Bacterial roles, genomic features, and their regulation in the cleaner recovery of low-grade chalcopyrite bioleaching: A critical review and future prospects

Abstract

Fluidized bioleaching is an efficient, environmentally friendly, and cost-effective mining method that has been widely explored and utilized for recovering low-grade copper sulfide minerals, such as chalcopyrite. However, the proliferation and apoptosis of dominant leaching bacteria, such as Acidithiobacillus ferrooxidans, within complex pore, void, and fracture structures in deep-earth environments commonly results in a dynamic bacterial community that evolves continuously. This unclear genetic-scale microbial succession often leads to low leaching reaction efficiency, undesirable reaction passivation, and poor bioleaching operations. This review integrates genetic-scale insights with industrial challenges in chalcopyrite bioleaching, proposing novel strategies for regulating microbial communities. A systematic analysis of five critical dimensions is conducted, focusing on: 1) The adaptations of Acidithiobacillus spp. to high Ag⁺ stress. 2) The direct, indirect, and cooperative bioleaching pathways are linked to bacterial extracellular polymer substance (EPS) and Fe/S oxidation genes. 3) The passivation dynamics governed by bacterial genomics, including thiosulfate, polysulfide, and biofilm mechanisms. 4) The microbial succession patterns under genetic control Hi-C sequencing-guided consortia design. 5) Molecular detection methods (16S rDNA, Hi-C) for optimizing leaching efficiency. The following innovations have been identified as being of key significance: A genomic-environmental interaction model has been developed to bridge the gap between bacterial genetics and passivation dynamics. A comprehensive analysis of Ag⁺ catalysis has been conducted, resulting in a 40% reduction in jarosite formation through jar gene suppression. Practical strategies, such as thermophilic consortia engineering, have been validated in pilot trials, achieving a 32% increase in copper recovery. Additionally, this study meticulously reviews and summarizes typical potential stimulations and enhanced bioleaching methods. The genetic sequencing methods, such as 16S rDNA and Hi-C, have been shown to hold promising potential for improving bioleaching reactions and delaying the formation of passivation substances like jarosite.

Keywords

Copper sulfide / Chalcopyrite / Bioleaching mechanism / Bacterial succession / Genetic detection

References

[1] K.R. Roy, J.D. Smith, S.C. Vonesch, G. Lin, C.S. Tu, A.R. Lederer, A. Chu, S. Suresh, M. Nguyen, J. Horecka, A. Tripathi, W.T. Burnett, M.A. Morgan, J. Schulz, K.M. Orsley, W. Wei, R.S. Aiyar, R.W. Davis, V.A. Bankaitis, J.E. Haber, M.L. Salit, R.P. St Onge, L.M. Steinmetz, Multiplexed precision genome editing with trackable genomic barcodes in yeast, Nat. Biotechnol. 36 (6) (2018) 512-520.

[2] D.B. Johnson, Biomining-biotechnologies for extracting and recovering metals from ores and waste materials, Curr. Opin. Biotechnol. 30 (2014) 24-31.

[3] X.C. Liu, K. Zhao, X.Y. Miao, H.L. Zhan, Characterization and evaluation of oil shale based on terahertz spectroscopy: a review, Energy Rev. 2 (4) (2023) 100041.

[4] J.X. Tang, H.H. Yang, H.J. Chen, F.Q. Li, C.Y. Wang, Q.P. Liu, Q. Zhang, R.K. Zhang, L.R. Yu, Potential and future direction for copper resource exploration in China, Green Smart Min. Eng. 1 (2) (2024) 127-131.

[5] Y.M. Wang, Q.S. Chen, B.B. Dai, D.L. Wang, Guidance and review: advancing mining technology for enhanced production and supply of strategic minerals in China, Green Smart Min. Eng. 1 (1) (2024) 2-11.

[6] S.H. Yin, L.M. Wang, A.X. Wu, E. Kabwe, X. Chen, R.F. Yan, Copper recycle from sulfide tailings using combined leaching of ammonia solution and alkaline bacteria, J. Clean. Prod. 189 (2018) 746-753.

[7] M. Onifade, T. Zvarivadza, J.A. Adebisi, K.O. Said, O. Dayo-Olupona, A.I. Lawal, M. Khandelwal, Advancing toward sustainability: the emergence of Green mining technologies and practices, Green Smart Min. Eng. 1 (2) (2024) 157-174.

[8] T. Rohwerder, T. Gehrke, K. Kinzler, W. Sand, Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation, Appl. Microbiol. Biotechnol. 63 (3) (2003) 239-248.

[9] J.G. Wang, H.P. Xie, C. Leung, X.Z. Li, New understandings on initiation and evolution of disasters in deep underground, Deep Undergr. Sci. Eng. 2 (3) (2023) 205-206.

[10] H.P. Xie, C. Leung, J.G. Wang, X.Z. Li, Advancing deep underground research through integration of engineering and science, Deep Undergr. Sci. Eng. 1 (1) (2022) 1-2.

[11] Y. He, Y.F. Cui, Z.X. Zhao, Y.T. Chen, W.X. Shang, P. Tan, Strategies for bubble removal in electrochemical systems, Energy Rev. 2 (1) (2023) 100015.

[12] Q.W. Guo, J.Q. Geng, J.W. Pan, L. Zou, Y.F. Tian, B. Chi, J. Pu, Brief review of hydrocarbon-reforming catalysts map for hydrogen production, Energy Rev. 2 (3) (2023) 100037.

[13] I.C. Moia, A. Kanaropoulou, D.F. Ghanotakis, P. Carlozzi, E. Touloupakis, Photofermentative hydrogen production by immobilized Rhodopseudomonas sp. S16-VOGS3 cells in photobioreactors , Energy Rev. 3 (1) (2024) 100055.

[14] H.R. Watling, Chalcopyrite hydrometallurgy at atmospheric pressure: 1. Review of acidic sulfate, sulfate-chloride and sulfate-nitrate process options, Hydrometallurgy 140 (2013) 163-180.

[15] D. Dreisinger, Copper leaching from primary sulfides: options for biological and chemical extraction of copper, Hydrometallurgy 83 (1-4) (2006) 10-20.

[16] R.A. Bobadilla-Fazzini, A. Pérez, V. Gautier, H. Jordan, P. Parada, Primary copper sulfides bioleaching vs. chloride leaching: advantages and drawbacks, Hydrometallurgy 168 (2017) 26-31.

[17] M.L. Free, Hydrometallurgy: fundamentals and applications, John Wiley & Sons, Inc., Hoboken, New Jersey, 2013.

[18] L.M. Wang, S.H. Yin, B.N. Deng, A.X. Wu, Copper sulfides leaching assisted by acidic seawater-based media: ionic strength and mechanism, Miner. Eng. 175 (2022) 107286.

[19] S.H. Yin, W. Chen, X. Chen, L.M. Wang, Bacterial-mediated recovery of copper from low-grade copper sulphide using acid-processed rice straw, Bioresour. Technol. 288 (2019) 121605.

[20] S.H. Yin, L.M. Wang, A.X. Wu, X. Chen, R.F. Yan, Research progress in enhanced bioleaching of copper sulfides under the intervention of microbial communities, Int. J. Miner. Metall. Mater. 26 (11) (2019) 1337-1350.

[21] D.B. Johnson, The evolution, current status, and future prospects of using biotechnologies in the mineral extraction and metal recovery sectors, Minerals 8 (8) (2018) 343.

[22] A.R. Colmer, K.L. Temple, M.E. Hinkle, An iron-oxidizing bacterium from the acid drainage of some bituminous coal mines, J. Bacteriol. 59 (3) (1950) 317-328.

[23] C.L. Brierley, Bacterial succession in bioheap leaching, in: R. Amils, A. Ballester (Eds.), Process Metallurgy, Vol. 9, Elsevier, 1999, pp. 91-97.

[24] L.M. Wang, S.H. Yin, A.X. Wu, W. Chen, Synergetic bioleaching of copper sulfides using mixed microorganisms and its community structure succession, J. Clean. Prod. 245 (2020) 118689.

[25] L.M. Wang, L. Cheng, S.H. Yin, Z.P. Yan, X.L. Zhang, Multiphase slurry flow regimes and its pipeline transportation of underground backfill in metal mine: mini review, Constr. Build. Mater. 402 (2023) 133014.

[26] L.M. Wang, L. Cheng, S.H. Yin, P.Z. Liu, Copper sulfides agglomeration using a novel lab-scale granulator: integrated evaluation of bonding, leaching and mechanical behavior, Case Stud. Constr. Mater. 20 (2024) e02705.

[27] M. Vera, A. Schippers, W. Sand, Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation: part A, Appl. Microbiol. Biotechnol. 97 (17) (2013) 7529-7541.

[28] A. Mahmoud, P. Cézac, A.F.A. Hoadley, F. Contamine, P. D’Hugues, A review of sulfide minerals microbially assisted leaching in stirred tank reactors, Int. Biodeterior. Biodegrad. 119 (2017) 118-146.

[29] A.H. Kaksonen, N.J. Boxall, Y. Gumulya, H.N. Khaleque, C. Morris, T. Bohu, K.Y. Cheng, K.M. Usher, A.M. Lakaniemi, Recent progress in biohydrometallurgy and microbial characterisation, Hydrometallurgy 180 (2018) 7-25.

[30] A. Orell, C.A. Navarro, R. Arancibia, J.C. Mobarec, C.A. Jerez, Life in blue: copper resistance mechanisms of bacteria and archaea used in industrial biomining of minerals, Biotechnol. Adv. 28 (6) (2010) 839-848.

[31] D.B. Johnson, F.F. Roberto, Heterotrophic acidophiles and their roles in the bioleaching of sulfide minerals, Biomining, Springer Berlin, Heidelberg, 1997, pp. 259-279.

[32] C.A. Jerez, Biomining of metals: how to access and exploit natural resource sustainably, Microb. Biotechnol. 10 (5) (2017) 1191-1193.

[33] A. Schippers, F. Glombitza, W. Sand, Geobiotechnology I Metal-related issues, Springer Berlin, Heidelberg, 2014.

[34] S. Panda, A. Akcil, N. Pradhan, H. Deveci, Current scenario of chalcopyrite bioleaching: a review on the recent advances to its heap-leach technology, Bioresour. Technol. 196 (2015) 694-706.

[35] A. Schippers, W. Sand, Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur, Appl. Environ. Microbiol. 65 (1) (1999) 319-321.

[36] W. Zhu, J.L. Xia, Y. Yang, Z.Y. Nie, L. Zheng, C.Y. Ma, R.Y. Zhang, A.N. Peng, L. Tang, G.Z. Qiu, Sulfur oxidation activities of pure and mixed thermophiles and sulfur speciation in bioleaching of chalcopyrite, Bioresour. Technol. 102 (4) (2011) 3877-3882.

[37] H.C. Liu, Z.Y. Nie, J.L. Xia, H.R. Zhu, Y. Yang, C.H. Zhao, L. Zheng, Y.D. Zhao, Investigation of copper, iron and sulfur speciation during bioleaching of chalcopyrite by moderate thermophile Sulfobacillus thermosulfidooxidans , Int. J. Miner. Process. 137 (2015) 1-8.

[38] D.E. Rawlings, H. Tributsch, G.S. Hansford, Reasons why ‘Leptospirillum’-like species rather than Thiobacillus ferrooxidans are the dominant iron-oxidizing bacteria in many commercial processes for the biooxidation of pyrite and related ores , Microbiology 145 (Pt 1) (1999) 5-13.

[39] D.E. Rawlings, S. Silver, Mining with microbes, Bio/Technology 13 (8) (1995) 773-778.

[40] R.P. Hackl, The Leaching and Passivation of Chalcopyrite in Acid Sulfate Media (Dissertation), University of British Columbia, Vancouver, Canada, 1995.

[41] R.Y. Zhang, T.R. Neu, V. Blanchard, M. Vera, W. Sand, Biofilm dynamics and EPS production of a thermoacidophilic bioleaching archaeon, New Biotechnol. 51 (2019) 21-30.

[42] J. Wang, X.W. Gan, H.B. Zhao, M.H. Hu, K.Y. Li, W.Q. Qin, G.Z. Qiu, Dissolution and passivation mechanisms of chalcopyrite during bioleaching: DFT calculation, XPS and electrochemistry analysis, Miner. Eng. 98 (2016) 264-278.

[43] T. Moyo, J. Petersen, M.J. Nicol, The electrochemistry and kinetics of the oxidative dissolution of chalcopyrite in ammoniacal solutions. Part II-Cathodic reactions, Hydrometallurgy 184 (2019) 67-74.

[44] A.F. Tshilombo, Mechanism and Kinetics of Chalcopyrite Passivation and Depassivation During Ferric and Microbial Leaching (Dissertation), University of British Columbia, Vancouver, Canada, 2006.

[45] Z.H. Ren, C. Chao, P. Krishnamoorthy, C. Heise, K. Sabzehei, E. Asselin, D.G. Dixon, N. Mora, New perspective on the depassivation mechanism of chalcopyrite by ethylene thiourea, Miner. Eng. 204 (2023) 108358.

[46] H.B. Zhao, Y.S. Zhang, X. Zhang, L. Qian, M.L. Sun, Y. Yang, Y.S. Zhang, J. Wang, H. Kim, G.Z. Qiu, The dissolution and passivation mechanism of chalcopyrite in bioleaching: an overview, Miner. Eng. 136 (2019) 140-154.

[47] M. Kartal, F. Xia, D. Ralph, W.D.A. Rickard, F. Renard, W. Li, Enhancing chalcopyrite leaching by tetrachloroethylene-assisted removal of sulphur passivation and the mechanism of jarosite formation, Hydrometallurgy 191 (2020) 105192.

[48] W.M. Zeng, Y.P. Peng, T.J. Peng, M.H. Nan, M. Chen, G.Z. Qiu, L. Shen, Electrochemical studies on dissolution and passivation behavior of low temperature bioleaching of chalcopyrite by Acidithiobacillus ferrivorans YL15 , Miner. Eng. 155 (2020) 106416.

[49] L. Ahonen, O.H. Tuovinen, Catalytic effects of silver in the microbiological leaching of finely ground chalcopyrite-containing ore materials in shake flasks, Hydrometallurgy 24 (2) (1990) 219-236.

[50] N. Pradhan, K.C. Nathsarma, K. Srinivasa Rao, L.B. Sukla, B.K. Mishra, Heap bioleaching of chalcopyrite: a review, Miner. Eng. 21 (5) (2008) 355-365.

[51] H.B. Zhao, J. Wang, X.W. Gan, M.H. Hu, L. Tao, W.Q. Qin, G.Z. Qiu, Role of pyrite in sulfuric acid leaching of chalcopyrite: an elimination of polysulfide by controlling redox potential, Hydrometallurgy 164 (2016) 159-165.

[52] H.B. Zhao, Y.S. Zhang, M.L. Sun, P.F. Ou, Y.J. Zhang, R. Liao, G.Z. Qiu, Catalytic mechanism of silver in the oxidative dissolution process of chalcopyrite: experiment and DFT calculation, Hydrometallurgy 187 (2019) 18-29.

[53] A. Ghahremaninezhad, E. Asselin, D.G. Dixon, Electrochemical evaluation of the surface of chalcopyrite during dissolution in sulfuric acid solution, Electrochim. Acta 55 (18) (2010) 5041-5056.

[54] R.L. Yu, Y. Ou, J.X. Tan, F.D. Wu, J. Sun, L. Miao, D.L. Zhong, Effect of EPS on adhesion of Acidithiobacillus ferrooxidans on chalcopyrite and pyrite mineral surfaces , Trans. Nonferrous Met. Soc. China 21 (2) (2011) 407-412.

[55] W. Sand, T. Gehrke, Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria, Res. Microbiol. 157 (1) (2006) 49-56.

[56] A.D. Agate, M.S. Korczynski, D.G. Lundgren, Extracellular complex from the culture filtrate of Ferrobacillus ferrooxidans , Can. J. Microbiol. 15 (3) (1969) 259-264.

[57] X.Q. Zhao, R.C. Wang, X.C. Lu, J.J. Lu, C.X. Li, J. Li, Bioleaching of chalcopyrite by Acidithiobacillus ferrooxidans , Miner. Eng. 53 (2013) 184-192.

[58] S. Panda, P.K. Parhi, B.D. Nayak, N. Pradhan, U.B. Mohapatra, L.B. Sukla, Two step meso-acidophilic bioleaching of chalcopyrite containing ball mill spillage and removal of the surface passivation layer, Bioresour. Technol. 130 (2013) 332-338.

[59] J.J. Eksteen, E.A. Oraby, B.C. Tanda, A conceptual process for copper extraction from chalcopyrite in alkaline glycinate solutions, Miner. Eng. 108 (2017) 53-66.

[60] W.M. Zeng, Z.R. Liu, C. Amanze, J.J. Cheng, W.Q. Liao, X.L. Wu, G.Z. Qiu, Q.K. Wang, Z.L. Wu, L.C. Zou, L. Shen, In situ detection of Cu²⁺, Fe³⁺ and Fe²⁺ ions at the microbe-mineral interface during bioleaching of chalcopyrite by moderate thermophiles , Miner. Eng. 191 (2023) 107936.

[61] W.M. Zeng, S. Tan, M. Chen, G.Z. Qiu, Detection and analysis of attached microorganisms on the mineral surface during bioleaching of pure chalcopyrite with moderate thermophiles, Hydrometallurgy 106 (1-2) (2011) 46-50.

[62] R.L. Yu, L.J. Shi, G.H. Gu, D. Zhou, L. You, M. Chen, G.Z. Qiu, W.M. Zeng, The shift of microbial community under the adjustment of initial and processing pH during bioleaching of chalcopyrite concentrate by moderate thermophiles, Bioresour. Technol. 162 (2014) 300-307.

[63] Q. Li, W. Sand, Mechanical and chemical studies on EPS from Sulfobacillus thermosulfidooxidans: from planktonic to biofilm cells , Colloids Surf. B Biointerfaces 153 (2017) 34-40.

[64] L. Jiang, H.Y. Zhou, X.T. Peng, Z.H. Ding, The use of microscopy techniques to analyze microbial biofilm of the bio-oxidized chalcopyrite surface, Miner. Eng. 22 (1) (2009) 37-42.

[65] S. Mishra, S. Panda, N. Pradhan, S.K. Biswal, L.B. Sukla, B.K. Mishra, Microbe-mineral interactions: exploring avenues towards development of a sustainable microbial technology for coal beneficiation, in: L. Sukla, N. Pradhan, S. Panda, B. Mishra (Eds.), Environmental Microbial Biotechnology. Soil Biology, Vol. 45, Springer, Cham, 2015, pp. 33-52.

[66] S. Saxena, Applied Microbiology, Springer, New Delhi, India, 2015.

[67] C.L. Brierley, Microbiological mining, Sci. Am. 247 (2) (1982) 44-53.

[68] D.W. Shiers, D.M. Collinson, N.J. Kelly, H.R. Watling, Copper extraction from chalcopyrite: comparison of three non-sulfate oxidants, hypochlorous acid, sodium chlorate and potassium nitrate, with ferric sulfate, Miner. Eng. 85 (2016) 55-65.

[69] H.R. Watling, D.W. Shiers, J. Li, N.M. Chapman, G.B. Douglas, Effect of water quality on the leaching of a low-grade copper sulfide ore, Miner. Eng. 58 (2014) 39-51.

[70] M.O. Schrenk, K.J. Edwards, R.M. Goodman, R.J. Hamers, J.F. Banfield, Distribution of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans: implications for generation of acid mine drainage , Science 279 (5356) (1998) 1519-1522.

[71] G.J. Olson, J.A. Brierley, C.L. Brierley, Bioleaching review part B: progress in bioleaching: applications of microbial processes by the minerals industries, Appl. Microbiol. Biotechnol. 63 (3) (2003) 249-257.

[72] C.A. du Plessis, J.D. Batty, D.W. Dew, Commercial applications of thermophile bioleaching, in: D.E. Rawlings, D.B. Johnson (Eds.), Biomining, Springer Berlin, Heidelberg, 2007, pp. 57-80.

[73] F.F. Roberto, A. Schippers, Progress in bioleaching: part B: applications of microbial processes by the minerals industries, Appl. Microbiol Biotechnol. 106 (18) (2022) 5913-5928.

[74] S.H. Yin, L.M. Wang, X. Chen, A.X. Wu, Agglomeration and leaching behaviors of copper oxides with different chemical binders, Int. J. Miner. Metall. Mater. 28 (7) (2021) 1127-1134.

[75] L.M. Wang, S.H. Yin, A.X. Wu, W. Chen, Effect of stratified stacks on extraction and surface morphology of copper sulfides, Hydrometallurgy 191 (2020) 105226.

[76] S.H. Yin, L.M. Wang, X. Chen, A.X. Wu, Effect of ore size and heap porosity on capillary process inside leaching heap, Trans. Nonferrous Met. Soc. China 26 (3) (2016) 835-841.

[77] L.X. Chen, L.N. Huang, C. Méndez-García, J.L. Kuang, Z.S. Hua, J. Liu, W.S. Shu, Microbial communities, processes and functions in acid mine drainage ecosystems, Curr. Opin. Biotechnol. 38 (2016) 150-158.

[78] H.L. Yang, S.S. Feng, Y. Xin, W. Wang, Community dynamics of attached and free cells and the effects of attached cells on chalcopyrite bioleaching by Acidithiobacillus sp , Bioresour. Technol. 154 (2014) 185-191.

[79] N. Noël, B. Florian, W. Sand, AFM & EFM study on attachment of acidophilic leaching organisms, Hydrometallurgy 104 (3-4) (2010) 370-375.

[80] W. Zhu, J.L. Xia, Y. Yang, Z.Y. Nie, A.N. Peng, H.C. Liu, G.Z. Qiu, Thermophilic archaeal community succession and function change associated with the leaching rate in bioleaching of chalcopyrite, Bioresour. Technol. 133 (2013) 405-413.

[81] W.M. Zeng, G.Z. Qiu, H.B. Zhou, J.H. Peng, M. Chen, S.N. Tan, W.L. Chao, X.D. Liu, Y.S. Zhang, Community structure and dynamics of the free and attached microorganisms during moderately thermophilic bioleaching of chalcopyrite concentrate, Bioresour. Technol. 101 (18) (2010) 7068-7075.

[82] C.X. Zhao, B.J. Yang, R. Liao, M.X. Hong, S.C. Yu, J. Wang, G.Z. Qiu, Catalytic mechanism of manganese ions and visible light on chalcopyrite bioleaching in the presence of Acidithiobacillus ferrooxidans , Chin. J. Chem. Eng. 41 (2022) 457-465.

[83] Z.H. Wang, X.H. Xie, J.S. Liu, Experimental measurements of short-term adsorption of Acidithiobacillus ferrooxidans onto chalcopyrite , Trans. Nonferrous Met. Soc. China 22 (2) (2012) 442-446.

[84] B.J. Yang, C.X. Zhao, W. Luo, R. Liao, M. Gan, J. Wang, X.D. Liu, G.Z. Qiu, Catalytic effect of silver on copper release from chalcopyrite mediated by Acidithiobacillus ferrooxidans , J. Hazard. Mater. 392 (2020) 122290.

[85] S. Panda, A. Biswal, S. Mishra, P.K. Panda, N. Pradhan, U. Mohapatra, L.B. Sukla, B.K. Mishra, A. Akcil, Reductive dissolution by waste newspaper for enhanced meso-acidophilic bioleaching of copper from low grade chalcopyrite: a new concept of biohydrometallurgy, Hydrometallurgy 153 (2015) 98-105.

[86] L.Y. Ma, X.J. Wang, X. Feng, Y.L. Liang, Y.H. Xiao, X.D. Hao, H.Q. Yin, H.W. Liu, X.D. Liu, Co-culture microorganisms with different initial proportions reveal the mechanism of chalcopyrite bioleaching coupling with microbial community succession, Bioresour. Technol. 223 (2017) 121-130.

[87] A. Levett, S.A. Gleeson, J. Kallmeyer, From exploration to remediation: a microbial perspective for innovation in mining, Earth Sci. Rev. 216 (2021) 103563.

[88] B. Ghorbani, A. Arulrajah, G. Narsilio, S. Horpibulsuk, M.W. Bo, Development of genetic-based models for predicting the resilient modulus of cohesive pavement subgrade soils, Soils Found. 60 (2) (2020) 398-412.

[89] R. Liao, B.J. Yang, X.T. Huang, M.X. Hong, S.C. Yu, S.T. Liu, J. Wang, G.Z. Qiu, Combined effect of silver ion and pyrite on AMD formation generated by chalcopyrite bio-dissolution, Chemosphere 279 (2021) 130516.

[90] S.Z. Li, H. Zhong, Y.H. Hu, Z.G. He, F.L. Gao, G.H. Gu, Microbial community shifts during the process of marmatite bioleaching, Hydrometallurgy 149 (2014) 127-131.

[91] L.A. Mutch, H.R. Watling, E.L.J. Watkin, Microbial population dynamics of inoculated low-grade chalcopyrite bioleaching columns, Hydrometallurgy 104 (3-4) (2010) 391-398.

[92] L.X. Xia, L. Tang, J.L. Xia, C. Yin, L.Y. Cai, X.J. Zhao, Z.Y. Nie, J.S. Liu, G.Z. Qiu, Relationships among bioleaching performance, additional elemental sulfur, microbial population dynamics and its energy metabolism in bioleaching of chalcopyrite, Trans. Nonferrous Met. Soc. China 22 (1) (2012) 192-198.

[93] J.M. Tao, X.D. Liu, X.Y. Luo, T.K. Teng, C.Y. Jiang, L. Drewniak, Z.D. Yang, H.Q. Yin, An integrated insight into bioleaching performance of chalcopyrite mediated by microbial factors: functional types and biodiversity, Bioresour. Technol. 319 (2021) 124219.

[94] W.Y. Liu, C.J. Moran, S. Vink, Impact of chalcopyrite depression by water-borne bacteria in pure and combined mineral systems, Int. J. Miner. Process. 123 (2013) 18-24.

[95] Z.G. He, Z. Yin, X. Wang, H. Zhong, W. Sun, Microbial community changes during the process of pyrite bioleaching, Hydrometallurgy 125 (2012) 81-89.

[96] S.S. Feng, H.L. Yang, W. Wang, Microbial community succession mechanism coupling with adaptive evolution of adsorption performance in chalcopyrite bioleaching, Bioresour. Technol. 191 (2015) 37-44.

[97] X.Y. Liu, B.W. Chen, J.H. Chen, M.J. Zhang, J.K. Wen, D.Z. Wang, R.M. Ruan, Spatial variation of microbial community structure in the zijinshan commercial copper heap bioleaching plant, Miner. Eng. 94 (2016) 76-82.

[98] S.S. Feng, H.L. Yang, W. Wang, Improved chalcopyrite bioleaching by Acidithiobacillus sp. via direct step-wise regulation of microbial community structure , Bioresour. Technol. 192 (2015) 75-82.

[99] L.M. Wang, X.Q. Zhang, S.H. Yin, X.L. Zhang, P.Z. Liu, I.M.S.K. Ilankoon, Three-dimensional characterisation of pore networks and fluid flow in segregated heaps in the presence of crushed ore and agglomerates, Hydrometallurgy 219 (2023) 106082.

[100] M.M. Ramsey, A.K. Korgaonkar, M. Whiteley, Quorum-sensing in bacteria, in: M. Schaechter (Ed.), Encyclopedia of Microbiology, 3rd Ed., Elsevier, 2009, pp. 357-374.

[101] N. Chabert, V. Bonnefoy, W. Achouak, Quorum sensing improves current output with Acidithiobacillus ferrooxidans , Microb. Biotechnol. 11 (1) (2018) 136-140.

[102] A. González, S. Bellenberg, S. Mamani, L. Ruiz, A. Echeverría, L. Soulère, A. Doutheau, C. Demergasso, W. Sand, Y. Queneau, M. Vera, N. Guiliani, AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans , Appl. Microbiol. Biotechnol. 97 (8) (2013) 3729-3737.

[103] H. Jung, Y. Inaba, A.C. West, S. Banta, Overexpression of quorum sensing genes in Acidithiobacillus ferrooxidans enhances cell attachment and covellite bioleaching , Biotechnol. Rep. 38 (2023) e00789.

[104] L.L. Liu, X.Y. Zeng, J. Zheng, Y.M. Zou, S.Y. Qiu, Y.F. Dai, AHL-mediated quorum sensing to regulate bacterial substance and energy metabolism: a review, Microbiol. Res. 262 (2022) 127102.

[105] H.Q. Yin, L.H. Cao, G.Z. Qiu, D.Z. Wang, L. Kellogg, J.Z. Zhou, X.X. Liu, Z.M. Dai, J.N. Ding, X.D. Liu, Molecular diversity of 16S rRNA and gyrB genes in copper mines, Arch. Microbiol. 189 (2) (2008) 101-110.

[106] N.J. Boxall, S.M. Rea, J. Li, C. Morris, A.H. Kaksonen, Effect of high sulfate concentrations on chalcopyrite bioleaching and molecular characterisation of the bioleaching microbial community, Hydrometallurgy 168 (2017) 32-39.

[107] A. Bakhti, H. Moghimi, A. Bozorg, S. Stankovic, Z. Manafi, A. Schippers, Comparison of bioleaching of a sulfidic copper ore (chalcopyrite) in column percolators and in stirred-tank bioreactors including microbial community analysis, Chemosphere 349 (2024) 140945.

[108] X.M. Zhang, S.H. Zhang, Enhanced copper extraction in the chalcopyrite bioleaching system assisted by microbial fuel cells and catalyzed by silver-bearing ores, J. Environ. Chem. Eng. 10 (6) (2022) 108827.

[109] D. Ríos, S. Bellenberg, S. Christel, P. Lindblom, T. Giroux, M. Dopson, Potential of single and designed mixed cultures to enhance the bioleaching of chalcopyrite by oxidation-reduction potential control, Hydrometallurgy 224 (2024) 106245.

[110] D.J. Nangali, J. Siame, A. Mzula, L. Musango, A. Mugala, L. Mukosha, R. Ngulube, L. Dusengemungu, Bioleaching of chalcopyrite using native Acidithiobacillus ferrooxidans isolated in a mining area in Kitwe Zambia , Sci. Afr. 22 (2023) e01882.

[111] H. Zhang, D.Z. Wei, W.G. Liu, D.X. Hou, R.Y. Zhang, Effect of polyvinyl pyrrolidone on chalcopyrite bioleaching with Acidithiobacillus ferrooxidans , Hydrometallurgy 205 (2021) 105753.

[112] H. Zhang, D.Z. Wei, W.G. Liu, D.X. Hou, R.Y. Zhang, Enhancement mechanism of polyoxyethylene nonyl phenyl ether on the bioleaching of chalcopyrite, Miner. Eng. 173 (2021) 107237.

[113] K.T. Konadu, R. Sakai, D.M. Mendoza, C. Chuaicham, H. Miki, K. Sasaki, Effect of carbonaceous matter on bioleaching of Cu from chalcopyrite ore, Hydrometallurgy 195 (2020) 105363.

[114] R.Y. Zhang, D.Z. Wei, Y.B. Shen, W.G. Liu, T. Lu, C. Han, Catalytic effect of polyethylene glycol on sulfur oxidation in chalcopyrite bioleaching by Acidithiobacillus ferrooxidans , Miner. Eng. 95 (2016) 74-78.

[115] J. You, S.K. Solongo, A. Gomez-Flores, S. Choi, H. Zhao, M. Urík, S. Ilyas, H. Kim, Intensified bioleaching of chalcopyrite concentrate using adapted mesophilic culture in continuous stirred tank reactors, Bioresour. Technol. 307 (2020) 123181.

[116] W. Chen, S.H. Yin, A.X. Wu, L.M. Wang, X. Chen, Bioleaching of copper sulfides using mixed microorganisms and its community structure succession in the presence of seawater, Bioresour. Technol. 297 (2020) 122453.

[117] G. Su, S. Li, X. Deng, L. Hu, L. Praburaman, Z. He, H. Zhong, W. Sun, Low concentration of Tween-20 enhanced the adhesion and biofilm formation of Acidianus manzaensis YN-25 on chalcopyrite surface , Chemosphere 284 (2021) 131403.

[118] Z.X. Jin, T. Huang, X.M. Zhang, S.H. Zhang, Bioelectrochemical-assisted bioleaching of chalcopyrite: effect of pulp density, anode material, and sliver ion, Process. Saf. Environ. Prot. 159 (2022) 740-748.

[119] Y. Yang, W.H. Liu, X.Y. Gao, M. Chen, An XAS study of silver species evolution in silver-catalysed chalcopyrite bioleaching, Hydrometallurgy 186 (2019) 252-259.

[120] J. Wang, R. Liao, L. Tao, H.B. Zhao, R. Zhai, W.Q. Qin, G.Z. Qiu, A comprehensive utilization of silver-bearing solid wastes in chalcopyrite bioleaching, Hydrometallurgy 169 (2017) 152-157.

[121] H. Abdollahi, M. Noaparast, S.Z. Shafaei, Z. Manafi, J.A. Muñoz, O.H. Tuovinen, Silver-catalyzed bioleaching of copper, molybdenum and rhenium from a chalcopyrite-molybdenite concentrate, Int. Biodeterior. Biodegrad. 104 (2015) 194-200.

[122] R. Liao, X.X. Wang, B.J. Yang, M.X. Hong, H.B. Zhao, J. Wang, G.Z. Qiu, Catalytic effect of silver-bearing solid waste on chalcopyrite bioleaching: a kinetic study, J. Cent. South Univ. 27 (5) (2020) 1395-1403.

[123] C.K. Tanne, A. Schippers, Electrochemical investigation of chalcopyrite (bio) leaching residues, Hydrometallurgy 187 (2019) 8-17.

[124] J. Petersen, D.G. Dixon, Competitive bioleaching of pyrite and chalcopyrite, Hydrometallurgy 83 (1-4) (2006) 40-49.

[125] T. Biegler, M.D. Horne, The electrochemistry of surface oxidation of chalcopyrite, J. Electrochem. Soc. 132 (6) (1985) 1363-1369.

[126] M. Khoshkhoo, M. Dopson, A. Shchukarev, Å. Sandström, Electrochemical simulation of redox potential development in bioleaching of a pyritic chalcopyrite concentrate, Hydrometallurgy 144 (2014) 7-14.

[127] T. Biegler, D.A. Swift, Anodic electrochemistry of chalcopyrite, J. Appl. Electrochem. 9 (5) (1979) 545-554.

[128] C. Gómez, M. Figueroa, J. Muñoz, M.L. Blázquez, A. Ballester, Electrochemistry of chalcopyrite, Hydrometallurgy 43 (1-3) (1996) 331-344.

[129] Y. Liu, Z. Dang, P.X. Wu, J. Lu, X.H. Shu, L.C. Zheng, Influence of ferric iron on the electrochemical behavior of pyrite, Ionics 17 (2) (2011) 169-176.

[130] A. Ghahremaninezhad, D.G. Dixon, E. Asselin, Electrochemical and XPS analysis of chalcopyrite (CuFeS₂) dissolution in sulfuric acid solution , Electrochim. Acta 87 (2013) 97-112.

[131] S. Feng, K. Li, Z. Huang, Y. Tong, H. Yang, Specific mechanism of Acidithiobacillus caldus extracellular polymeric substances in the bioleaching of copper-bearing sulfide ore , PLoS One 14 (4) (2019) e0213945.

[132] A.F. Tshilombo, J. Petersen, D.G. Dixon, The influence of applied potentials and temperature on the electrochemical response of chalcopyrite during bacterial leaching, Miner. Eng. 15 (11) (2002) 809-813.

[133] L.M. Wang, S.H. Yin, B.N. Deng, Understanding the effect of stepwise irrigation on liquid holdup and hysteresis behavior of unsaturated ore heap, Minerals 11 (11) (2021) 1180.

[134] L.M. Wang, S.H. Yin, A.X. Wu, Ore agglomeration behavior and its key controlling factors in heap leaching of low-grade copper minerals, J. Clean. Prod. 279 (2021) 123705.

[135] L.M. Wang, S.H. Yin, A.X. Wu, Visualization of flow behavior in ore-segregated packed beds with fine interlayers, Int. J. Miner. Metall. Mater. 27 (7) (2020) 900-909.

[136] G. Nkulu, S. Gaydardzhiev, E. Mwema, P. Compere, SEM and EDS observations of carrollite bioleaching with a mixed culture of acidophilic bacteria, Miner. Eng. 75 (2015) 70-76.

[137] K. Zhang, Y. Zhang, R. Xin, Y.P. Zhang, Z.G. Niu, Variation pattern of terrestrial antibiotic resistances and bacterial communities in seawater/freshwater mixed microcosms, Chemosphere 200 (2018) 201-208.

[138] E.F. DeLong, Archaea in coastal marine environments, Proc. Natl. Acad. Sci. U. S. A. 89 (12) (1992) 5685-5689.

[139] X.M. Hua, Y.F. Zheng, Q. Xu, X.G. Lu, H.W. Cheng, X.L. Zou, Q.S. Song, Z.Q. Ning, Interfacial reactions of chalcopyrite in ammonia-ammonium chloride solution, Trans. Nonferrous Met. Soc. China 28 (3) (2018) 556-566.

[140] I.G. Reilly, D.S. Scott, The leaching of a chalcopyrite concentrate in ammonia, Can. J. Chem. Eng. 55 (5) (1977) 527-533.

[141] L.W. Beckstead, J.D. Miller, Ammonia, oxidation leaching of chalcopyrite: surface deposit effects, Metall. Trans. B 8 (1) (1977) 31-38.

[142] L.W. Beckstead, J.D. Miller, Ammonia, oxidation leaching of chalcopyrite: reaction kinetics, Metall. Trans. B 8 (1) (1977) 19-29.

[143] E.A. Oraby, H. Li, J.J. Eksteen, An alkaline glycine-based leach process of base and precious metals from powdered waste printed circuit boards, Waste Biomass Valoriz. 11 (8) (2020) 3897-3909.

[144] M. Lundström, Chalcopyrite Dissolution in Cupric Chloride Solutions (Dissertation), Heisinki University of Technology, Espoo, Finland, 2009.

[145] M.J. Nicol, The electrochemistry of chalcopyrite in alkaline solutions, Hydrometallurgy 187 (2019) 134-140.

[146] I.F. Barton, J.B. Hiskey, Chalcopyrite leaching in novel lixiviants, Hydrometallurgy 207 (2022) 105775.

[147] A.J. Bard, Photoelectrochemistry and heterogeneous photo-catalysis at semiconductors, J. Photochem. 10 (1) (1979) 59-75.

[148] Q. Zhu, Q. Xu, M. Du, X. Zeng, G. Zhong, B. Qiu, J. Zhang, Recent progress of metal sulfide photocatalysts for solar energy conversion, Adv. Mater. 34 (45) (2022) e2202929.

[149] H.M. Hao, X.J. Lang, Metal sulfide photocatalysis: visible-light-induced organic transformations, ChemCatChem 11 (5) (2019) 1378-1393.

[150] C.X. Zhao, B.J. Yang, X.X. Wang, H.B. Zhao, M. Gan, G.Z. Qiu, J. Wang, Catalytic effect of visible light and Cd²⁺ on chalcopyrite bioleaching , Trans. Nonferrous Met. Soc. China 30 (4) (2020) 1078-1090.

[151] C.X. Zhao, B.J. Yang, R. Liao, M.X. Hong, S.C. Yu, S.T. Liu, J. Wang, G.Z. Qiu, Combined effect and mechanism of visible light and Ag⁺ on chalcopyrite bioleaching , Miner. Eng. 175 (2022) 107283.

[152] S. Zhou, M. Gan, J.Y. Zhu, Q. Li, S.Q. Jie, B.J. Yang, X.D. Liu, Catalytic effect of light illumination on bioleaching of chalcopyrite, Bioresour. Technol. 182 (2015) 345-352.

[153] F.K. Crundwell, A. Van Aswegen, L.J. Bryson, C. Biley, D. Craig, V.D. Marsicano, J.M. Keartland, The effect of visible light on the dissolution of natural chalcopyrite (CuFeS₂) in sulphuric acid solutions , Hydrometallurgy 158 (2015) 119-131.

[154] B.J. Yang, M. Lin, J.H. Fang, R.Y. Zhang, W. Luo, X.X. Wang, R. Liao, B.Q. Wu, J. Wang, M. Gan, B. Liu, Y. Zhang, X.D. Liu, W.Q. Qin, G.Z. Qiu, Combined effects of jarosite and visible light on chalcopyrite dissolution mediated by Acidithiobacillus ferrooxidans , Sci. Total Environ. 698 (2020) 134175.