditions, where factors such as: pH, temperature, redox potential, oxygen concentration, and the presence of metal ions can influence the growth and the activity of Acidithiobacillus, as well as the kinetics and leaching mechanisms. Research opportunities were identified for improving this innovative technology.

Keywords

Main Subjects


[1] Chaudhary, S., Sindhu, S. S., Dhanker, R., Kumari, A. (2023). Microbes-mediated sulphur cycling in soil: Impact on soil fertility, crop production and environmental sustainability. Microbiological Research, 271(127340), 127340.
[2] Wang, Y., Zhao, Z., Lin, J., Ma, Q., Chen, L. (2024). A new bio-oxidation method for removing iron deposits from waterlogged wood of Nanhai I shipwreck, Guangdong, China. Engineering Microbiology, 4(1), 100107. https://doi.org/10.1016/j.engmic.2023.100107
[3] Zhang, S., Yan, L., Xing, W., Chen, P., Zhang, Y., Wang, W. (2018). Acidithiobacillus ferrooxidans and its potential application. Extremophiles: Life under Extreme Conditions, 22(4), 563-579. https://doi.org/10.1007/s00792-018-1024-9
[4] Abdollahi, H., Shafaei, S. Z., Noaparast, M. and Manafi, Z. (2017). Mixed moderate thermophilic bioleaching of Cu, Mo and Re from molybdenite concentrate: effects of silver ion, medium and energy sources. International Journal of Mining and Geo-Engineering51(2), 151-159. doi: 10.22059/ijmge.2017.220805.594640
[5] Ye, M., Yan, P., Sun, S., Han, D., Xiao, X., Zheng, L., Huang, S., Chen, Y., Zhuang, S. (2017). Bioleaching combined brine leaching of heavy metals from lead-zinc mine tailings: Transformations during the leaching process. Chemosphere, 168, 1115-1125. https://doi.org/10.1016/j.chemosphere.2016.10.095
[6] Ouyang, J., Guo, W., Li, B., Gu, L., Zhang, H., Chen, X. (2013). Proteomic analysis of differential protein expression in Acidithiobacillus ferrooxidans cultivated in high potassium concentration. Microbiological Research, 168(7), 455-460. https://doi.org/10.1016/j.micres.2013.01.007
[7] Wang, R., Lin, J.-Q., Liu, X.-M., Pang, X., Zhang, C.-J., Yang, C.-L., Gao, X.-Y., Lin, C.-M., Li, Y.-Q., Li, Y., Lin, J.-Q., Chen, L.-X. (2019). Sulfur Oxidation in the Acidophilic Autotrophic Acidithiobacillus spp. Frontiers in microbiology, 10;9:3290. https://doi.org/10.3389/fmicb.2018.03290
[8] Ibáñez, A., Garrido-Chamorro, S., Coque, J. J. R., Barreiro, C. (2023). From Genes to Bioleaching: Unraveling Sulfur Metabolism in Acidithiobacillus Genus. Genes, 14(9), 1772. https://doi.org/10.3390/genes14091772
[9] Nuñez, H., Covarrubias, P. C., Moya-Beltrán, A., Issotta, F., Atavales, J., Acuña, L. G., Johnson, D. B., Quatrini, R. (2016). Detection, identification and typing of Acidithiobacillus species and strains: a review. Research in Microbiology, 167(7), 555-567. https://doi.org/10.1016/j.resmic.2016.05.006
[10] Yang, L., Zhao, D., Yang, J., Wang, W., Chen, P., Zhang, S., Yan, L. (2019). Acidithiobacillus  thiooxidans and its potential application. Applied Microbiology and Biotechnology, 103(19), 7819-7833. https://doi.org/10.1007/s00253-019-10098-5
[11] Falagán C, Moya-Beltrán A, Castro M, Quatrini R, Johnson D. B. (2019). Acidithiobacillus  sulfuriphilus sp. nov.: an extremely acidophilic sulfur-oxidizing chemolithotroph isolated from a neutral pH environment. Int J Syst Evol Microbiol. 69(9):2907-2913. doi: 10.1099/ijsem.0.003576.
[12] Díaz, M, Castro M, Copaja S, Guiliani N. 2018. Biofilm Formation by the Acidophile Bacterium Acidithiobacillus thiooxidans Involves c-di-GMP Pathway and Pel exopolysaccharide. Genes. 9(2):113. doi: 10.3390/genes9020113.
[13] Heydarzadeh Sohi, F., Akhavan Sepahi, A., Rashchi, F., Kargar, M. and Angaji, S. A. (2022). Thermoacidophilic bacteria isolated from Sarcheshmeh low-grade copper ore in chalcopyrite bioleaching from mineral tailing. International Journal of Mining and Geo-Engineering56(4), 323-330. doi: 10.22059/ijmge.2022.329157.594925
[14] Johnson, D. B. (2014). Biomining-biotechnologies for extracting and recovering metals from ores and waste materials. Current Opinion in Biotechnology, 30, 24-31. https://doi.org/10.1016/j.copbio.2014.04.008
[15] Zhang, H., Wei, D., Liu, W., Hou, D., Zhang, R. (2021). Effect of polyvinyl pyrrolidone on chalcopyrite bioleaching with Acidithiobacillus ferrooxidans. Hydrometallurgy, 205(105753), 105753. https://doi.org/10.1016/j.hydromet.2021.105753
[16] Meng, J., Wang, H., Liu, X., Lin, J., Pang, X., Lin, J. (2013). Construction of small plasmid vectors for use in genetic improvement of the extremely acidophilic Acidithiobacillus caldus. Microbiological Research, 168(8), 469-476. https://doi.org/10.1016/j.micres.2013.04.003
[17] Ranjbar, M., Fazaelipoor, M. H., Ranjbar Hamghavandi, M., Schaffie, M., Manafi, Z. (2020). Modeling study of the bio-dissolution of copper concentrate in a continuous bioreactors system. Minerals Engineering, 153(106384), 106384. https://doi.org/10.1016/j.mineng.2020.106384
[18] Johnson, D. B., Aguilera, A. (2019). Extremophiles and acidic environments. In Reference Module in Life Sciences. Elsevier.
[19] Hallberg, K. B., Grail, B. M., Du Plessis, C. A., Johnson, D. B. (2011). Reductive dissolution of ferric iron minerals: A new approach for bio-processing nickel laterites. Minerals Engineering, 24(7), 620-624. https://doi.org/10.1016/j.mineng.2010.09.005
[20] Li, W., Feng Q, Li Z. (2023). Isolation and Characterization of A Novel Iron-Sulfur Oxidizing Bacterium Acidithiobacillus  Ferrooxidans YQ-N3 and its Applicability in Coal Biodesulfurization. Minerals, 13(1):95. https://doi.org/10.3390/min13010095
[21] Ríos, D., Bellenberg, S., Christel, S., Lindblom, P., Giroux, T., Dopson, M. (2024). Potential of single and designed mixed cultures to enhance the bioleaching of chalcopyrite by oxidation-reduction potential control. Hydrometallurgy, 224(106245), 106245. https://doi.org/10.1016/j.hydromet.2023.106245
[22] Inaba, Y., West, A. C.,  Banta, S. (2020). Enhanced microbial corrosion of stainless steel by Acidithiobacillus  ferrooxidans through the manipulation of substrate oxidation and overexpression of rus. Biotechnology and Bioengineering, 117(11), 3475-3485. https://doi.org/10.1002/bit.27509
[23] Jung, H., Inaba, Y., Jiang, V., West, A. C., Banta, S. (2022). Engineering polyhistidine tags on surface proteins of Acidithiobacillus  ferrooxidans: Impact of localization on the binding and recovery of divalent metal cations. ACS Applied Materials & Interfaces, 14(8), 10125-10133. https://doi.org/10.1021/acsami.1c23682
[24] Ramos-Zúñiga, J., Gallardo, S., Martínez-Bussenius, C., Norambuena, R., Navarro, C. A., Paradela, A., Jerez, C. A. (2019). Response of the biomining Acidithiobacillus  ferrooxidans to high cadmium concentrations. Journal of Proteomics, 198, 132-144. https://doi.org/10.1016/j.jprot.2018.12.013
[25] Vargas-Straube, M. J., Beard, S., Norambuena, R., Paradela, A., Vera, M., Jerez, C. A. (2020). High copper concentration reduces biofilm formation in Acidithiobacillus  ferrooxidans by decreasing production of extracellular polymeric substances and its adherence to elemental sulfur. Journal of Proteomics, 225(103874), 103874. https://doi.org/10.1016/j.jprot.2020.103874
[26] Hong, M., Wang, X., Wu, L., Fang, C., Huang, X., Liao, R., Zhao, H., Qiu, G., Wang, J. (2019). Intermediates Transformation of Bornite Bioleaching by Leptospirillum ferriphilum and Acidithiobacillus caldus. Minerals (Basel, Switzerland), 9(3), 159. https://doi.org/10.3390/min9030159
[27] Huang, T., Wei, X., Zhang, S. (2019). Bioleaching of copper sulfide minerals assisted by microbial fuel cells. Bioresource Technology, 288(121561), 121561. https://doi.org/10.1016/j.biortech.2019.121561
[28] Hallberg, K. B., González-Toril, E., Johnson, D. B. (2010). Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles: Life under Extreme Conditions, 14(1), 9-19. https://doi.org/10.1007/s00792-009-0282-y
[29] Talla, E., Hedrich, S., Mangenot, S., Ji, B., Johnson, D.B., Barbe, V. et al. (2014) Insights into the pathways of iron- and sulfur-oxidation, and bio?lm formation from the chemolithotrophic acidophile Acidithiobacillus ferrivorans CF27. Res. Microbiol. 165, 753-760, https://doi.org/10.1016/j.resmic.2014.08.002
[30] Christel, S., Fridlund, J., Buetti-Dinh, A., Buck, M., Watkin, E. L., Dopson, M. (2016). RNA transcript sequencing reveals inorganic sulfur compound oxidation pathways in the acidophileAcidithiobacillus ferrivorans. FEMS Microbiology Letters, 363(7), fnw057. https://doi.org/10.1093/femsle/fnw057
[31] Tonietti, L., Esposito, M., Cascone, M., Barosa, B., Fiscale, S., Muscari Tomajoli, M. T., Sbaffi, T., Santomartino, R., Covone, G., Cordone, A., Rotundi, A., Giovannelli, D. (2024). Unveiling the bioleaching versatility of Acidithiobacillus ferrooxidans. Microorganisms, 12(12), 2407. https://doi.org/10.3390/microorganisms12122407
[32] Chen, J., Liu, Y., Diep, P., Mahadevan, R. (2022a). Genetic engineering of extremely acidophilic Acidithiobacillus species for biomining: Progress and perspectives. Journal of Hazardous Materials, 438(129456), 129456. https://doi.org/10.1016/j.jhazmat.2022.129456
[33] Borja, D., Nguyen K. A., Silva, R. A., Park, J. H., Gupta, V., Han, Y., Lee, Y., Kim, H. (2016). Experiences and Future Challenges of Bioleaching Research in South Korea. Minerals, 6(4):128. https://doi.org/10.3390/min6040128
[34] Dong, Y., Zan, J., Lin, H. (2023). Bioleaching of heavy metals from metal tailings utilizing bacteria and fungi: Mechanisms, strengthen measures, and development prospect. Journal of Environmental Management, 344(118511), 118511. https://doi.org/10.1016/j.jenvman.2023.118511
[35] Mehrabani, J. vazife, Shafaei, S. Z., Noaparast, M. and Mousavi, M. (2016). Bioleaching of a low grade sphalerite concentrate produced from flotation tailings. International Journal of Mining and Geo-Engineering50(2), 169-173. doi: 10.22059/ijmge.2016.59825
[36] Methley, A. M., Campbell, S., Chew-Graham, C., McNally, R., Cheraghi-Sohi, S. (2014). PICO, PICOS, and SPIDER: a comparison study of specificity and sensitivity in three search tools for qualitative systematic reviews. BMC Health Serv Res. Nov 21; 14:579. doi: 10.1186/s12913-014-0579-0
[37] García-Ávila, F., Zhindón-Arévalo, C., Valdiviezo-Gonzales, L., Sánchez-Albarracín, Criollo-Bravo, J., Albuja-Arias, D., Vivar-Martínez, E. (2023) Domestic wastewater treatment at the single-family level using a septic tank and constructed wetland system: A scientometric and systematic analysis. Journal of Engineering and Applied Sciences, 18(13), 1573–1584. https://doi.org/10.59018/0723197
[38] Shamseer, L., Moher, D., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P., Stewart, L. A., the PRISMA-P Group. (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ (Clinical Research Ed.), 349(jan02 1), g7647-g7647. https://doi.org/10.1136/bmj.g7647
[39] Valdiviezo Gonzales, L. G., García Ávila, F. F., Cabello Torres, R. J., Castañeda Olivera, C. A., Alfaro Paredes, E. A. (2021). Scientometric study of drinking water treatments technologies: Present and future challenges. Cogent Engineering, 8(1). https://doi.org/10.1080/23311916.2021.1929046
[40] Mejía-Marchena, R., Maturana-Córdoba, A., Gómez-Cerón, D., Quintero-Monroy, C., Arismendy-Montes, L., Cárdenas-Pérez, C. (2023). Industrial wastewater treatment technologies for reuse, recycle, and recovery: advantages, disadvantages, and gaps. Environmental Technology Reviews, 12(1), 205–250. https://doi.org/10.1080/21622515.2023.2198147
[41] Castro, M., Deane, S. M., Ruiz, L., Rawlings, D. E., Guiliani, N. (2015). Diguanylate cyclase null mutant reveals that C-Di-GMP pathway regulates the motility and adherence of the extremophile bacterium Acidithiobacillus caldus. PLoS One.;10: e0116399. doi: 10.1371/journal.pone.0116399
[42] Gómez-Ramírez-, M., Moreno-Villanueva, F., Rojas-Avelizapa, N. G. (2020). Acidithiobacillus thiooxidans DSM 26636: An alternative for the bioleaching of metallic burrs. Catalysts (Basel, Switzerland), 10(11), 1230. https://doi.org/10.3390/catal10111230
[43] Jalali, F., Fakhar, J., Zolfaghari, A. (2020). On using a new strain of Acidithiobacillus ferridurans for bioleaching of low-grade uranium. Separation Science and Technology, 55(5), 994-1004. https://doi.org/10.1080/01496395.2019.1575417
[44] Ccorahua, R., Eca, A., Ramírez, P., Abanto, M., Garcia-de-la-Guarda, R., Sánchez, T., Sánchez-Venegas, J. (2021). Comparative genomic analysis of two novel plasmids from Acidithiobacillus ferrivorans strain PQ33. Revista peruana de biologia, 28(1), e19743. https://doi.org/10.15381/rpb.v28i1.19743
[45] Castro, M., Moya-Beltrán, A., Covarrubias, P. C., Gonzalez, M., Cardenas, J. P., Issotta, F., Nuñez, H., Acuña, L. G., Encina, G., Holmes, D. S., Johnson, D. B., Quatrini, R. (2017). Draft genome sequence of the type strain of the sulfur-oxidizing acidophile, Acidithiobacillus albertensis (DSM 14366). Standards in Genomic Sciences, 12(1). https://doi.org/10.1186/s40793-017-0282-y
[46] Falagán, C., Johnson, D. B. (2016). Acidithiobacillus ferriphilus sp. nov., a facultatively anaerobic iron- and sulfur-metabolizing extreme acidophile. International Journal of Systematic and Evolutionary Microbiology, 66(1), 206-211. https://doi.org/10.1099/ijsem.0.000698
[47] Feng, S., Yang, H., Xin, Y., Zhang, L., Kang, W., Wang, W. (2012). Isolation of an extremely acidophilic and highly efficient strain Acidithiobacillus sp. for chalcopyrite bioleaching. Journal of Industrial Microbiology & Biotechnology, 39(11), 1625-1635. https://doi.org/10.1007/s10295-012-1174-1
[48] Moya-Beltrán, A., Beard, S., Rojas-Villalobos, C. et al. (2021). Evolución genómica de la clase Acidithiobacillia: Proteobacterias de ramificación profunda que viven en condiciones ácidas extremas. ISME J 15, 3221-3238. https://doi.org/10.1038/s41396-021-00995-x
[49] Temple, K. L., Colmer, A. R. (1951). The autotrophic oxidation of iron by a new bacterium: Thiobacillus ferrooxidans. Journal of Bacteriology, 62(5), 605-611. https://doi.org/10.1128/jb.62.5.605-611.1951
[50] Waksman, S. A., Joffe, J. S. (1922). Microörganisms concerned in the oxidation of sulfur in the soil ii. Thiobacillus thiooxidans, a new sulfur-oxidizing organism isolated from the soil. Journal of Bacteriology, 7(2), 239-256. https://doi.org/10.1128/jb.7.2.239-256.1922
[51] Hedrich, S., Johnson, D. B. (2013). Acidithiobacillus ferridurans sp. nov., an acidophilic iron-, sulfur- and hydrogen-metabolizing chemolithotrophic gammaproteobacterium. International Journal of Systematic and Evolutionary Microbiology, 63(Pt_11), 4018-4025. https://doi.org/10.1099/ijs.0.049759-0
[52] Bryant, R. D., McGroarty, K. M., Costerton, J. W., Laishley, E. J. (1983). Isolation and characterization of a new acidophilic Thiobacillus species (T. albertis). Canadian Journal of Microbiology, 29(9), 1159-1170. https://doi.org/10.1139/m83-178
[53] Li, X.-T., Liang, Z.-L., Huang, Y., Jiang, Z., Yang, Z.-N., Zhou, N., Liu, Y., Liu, S.-J., Jiang, C.-Y. (2024). Acidithiobacillus acidisediminis sp. nov., an acidophilic sulphur-oxidizing chemolithotroph isolated from acid mine drainage sediment. International Journal of Systematic and Evolutionary Microbiology, 74(5). https://doi.org/10.1099/ijsem.0.005868
[54] Mandl, M., Pakostova, E., & Poskerova, L. (2014). Critical values of the volumetric oxygen transfer coefficient and oxygen concentration that prevent oxygen limitation in ferrous iron and elemental sulfur oxidation by Acidithiobacillus ferrooxidans. Hydrometallurgy, 150, 276-280. https://doi.org/10.1016/j.hydromet.2014.09.009
[55] Huang, M.-Q., Zhang, M., Zhan, S.-L., Chen, L., Xue, Z. L. (2022). Saturated dissolved oxygen concentration in in situ fragmentation bioleaching of copper sulfide ores. Frontiers in microbiology, 13. https://doi.org/10.3389/fmicb.2022.821635
 
[56] Alaba, O. Clement, Akomolafe, K. and Adepeju, A. Grace (2024). The prediction of heavy metal pollution in gemstone mines using contamination variables. International Journal of Mining and Geo-Engineering58(4), 351-358. doi: 10.22059/ijmge.2024.360223.595068
 
[57] Falagán, C., Sbaffi, T., Williams, G. B., Bargiela, R., Dew, D. W., Hudson-Edwards, K. A. (2024). Nutrient optimization in bioleaching: are we overdosing? Frontiers in microbiology, 15. https://doi.org/10.3389/fmicb.2024.1359991
[58] Jerez, C. A. (2017). Biomining of metals: how to access and exploit natural resource sustainably. Microbial Biotechnology, 10(5), 1191-1193. https://doi.org/10.1111/1751-7915.12792
[59] Jafari, M., Shafaei, S., Abdollahi, H., Gharabaghi, M., Chehreh Chelgani, S. (2016). A comparative study on the effect of flotation reagents on growth and iron oxidation activities of Leptospirillum ferrooxidans and Acidithiobacillus ferrooxidans. Minerals (Basel, Switzerland), 7(1), 2. https://doi.org/10.3390/min7010002
[60] Liao, X., Sun, S., Zhou, S., Ye, M., Liang, J., Huang, J., Guan, Z., Li, S. (2019). A new strategy on biomining of low grade base-metal sulfide tailings. Bioresource Technology, 294(122187), 122187. https://doi.org/10.1016/j.biortech.2019.122187
[61] Nguyen, V. K., Lee, M. H., Park, H. J., Lee, J.-U. (2015). Bioleaching of arsenic and heavy metals from mine tailings by pure and mixed cultures of Acidithiobacillus  spp. Journal of Industrial and Engineering Chemistry, 21, 451-458. https://doi.org/10.1016/j.jiec.2014.03.004
[62] Johnson, D. B., Smith, S. L., Santos, A. L. (2021). Bioleaching of transition metals from limonitic laterite deposits and reassessment of the multiple roles of sulfur-oxidizing acidophiles in the process. Frontiers in microbiology, 12. https://doi.org/10.3389/fmicb.2021.703177
[63] Pakostova, E., Grail, B. M., Johnson, D. B. (2017). Indirect oxidative bioleaching of a polymetallic black schist sulfide ore. Minerals Engineering, 106, 102-107. https://doi.org/10.1016/j.mineng.2016.08.028
[64] Pakostova, E., Herath, A. (2023). A bioleaching process for sustainable recycling of complex structures with multi-metal layers. Sustainability, 15(19), 14068. https://doi.org/10.3390/su151914068
[65] Shiers, D. W., Collinson, D. M., Watling, H. R. (2016). Life in heaps: a review of microbial responses to variable acidity in sulfide mineral bioleaching heaps for metal extraction. Research in Microbiology, 167(7), 576-586. https://doi.org/10.1016/j.resmic.2016.05.007
[66] Chen, J., Liu, Y., Diep, P., Mahadevan, R. (2022b). Harnessing synthetic biology for sustainable biomining with Fe/S-oxidizing microbes. Frontiers in bioengineering and biotechnology, 10. https://doi.org/10.3389/fbioe.2022.920639
[67] Muñoz-Villagrán, C., Grossolli-Gálvez, J., Acevedo-Arbunic, J., Valenzuela, X., Ferrer, A., Díez, B., Levicán, G. (2022). Characterization and genomic analysis of two novel psychrotolerant Acidithiobacillus ferrooxidans strains from polar and subpolar environments. Frontiers in microbiology, 13. https://doi.org/10.3389/fmicb.2022.960324  
[68] Mahmoud, A., Cézac, P., Hoadley, A. F. A., Contamine, F., D'Hugues, P. (2017). A review of sulfide minerals microbially assisted leaching in stirred tank reactors. International Biodeterioration & Biodegradation, 119, 118-146. https://doi.org/10.1016/j.ibiod.2016.09.015
[69] Johnson, D. B., Schippers, A. (2017). Editorial: Recent advances in acidophile microbiology: Fundamentals and applications. Frontiers in microbiology, 8. https://doi.org/10.3389/fmicb.2017.00428
[70] Holmes, D. (2008). Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications, BMC Genomics, 9(1), 597, https://doi.org/10.1186/1471-2164-9-597
[71] Naseri, T., Beiki, V., Mousavi, S. M., Farnaud, S. (2023). A comprehensive review of bioleaching optimization by statistical approaches: recycling mechanisms, factors affecting, challenges, and sustainability. RSC Advances, 13(34), 23570-23589. https://doi.org/10.1039/d3ra03498d
[72] Campodonico, M. A., Vaisman, D., Castro, J. F., Razmilic, V., Mercado, F., Andrews, B. A., Feist, A. M., Asenjo, J. A. (2016). Acidithiobacillus  ferrooxidans's comprehensive model driven analysis of the electron transfer metabolism and synthetic strain design for biomining applications. Metabolic Engineering Communications, 3, 84-96. https://doi.org/10.1016/j.meteno.2016.03.003
[73] Gao, X.-Y., Liu, X.-J., Fu, C.-A., Gu, X.-F., Lin, J.-Q., Liu, X.-M., Pang, X., Lin, J.-Q., Chen, L.-X. (2020). Novel strategy for improvement of the bioleaching efficiency of Acidithiobacillus  ferrooxidans based on the AfeI/R quorum sensing system. Minerals (Basel, Switzerland), 10(3), 222. https://doi.org/10.3390/min10030222
[74] Tezyapar Kara, I., Kremser, K., Wagland, S. T., Coulon, F. (2023). Bioleaching metal-bearing wastes and by-products for resource recovery: a review. Environmental Chemistry Letters, 21(6), 3329-3350. https://doi.org/10.1007/s10311-023-01611-4
[75] Larner, B. L., Seen, A. J., Townsend, A. T. (2006). Comparative study of optimised BCR sequential extraction scheme and acid leaching of elements in the certified reference material NIST 2711. Analytica Chimica Acta, 556(2), 444-449.
[76] Gao, X., Jiang, L., Mao, Y., Yao, B., Jiang, P. (2021). Progress, challenges, and perspectives of bioleaching for recovering heavy metals from mine tailings. Adsorption Science & Technology: Interface Science for Advanced Materials & Technologies, 2021. https://doi.org/10.1155/2021/9941979
[77] Song, Z., Song, G., Tang, W. et al. (2021). Molybdenum contamination dispersion from mining site to a reservoir. Ecotoxicology and Environmental Safety, 208, 111631.
[78] Belle, G., Fossey, A., Esterhuizen, L., Moodley, R. (2021). Contamination of groundwater by potential harmful elements from gold mine tailings and the implications to human health: a case study in Welkom and Virginia, Free State Province, South Africa. Groundwater for Sustainable Development, 12, 100507.
[79] Li, S., Zhong, H., Hu, Y., Zhao, J., He, Z., Gu, G. (2014). Bioleaching of a low-grade nickel-copper sulfide by mixture of four thermophiles. Bioresource Technology, 153, 300-306. https://doi.org/10.1016/j.biortech.2013.12.018
[80] Nguyen, T. H., Won, S., Ha, M.-G., Nguyen, D. D., Kang, H. Y. (2021). Bioleaching for environmental remediation of toxic metals and metalloids: A review on soils, sediments, and mine tailings. Chemosphere, 282(131108), 131108. https://doi.org/10.1016/j.chemosphere.2021.131108
[81] Pathak, A., Morrison, L., Healy, M. G. (2017). Catalytic potential of selected metal ions for bioleaching, and potential techno-economic and environmental issues: A critical review. Bioresource Technology, 229, 211-221. https://doi.org/10.1016/j.biortech.2017.01.001
[82] Baniasadi, M., Vakilchap, F., Bahaloo-Horeh, N., Mousavi, S. M., Farnaud, S. (2019). Advances in bioleaching as a sustainable method for metal recovery from e-waste: A review. Journal of Industrial and Engineering Chemistry, 76, 75-90. https://doi.org/10.1016/j.jiec.2019.03.047
[83] Jianlan, S. (2018). Greener copper from low- grade ore - catalyzed by bacteria. Bulletin of the Chinese Academy of Sciences. BCAS Vol.32 No.3.
[84] Kinnunen, P., Hedrich, S. (2023). Biotechnological strategies to recover value from waste. Hydrometallurgy, 222(106182), 106182. https://doi.org/10.1016/j.hydromet.2023.106182
[85] Schippers, A., Hedrich, S., Vasters, J., Drobe, M., Sand, W., & Willscher, S. (2013). Biomining: Metal recovery from ores with microorganisms. En Advances in Biochemical Engineering/Biotechnology (pp. 1-47). Springer Berlin Heidelberg.
[86] Calvo, G., Palacios, J.-L., Valero, A. (2022). The influence of ore grade decline on energy consumption and GhG emissions: The case of gold. Environmental Development, 41(100683), 100683. https://doi.org/10.1016/j.envdev.2021.100683
[87] Thenepalli, T., Chilakala, R, Habte, L, Tuan L. Q., Kim, C. S., et al. (2019) A brief note on the heap leaching technologies for the recovery of valuable metals. Sustain 11: 1-10.
[88] Rendón-Castrillón, L., Ramírez-Carmona, M., Ocampo-López, C., Gómez-Arroyave, L. (2023). Bioleaching techniques for sustainable recovery of metals from solid matrices. Sustainability, 15(13), 10222. https://doi.org/10.3390/su151310222
[89] Spooren, J., Binnemans, K., Björkmalm, J., Breemersch, K., Dams, Y., Folens, K., González-Moya, M., Horckmans, L., Komnitsas, K., Kurylak, W., Lopez, M., Mäkinen, J., Onisei, S., Oorts, K., Peys, A., Pietek, G., Pontikes, Y., Snellings, R., Tripiana, M., … Kinnunen, P. (2020). Near-zero-waste processing of low-grade, complex primary ores and secondary raw materials in Europe: technology development trends. Resources, Conservation, and Recycling, 160(104919), 104919. https://doi.org/10.1016/j.resconrec.2020.104919
[90] Nkuna, R., Ijoma, G. N., Matambo, T. S., Chimwani, N. (2022). Accessing metals from low-grade ores and the environmental impact considerations: A review of the perspectives of conventional versus bioleaching strategies. Minerals (Basel, Switzerland), 12(5), 506. https://doi.org/10.3390/min12050506
[91] Vera, M., Schippers, A., Hedrich, S., Sand, W. (2022). Progress in bioleaching: fundamentals and mechanisms of microbial metal sulfide oxidation - part A. Applied Microbiology and Biotechnology, 106(21), 6933-6952. https://doi.org/10.1007/s00253-022-12168-7
[92] Andrzejewska-Górecka, D., Poniatowska, A., Macherzynski, B., Wojewódka, D., Wszelaka-Rylik, M. (2019). Comparison of the effectiveness of biological and chemical leaching of copper, nickel and zinc from circuit boards. In?ynieria Ekologiczna, 20(9), 62-69. https://doi.org/10.12911/22998993/112485
[93] Opara, C. B., Blannin, R., Ebert, D., Frenzel, M., Pollmann, K., Kutschke, S. (2022). Bioleaching of metal(loid)s from sulfidic mine tailings and waste rock from the Neves Corvo mine, Portugal, by an acidophilic consortium. Minerals Engineering, 188(107831), 107831. https://doi.org/10.1016/j.mineng.2022.107831
[94] Sana, S., Neelam, D., Gupta, V., Devki, D., Rahi, R. (2021). An overview: Application of microorganisms in bio-mining of metals (review article). International journal of pharmacy and biological sciences, 11(1), 01-08. https://doi.org/10.21276/ijpbs.2021.11.1.1
[95] Sajjad W., Zheng G., Din G., Ma X., Rafiq M., Xu W. (2019). Metals Extraction from Sulfide Ores with Microorganisms: The Bioleaching Technology and Recent Developments. Trans. Indian Institute Metals 72 559-579. 10.1007/S12666-018-1516-4
[96] Le, M. N., Lee, M. S. (2021). A review on hydrometallurgical processes for the recovery of valuable metals from spent catalysts and life cycle analysis perspective. Mineral Processing and Extractive Metallurgy Review, 42(5), 335-354. https://doi.org/10.1080/08827508.2020.1726914
[97] Ibrahim, A. H., Lyu, X., Atia, B. M., Gado, M. A., ElDeeb, A. B. (2022). Cost-effective and high purity valuable metals extraction from water leaching solid residues obtained as a by-product from processing the Egyptian boiler ash. Minerals (Basel, Switzerland), 12(9), 1084. https://doi.org/10.3390/min12091084
[98] Ma, X., Ge, P., Wang, L., Sun, W., Bu, Y., Sun, M., Yang, Y. (2023). The recycling of spent lithium-ion batteries: Crucial flotation for the separation of cathode and anode materials. Molecules (Basel, Switzerland), 28(10), 4081. https://doi.org/10.3390/molecules28104081
[99] Liu, Z.-W., Guo, X.-Y., Tian, Q.-H., Zhang, L. (2022). A systematic review of gold extraction: Fundamentals, advancements, and challenges toward alternative lixiviants. Journal of Hazardous Materials, 440(129778), 129778. https://doi.org/10.1016/j.jhazmat.2022.129778
[100] Rai, V., Liu, D., Xia, D., Jayaraman, Y., Gabriel, J.-C. P. (2021). Electrochemical approaches for the recovery of metals from electronic waste: A critical review. Recycling, 6(3), 53. https://doi.org/10.3390/recycling6030053
[101] Cesiulis, H., Tsyntsaru, N. (2023). Eco-friendly electrowinning for metals recovery from waste electrical and electronic equipment (WEEE). Coatings, 13(3), 574. https://doi.org/10.3390/coatings13030574
[102] Camacho, D., Frazao, R., Fouillen, A., Nanci, A., Lang, B. F., Apte, S. C., Baron, C., Warren, L. A. (2020). New insights into Acidithiobacillus thiooxidans sulfur metabolism through coupled gene expression, solution chemistry, microscopy, and spectroscopy analyses. Frontiers in microbiology, 11. https://doi.org/10.3389/fmicb.2020.00411
[103] Jones, S., Santini, J. M. (2023). Mechanisms of bioleaching: iron and sulfur oxidation by acidophilic microorganisms. Essays in Biochemistry, 67(4), 685-699. https://doi.org/10.1042/ebc20220257
[104] Chen, J., Liu, Y., Mahadevan, R. (2023). Genetic engineering of Acidithiobacillus ferridurans with CRISPR-Cas9/dCas9 systems. En bioRxiv. https://doi.org/10.1101/2022.03.14.484339
[105] Aromaa, J., Makinen, J., Vepsalainen, H., Kaartinen, T., Wahlstrom, M., Forsen, O. (2013). Comparison of chemical and biological leaching of sulfide tailings. https://doi.org/10.5277/ppmp130220
[106] De Souza, A. D., Pina, P. S., Leão, V. A. (2007). Bioleaching and chemical leaching as an integrated process in the zinc industry. Minerals Engineering, 20(6), 591-599. https://doi.org/10.1016/j.mineng.2006.12.014
[107] Mishra, S., Panda, S., Akcil, A., Dembele, S., Agcasulu, I. (2021). A review on chemical versus microbial leaching of electronic wastes with emphasis on base metals dissolution. Minerals (Basel, Switzerland), 11(11), 1255. https://doi.org/10.3390/min11111255
[108] Stankovic, S., Schippers, A. (2023). Bioleaching and chemical leaching of lateritic ore in percolators. Metallurgical and Materials Data, 1(2), 45-49. https://doi.org/10.30544/mmd9
[109] Castro, L., Blázquez, M. L., Muñoz, J. Á. (2021). Leaching/bioleaching and recovery of metals. Metals, 11(11), 1732. https://doi.org/10.3390/met11111732
[110] Sikander, A., Kelly, S., Kuchta, K., Sievers, A., Willner, T., Hursthouse, A. S. (2022). Chemical and microbial leaching of valuable metals from PCBs and tantalum capacitors of spent mobile phones. International Journal of Environmental Research and Public Health, 19(16), 10006. https://doi.org/10.3390/ijerph191610006
[111] Nguyen, V. K., Lee, J.-U. (2015). A comparison of microbial leaching and chemical leaching of arsenic and heavy metals from mine tailings. Biotechnology and Bioprocess Engineering: BBE, 20(1), 91-99. https://doi.org/10.1007/s12257-014-0223-1
[112] Choi, N.S.; Cho, K.S.; Kim, D.S.; Kim, D.J. (2004) Microbial recovery of copper from printed circuit boards of waste computer by Acidithiobacillus ferrooxidans. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng, 39, 2973-2982
[113] Pourhossein, F.; Rezaei, O.; Mousavi, S.M.; Beolchini, F. (2021). Bioleaching of critical metals from waste OLED touch screens using adapted acidophilic bacteria. J. Environ. Health Sci. Eng, 19, 893-906.
[114] Velgosová, O.; Kaduková, J.; Marcinc?áková, R. (2012). Study of Ni and Cd bioleaching from spent Ni-Cd batteries. Nova Biotechnol. Chim, 11, 117-123
[115] Arshadi, M.  Mousavi, S.M. (2015). Multi-objective optimization of heavy metals bioleaching from discarded mobile phone PCBs: Simultaneous Cu and Ni recovery using Acidithiobacillus ferrooxidans. Sep. Purif. Technol., 147, 210-219.
[116] Mishra, D.; Kim, D.J.; Ralph, D.; Ahn, J.G.; Rhee, Y.H. (2008). Bioleaching of metals from spent lithium ion secondary batteries using Acidithiobacillus ferrooxidans. Waste Manag, 28, 333-338
[117] Kadivar, S.; Pourhossein, F.; Mousavi, S.M. Recovery of valuable metals from spent mobile phone printed circuit boards using biochar in indirect bioleaching. J. Environ. Manag. 2021, 280, 111642.
[118] Natarajan, G.; Ting, Y.-P. (2014). Pretreatment of e-waste and mutation of alkali-tolerant cyanogenic bacteria promote gold biorecovery. Bioresour. Technol., 152, 80-85
[119] Kim, S. D., Bae, J. E., Park, H. S., Cha, D. K. (2005). Bioleaching of cadmium and nickel from synthetic sediments by Acidithiobacillus ferrooxidans. Environmental Geochemistry and Health, 27(3), 229-235. https://doi.org/10.1007/s10653-004-3479-0
[120] Coto, O., Galizia, F., Hernández, I., Marrero, J., Donati, E. (2008). Cobalt and nickel recoveries from laterite tailings by organic and inorganic bio-acids. Hydrometallurgy, 94(1-4), 18-22. https://doi.org/10.1016/j.hydromet.2008.05.017
[121] Nancucheo, I., Grail, B. M., Hilario, F., du Plessis, C., Johnson, D. B. (2014). Extraction of copper from an oxidized (lateritic) ore using bacterially catalysed reductive dissolution. Applied Microbiology and Biotechnology. https://doi.org/10.1007/s00253-014-5687-6
[122] Netpae, T., Suckley, S. (2020). Comparación de tres medios de cultura para biologación en un solo paso y dos pasos de níquel y cadmio de las baterías de Ni-Cd gastadas por Aspergillus niger. Avances en Tecnología Ambiental, 6 (3, 167-172. doi: 10.22104/aet.2021.4759.1286
[123] Chaturvedi, K., Singhwane, A., Dhangar, M., Raghuwanshi, S., Tak, D., Srivastava, A. K., Verma, S. (2024). State-of-the-art review on the Potentiality of Microorganisms for extracting metals from E-Waste i.e, PCBs of Mobile phones and Computers. Environmental Technology Reviews, 13(1), 186–213. https://doi.org/10.1080/21622515.2023.2290601
[124] Bauermeister, A., Rettberg, P., Flemming, H.-C. (2014). Growth of the acidophilic iron-sulfur bacterium Acidithiobacillus ferrooxidans under Mars-like geochemical conditions. Planetary and Space Science, 98, 205-215. https://doi.org/10.1016/j.pss.2013.09.009
[125] Sriaporn, C., Campbell, K. A., Van Kranendonk, M. J., Handley, K. M. (2021). Genomic adaptations enabling Acidithiobacillus distribution across wide-ranging hot spring temperatures and pHs. Microbiome, 9(1). https://doi.org/10.1186/s40168-021-01090-1
[126] Santaolalla, A., Gutierrez, J., Gallastegui, G., Barona, A., Rojo, N. (2021). Immobilization of Acidithiobacillus ferrooxidans in bacterial cellulose for a more sustainable bioleaching process. Journal of Environmental Chemical Engineering, 9(4), 105283. https://doi.org/10.1016/j.jece.2021.105283
[127] Watling, H. (2014). Review of biohydrometallurgical metals extraction from polymetallic mineral resources. Minerals (Basel, Switzerland)5(1), 1–60. https://doi.org/10.3390/min5010001
[128]. Wang, H., Ju, L.-K., Castaneda, H., Cheng, G., Newby, B.-M. Z. (2015). Corrosion behaviors of carbon steel and stainless steel in the presence of iron oxidizing bacteria Acidithiobacillus ferrooxidansCORROSION 2015, 1–15.
[129] Nordstrom, D. K., Blowes, D. W., Ptacek, C. J. (2015). Hydrogeochemistry and microbiology of mine drainage: An update. Applied Geochemistry: Journal of the International Association of Geochemistry and Cosmochemistry57, 3–16. https://doi.org/10.1016/j.apgeochem.2015.02.008
[130] Kaksonen, AH., Deng, X., Bohu, T., Zea, L., Khaleque, HN, Gumulya, Y., Boxall, Nueva Jersey, Morris, C. y Cheng, KY (2020). Direcciones prospectivas para la biohidrometalurgia. Hidrometalurgia195 (105376), 105376. https://doi.org/10.1016/j.hidromet.2020.105376
[131] Gumulya, Y., Boxall, N. J., Khaleque, H. N., Santala, V., Carlson, R. P., Kaksonen, A. H. (2018). In a quest for engineering acidophiles for biomining applications: challenges and opportunities. Genes9(2), 116. https://doi.org/10.3390/genes9020116
[132] Newsome, L., Falagán, C. (2021). The microbiology of metal mine waste: Bioremediation applications and implications for planetary health. GeoHealth, 5(10). https://doi.org/10.1029/2020gh000380
[133] Puyol, D., Batstone, D. J., Hülsen, T., Astals, S., Peces, M., Krömer, J. O. (2017). Resource recovery from wastewater by biological technologies: Opportunities, challenges, and prospects. Frontiers in microbiology, 7. https://doi.org/10.3389/fmicb.2016.02106
[134] Kelly, D.P., Wood, A.P. (2014). The Family Acidithiobacillaceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-38922-1_250