Skip to main content
Log in

Biogenesis of thiosulfate in microorganisms and its applications for sustainable metal extraction

  • Review paper
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Thiosulfate is a lixiviant with potential applications for extraction of precious metals with lower environmental impact. As an alternative leaching reagent to cyanide, thiosulfate has promising gold extraction efficiency with much lower risk to operators and the environment. Thiosulfate is often produced at high temperatures via processes utilizing sulfide or sulfur and an oxidant. However, certain microorganisms can produce thiosulfate as the final product of their metabolism. This represents potential for lower emissions and costs in the manufacture of gold leaching reagents. Biotechnological applications of these processes have not been reported in the past and need to be investigated in depth. This review serves as a study of microorganisms to collect and analyze the reported species for potential utilization of biogenic thiosulfate in industrial applications, with a specific focus on precious metals extraction. Bacteria were identified and compared with respect to thiosulfate producing ability, feasibility for the mining industry, and cost of substrates. The future applications of biogenic thiosulfate and further direction of research on the topic have been identified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071

    Article  CAS  Google Scholar 

  • Akcil A (2010) A new global approach of cyanide management: international cyanide management code for the manufacture, transport, and use of cyanide in the production of gold. Miner Process Extr Metall Rev 31:135–139

    Article  CAS  Google Scholar 

  • Antón J et al (2002) Salinibacter ruber gen. nov., sp. nov., a novel extreme halophilic member of the Bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 52:485–491

    Article  Google Scholar 

  • Aylmore MG (2016) Thiosulfate as an alternative lixiviant to cyanide for gold ores. In: Adams M (ed) Gold ore processing, 2nd edn. Elsevier, Singapore, pp 485–523

    Chapter  Google Scholar 

  • Banijamali S, Raygan S, Amadeh A (2021) Leaching behavior of silver sulfide in the sodium thiosulfate-copper sulfate- sodium metabisulfite system. Miner Eng 174:107275

    Article  CAS  Google Scholar 

  • Barton L, Fardeau M, Fauque G (2014) Hydrogen sulfide: a toxic gas produced by dissimilatory sulfate and sulfur reduction and consumed by microbial oxidation. Metal Ions Life Sci 14:237–277

    Article  CAS  Google Scholar 

  • Berben T, Overmars L, Sorokin D, Gerard M (2019) Diversity and distribution of sulfur oxidation-related genes in Thioalkalivibrio, a genus of chemolithoautotrophic and haloalkaliphilic sulfur-oxidizing bacteria. Front Microbiol 10:160

    Article  Google Scholar 

  • Bertin F et al (2013) Arsenic toxicosis in cattle: meta-analysis of 156 cases. Vet Intern Met 27(4):977–981

    Article  CAS  Google Scholar 

  • Bilska A et al (2008) Biological actions of lipoic acid associated with sulfane sulfur metabolism. Pharmacol Rep 60:225–232

    CAS  Google Scholar 

  • Bilska-Wilkosz A, Iciek M, Górny M, Kowalczyk-Pachel D (2017) The role of hemoproteins: hemoglobin, myoglobin and neuroglobin in endogenous thiosulfate production processes. Int J Mol Sci 18(6):1315

    Article  Google Scholar 

  • Birloaga I, Veglio F (2018) Overview on hydrometallurgical procedures for silver recovery from various wastes. J Environ Chem Eng 6(2):2932–2938

    Article  CAS  Google Scholar 

  • Boden R, Kelly DP, Murrell JC, Schäfer H (2010) Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle. Environ Microbiol 12:2688–2699

    CAS  Google Scholar 

  • Bohu T et al (2019) Evidence for fungi and gold redox interaction under Earth surface conditions. Nat Commun 10:2290

    Article  Google Scholar 

  • Booker A et al (2017) Sulfide generation by dominant halanaerobium microorganisms in hydraulically fractured shales. mSphere 2(4):e00257–e002517

    Article  CAS  Google Scholar 

  • Brandelli A (2008) Bacterial Keratinases: useful enzymes for bioprocessing agroindustrial wastes and beyond. Food Bioprocess Technol 1:105–116

    Article  Google Scholar 

  • Calvo G, Mudd G, Valero A (2016) Decreasing ore grades in global metallic mining: a theoretical issue or a global reality? Resources 5(4):36

    Article  Google Scholar 

  • Camacho D et al (2020) New Insights into acidithiobacillus thiooxidans sulfur metabolism through coupled gene expression, Solution Chemistry, Microscopy, and Spectroscopy Analyses.Front. Microbiol.,11

  • Chen Z et al (1994) The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266:430–432

    Article  CAS  Google Scholar 

  • Chen X (2008) Associated sulfide minerals in thiosulfate leaching of gold: problems and solutions. Queen’s University, Kingston

    Google Scholar 

  • Chen C et al (2013) Autotrophic and heterotrophic denitrification by a newly isolated strain Pseudomonas sp. C27. Bioresour Technol 145:351–356

    Article  CAS  Google Scholar 

  • Choudhary L, MacDonald D, Alfantazi A (2015) Role of thiosulfate in the corrosion of steels: a review. Corrosion 71(9):1147–1168

    Article  CAS  Google Scholar 

  • Chung YC, Huang C, Tseng CP (1996) Operation optimization of Thiobacillus thioparus CH11 biofilter for hydrogen sulfide removal. J Biotechnol 52(1):31–38

    Article  CAS  Google Scholar 

  • Dehshahri A et al (2021) Editing SOX genes by CRISPR-Cas: current insights and future perspectives. Int J Mol Sci 22:11321

    Article  CAS  Google Scholar 

  • de Wit R, van Gemerden H (1987) Oxidation of sulfide to thiosulfate by Microcoleus chtonoplastes. FEMS Microbiol 45:7–13

    Article  Google Scholar 

  • de Wit R, van Boekel W, van Gemerden H (1988) Growth of the cyanobacterium Microcoleus chtonoplastes. FEMS Microbiol Ecol 53:203–209

    Article  Google Scholar 

  • de Zwart J, Kuenen J (1997) Aerobic conversion of dimethyl sulfide and hydrogen sulfide by Methylophaga sulfidovorans: implications for modeling DMS conversion in a microbial mat. FEMS Microbiol Ecol 22:155–165

    Article  Google Scholar 

  • de Zwart J, Neisse P, Kuenen JG (1996) Isolation and characterization of Methylophagasulfidovorans,sp.nov.;an obligately methylotrophic, aerobic, dimethyl sulfide oxidizing bacterium from a microbial mat. FEMS Microbiol Ecol 20:261–270

    Article  Google Scholar 

  • de Zwart J, Neisse P, Kuenen JG (1997) Competition for dimethyl sulfide and hydrogen sulfide by methylophaga sulfidovorans and thiobacillus thioparus T5 in continuous cultures. Appl Environ Microbiol 63(8):3318–3322

    Article  Google Scholar 

  • Dong K et al (2021) The detoxification and utilization of cyanide tailings: A critical review. J Clean Prod 302:126946

    Article  Google Scholar 

  • Dong Z, Jiang T, Xu B, Yang Y, Li Q (2019) An eco-friendly and efficient process of low potential thiosulfate leaching-resin adsorption recovery for extracting gold from a roasted gold concentrate. J Clean Prod 229:387–398

    Article  CAS  Google Scholar 

  • Esdaile L, Chalker J (2018) The mercury problem in artisanal and small-scale gold mining. Chemistry 24(27):6905–6916

    Article  CAS  Google Scholar 

  • Faraji F, Wang J, Mahandra H, Ghahreman A (2021) A green and sustainable process for the recovery of gold from lowgrade sources using biogenic cyanide generated by bacillus. ACS Sustainible Chem Eng 9:236–245

    Article  CAS  Google Scholar 

  • Findlay A, Alexey K (2017) Turnover rates of intermediate sulfur species (Sx2-, S0, S2O32-, S4O62-, SO32-) in anoxic freshwater and sediments. FrontMicrobiol 8:2551

    Google Scholar 

  • Fitz R, Cypionka H (1990) Formation of thiosulfate and trithionate during sulfite reduction by washed cells of Desulfovibrio desulfuricans. Arch Microbiol 154:400–406

    Article  CAS  Google Scholar 

  • Friedrich C et al (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol Volume 8:253–259

    Article  CAS  Google Scholar 

  • Frigaard N, Dahl C (2008) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200

    Article  Google Scholar 

  • Gajigo O, Dhaou M (2015) Economy of scale in gold mining. African Development Bank, Abidjan

    Google Scholar 

  • Ghosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 33:999–1043

    Article  CAS  Google Scholar 

  • Gorain B, Kondos P, Lakshmanan V (2016) Innovations in gold and silver processing. In: Lakshmanan V, Roy R, Ramachandran V (eds) Innovative process development in metallurgical industry. Springer, Cham

    Google Scholar 

  • Grabarczyk D, Berks B (2017) Intermediates inthe sox sulfur oxidation pathway are bound to a sulfaneconjugate of the carrier protein SoxYZ. PLoS ONE 12:e0173395

    Article  Google Scholar 

  • Griffin P, Hammond G, Norman J (2018) Industrial energy use and carbon emissions reduction in the chemicals sector: A UK perspective. Appl Energy 227(1):587–602

    Article  CAS  Google Scholar 

  • Grosse A, Dicinoski G, Shaw M, Haddad P (2003) Leaching and recovery of gold using ammoniacal thiosulfate leach liquors (a review). Hydromet 69:1–21

    Article  CAS  Google Scholar 

  • Habicht K, Canfield D, Rethmeier J (1998) Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite. Geochim Cosmochim Acta 62(15):2585–2595

    Article  CAS  Google Scholar 

  • Hao J, Wang Y, Wu Y, Guo F (2020) Metal recovery from waste printed circuit boards: A review for current status and perspectives. Resour Conserv Recycl 157:104787

    Article  Google Scholar 

  • Hildebrant T, Grieshaber M (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275(13):3352–3361

    Article  Google Scholar 

  • Hilson G, Monhemius A (2006) lternatives to cyanide in the gold mining industry: What prospects for the future? J Clean Prod 14:1158–1167

    Article  Google Scholar 

  • Hinckley E, Crawford J, Fakhraei H, Driscoll C (2020) A shift in sulfur-cycle manipulation from atmospheric emissions to agricultural additions. Nat Geosci 14:597–604

    Article  Google Scholar 

  • Howarth R (1982) The ecological significance of sulfur in the energy dynamics of salt marsh and coastal marine sediments. Biogeochemistry 1:5–27

    Article  Google Scholar 

  • Howarth RW, Teal J (1980) Energy flow in a salt marsh ecosystem: the role of reduced inorganic sulfur compounds. Am Nat 116:862–870

    Article  CAS  Google Scholar 

  • Hubert C, Voordouw G (2020) Oil field souring control by nitrate-reducing sulfurospirillum spp. That outcompete sulfate-reducing bacteria for organic electron donors. Appl Environ Microbiol, 73(8)

  • Hutt L (2016) Taxonomy, physiology and biochemistry of the sulfur Bacteria, s.l.: The University of Plymouth. PhD Thesis

  • Hutt L et al (2017) Permanent draft genome of Thiobacillus thioparus DSM 505 T, an obligately chemolithoautotrophic member of the Betaproteobacteria. Environ microbiome 12:10

    Article  Google Scholar 

  • Imhoff J (1983) Rhodopseudomonas marina sp. nov., a new marine phototrophic purple bacterium. Syst Appl Microbiol 4(4):512–521

    Article  CAS  Google Scholar 

  • Janssen A et al (1995) Biological sulphide oxidation in a fed-batch reactor. Biotechnol Bioeng 47:327–333

    Article  CAS  Google Scholar 

  • Jerez C (2017) Biomining of metals: how to access and exploit natural resource sustainably. Microb Biotechnol 10(5):1191–1193

    Article  Google Scholar 

  • Jeronimo R, Rap E, Vos J (2015) The politics of land use planning: gold mining in Cajamarca, Peru. Land Use Policy 49:104–117

    Article  Google Scholar 

  • Ji J, Fleming C, West-Sells P, Hackl R (2003) A novel thiosulfate system for leaching gold without the use of copper and ammonia. s.l., TMS, pp. 227–244.

  • Jørgensen B (1982) Mineralization of organic matter in the sea bed - the role of sulfate reduction. Nature 296:643–645

    Article  Google Scholar 

  • Jorgensen B (1990) A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249(4965):152–154

    Article  CAS  Google Scholar 

  • Jorgensen B, Bak F (1991) Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Appl aned Environ Microbiol 57(3):847–856

    Article  CAS  Google Scholar 

  • Jørgensen B, Findlay A, Pellerin A (2019) The biogeochemical sulfur cycle of marine sediments. Front Microbiol 10:849

    Article  Google Scholar 

  • Jorjani E, Sabzkoohi H (2022) Gold leaching from ores using biogenic lixiviants – A review. Curr Res Biotechnol 4:10–20

    Article  CAS  Google Scholar 

  • Kaksonen A et al (2014b) Evaluation of submerged bio-oxidation concept for refractory gold ores. Hydromet 141:117–125

    Article  CAS  Google Scholar 

  • Kaksonen A et al (2018) Recent progress in biohydrometallurgy and microbial characterisation. Hydromet 180:7–25

    Article  CAS  Google Scholar 

  • Kaksonen A et al (2020) Prospective directions for biohydrometallurgy. Hydromet 195:105375

    Article  Google Scholar 

  • Kaksonen A, Mudunuru B, Hackl R (2014a) The role of microorganisms in gold processing and recovery—A review. Hydromet 142:70–83

    Article  CAS  Google Scholar 

  • Kelly D (1982) Biochemistry of chemolithotrophic oxidation of inorganic sulphur. Philoso Trans Royal Soc London B 298:499–528

    CAS  Google Scholar 

  • Kelly D, Shergill J, Lu W, Wood A (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71:95–107

    Article  CAS  Google Scholar 

  • Kelsall G, Thompson I (1993) Redox chemistry of H2S oxidation in the British Gas Stretford Process Part I: Thermodynamics of sulphur-water systems at 298 K. J Appl Electrochemsity 23(4):279–286

    Article  CAS  Google Scholar 

  • Kiragosyan K et al (2019) Development and validation of a physiologically based kinetic model for starting up and operation of the biological gas desulfurization process under haloalkaline conditions. Water Research X,4

  • Kletzin A (1989) Coupled enzymatic production of sulfite, thiosulfate, and hydrogen sulfide from sulfur: purification and properties of a sulfur oxygenase reductase from the facultatively anaerobic archaebacterium Desulfurolobus ambivalens. J Bacteriol 171(3):1638–1643

    Article  CAS  Google Scholar 

  • Krober E, Schafer H (2019) Identification of proteins and genes expressed by methylophaga thiooxydans during growth on dimethylsulfide and their presence in other members of the genus. Front Microbiol, 32

  • Kubo K et al (2011) Sulfur-metabolizing bacterial populations in microbial mats of the Nakabusa hot spring, Japan. Syst Appl Microbiol 34(4):293–302

    Article  Google Scholar 

  • Kuenen J (1975) Colourless sulfur bacteria and their role in the sulfur cycle. Plant Soil 43:49–76

    Article  CAS  Google Scholar 

  • Kunert J (1989) Biochemical mechanism of keratin degradation by the actinomycete Streptomyces fradiae and the fungus Microsporum gypseum: A comparison. J Basic Microbiol 29(9):597–604

    Article  CAS  Google Scholar 

  • Kunert J, Stránský Z (1988) Thiosulfate production from cystine by the keratinolytic prokaryote Streptomyces fradiae. Arch Microbiol 150:600–601

    Article  CAS  Google Scholar 

  • Lahme S et al (2020) Comparison of sulfide-oxidizing Sulfurimonas strains reveals a new mode of thiosulfate formation in subsurface environments. Mar Microb Ecol 22(5):1784–1800

    CAS  Google Scholar 

  • Langhans J Jr, Lei K, Carnahan T (1992) Copper-catalyzed thiosulfate leaching of low-grade gold ores. Hydromet 29(1–3):191–203

    Article  CAS  Google Scholar 

  • Lee J et al (2021) Toward sustainable solution for biooxidation of waste and refractory materials using neutrophilic and alkaliphilic microorganisms - a review. ACS Appl Bio Mater 4:2274–2292

    Article  CAS  Google Scholar 

  • Lee JC, Pandey D (2012) Bio-processing of solid wastes and secondary resources for metal extraction – A review. Waste Manag 32(1):3–18

    Article  CAS  Google Scholar 

  • Luthur IIIG (1987) Pyrite oxidation and reduction: Molecular orbital theory considerations. Geochim Cosmochim Acta 51(12):3193–3199

    Article  Google Scholar 

  • Luthur IIIG, Church T, Scudlark J, Cosman M (1986) Inorganic and organic sulfir cycling in salt-marsh pore waters. Science 232(4751):746–749

    Article  Google Scholar 

  • Madigan M, Martinko J, Parker J (2006) Brock biology of microorganisms, 11 edn. Prentince Hall, Upper Saddle River, NJ

    Google Scholar 

  • Mahmoud A et al (2017) A review of sulfide minerals microbially assisted leaching in stirred tank reactors. Int Biodeterior Biodegradation 119:118–164

    Article  CAS  Google Scholar 

  • Maki Y (1987) Biological oxidation of sulfide and elemental sulfur by the a-type sulfur-turf growing in hot spring effluents. J Gen Appl Microbiol 33(2):123–134

    Article  CAS  Google Scholar 

  • Marchbank AR, Thomas KG, Dreisinger D, Fleming C (1996) Gold recovery from refractory carbonaceous ores by pressure oxidation and thiosulfate leaching. U.S.A, Patent No. 5536297

  • Marcia M, Ermler U, Peng G, Michel H (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc. Natl. Acad. Sci. U.S.A., 106: 9625–9630

  • Marsden J, House C (2006) Chemistry of gold extraction (2nd Edition). SME

  • McGreer P, McGreer E, Lee M (2016) Medical uses of sodium thiosulfate. J Neurol Neuromedicine 1(3):28–30

    Article  Google Scholar 

  • McNeice J, Marzoughi O, Kim R, Ghahreman A (2021) Gold extraction from refractory sulfide gold concentrates: a comparison of bio-oxidation and neutral atmospheric pre-treatment and economic implications. J Sustainable Metal 7:1354–1367

    Article  Google Scholar 

  • McNeice J, Mahandra H, Ghahreman A (2022) Application of biogenic thiosulfate produced by Methylophaga sulfidovorans for Sustainible gold Extraction. ACS Sustainible Chem Eng, In press

  • Meier D et al (2017) Niche partitioning of diversesulfur-oxidizing Bacteria at hydrothermal vents. SME J 11:1545–1558

    CAS  Google Scholar 

  • Mills J, Antler G, Turchyn A (2016) Geochemical evidence for cryptic sulfur cycling in salt marsh sediments. Earth Planet Sci Lett 453(1):23–32

    Article  CAS  Google Scholar 

  • Mohagheghi A, Updegraff D, Goldhaber M (1985) The role of sulfate-reducing bacteria in the deposition of sedimentary uranium ores. Geomicrobiol J 4(2):153–173

    Article  CAS  Google Scholar 

  • Mubarok Z et al (2016) Improving gold recovery from refractory gold ores through biooxidation using iron-sulfur-oxidizing/sulfur-oxidizing mixotrophic bacteria. Hydromet 168:69–75

    Article  Google Scholar 

  • Murphy A et al (2020) Sulphide addition favours respiratory ammonification (DNRA) over complete denitrification and alters the active microbial community in salt marsh sediments. Environ Microbiol 22(6):2124–2139

    Article  CAS  Google Scholar 

  • Nielsen M, Revsbech N, Kühl M (2015) Microsensor measurements of hydrogen gas dynamics in cyanobacterial microbial mats. Front Microbiol 6:726

    Article  Google Scholar 

  • Norgate T, Jahanshahi S (2011) Assessing the energy and greenhouse gas footprints of nickel laterite processing. Min Eng 24(7):698–707

    Article  CAS  Google Scholar 

  • Norris P (2007) Acidophile diversity in mineral sulfide oxidation. In: Rawlings D, Johnson B (eds) Biomining. Springer-verlag, Berlin, pp 199–212

    Chapter  Google Scholar 

  • Oh S, Kim J, Lee M, Choi K (2008) Dechlorination with sodium thiosulfate affectsthe toxicity of wastewater contaminated withcopper, cadmium, nickel, or zinc. Environ Toxicol 2:211–217

    Article  Google Scholar 

  • Olguín-Lora P et al (2011) Evaluation of haloalkaliphilic sulfur-oxidizing microorganisms with potential application in the effluent treatment of the petroleum industry. Biodegradation 22:83–93

    Article  Google Scholar 

  • Oyarzún P, Arancibia F, Canales C, Aroca GE (2003) Biofiltration of high concentration of hydrogen sulphide using thiobacillus thioparus. Process Biochem 39(2):165–170

    Article  Google Scholar 

  • Pannekens M et al (2019) Oil reservoirs, an exceptional habitat for microorganisms. New Biotechnol 49:1–9

    Article  CAS  Google Scholar 

  • Pjevac P et al (2018) Metaproteogenomicprofiling of microbial communities colonizing activelyventing hydrothermal chimneys. Front Microbiol 9:1–12

    Article  Google Scholar 

  • Pott A, Dahl C (1998) Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894

    Article  CAS  Google Scholar 

  • Quatrini R et al (2009) Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics, 10(394)

  • Rabenstein A, Rethmeier J, Fischer U (1995) Cyanobacteria, sulphite as intermediate sulphur compound in anaerobic sulphide oxidation to thiosulphate by Marine. Z für Naturforschung C 50(11–12):769–774

    Article  CAS  Google Scholar 

  • Austaralian Gold Reagents (2002) Transport of solid sodium cyanide, change to environmental conditions. Austaralian Gold Reagents, Perth, Australia

  • Reith F, McPhail D (2007) Microbial influences on solubilisation and mobility of gold and arsenic in regolith samples from two gold mines in semi-arid and tropical Australia. Geochim Cosmochim Acta 71:1183–1196

    Article  CAS  Google Scholar 

  • Reith F, Zammit Z, McPhail D, Brugger J (2012) Potential for the utilisation of micro-organisms in gold processing: a review. Mineral Process Extractive Metall IMM Trans Sect C 121(4):251–260

    Article  CAS  Google Scholar 

  • Reuter M, Schaik A (2016) Gold - a key enabler of a circular economy: recycling of waste electric and electronic equipment. Gold ore processing - project development and operations. Elsevier, Singapore, pp 937–958

    Chapter  Google Scholar 

  • Richter C et al (2018) Constraints of bioleaching in in-situ recovery applications. Hydromet 178:209–214

    Article  CAS  Google Scholar 

  • Rohwerder T, Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149(7):1699–1709

    Article  CAS  Google Scholar 

  • Roldán-Contreras E et al (2020) Leaching of silver and gold contained in a sedimentary ore, using sodium thiosulfate; a preliminary kinetic study. Metals 10(2):159

    Article  Google Scholar 

  • Rühl P et al (2017) A sulfur oxygenase from the haloalkaliphilic bacterium Thioalkalivibrio paradoxus with Atypically low reductase activity. J Bacteriol 199(4):e00675–e00616

    Article  Google Scholar 

  • Sakurai H, Ogawa T, Shiga M, Inoue K (2010) Inorganic sulfur oxidizing system in green sulfur bacteria. Photosynth Res 104:163–176

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schippers A et al (2014) Biomining: metal recovery from ores with microorganisms. In: Schippers A, Glombitza F, Sand W (eds) Geobiotechnologogy I Metal-related Issues. Springer-Verlag, Berl, pp 1–47

    Google Scholar 

  • Schippers A, Rohwinder T, Sand W (1999) Intermediary sulfur compounds in pyrite oxidation: implications for bioleaching andd biodepyritization of coal. Appl Micvrobial Biotechnol 52:104–110

    Article  CAS  Google Scholar 

  • Senanayake G (2004) Analysis of reaction kinetics, speciation and mechanism of gold leaching and thiosulfate oxidation by ammoniacal copper(II) solutions. Hydromet 75(1–4):55–75

    Article  CAS  Google Scholar 

  • Senanayake G (2005) Role of copper(II), carbonate and sulphite in gold leaching and thiosulphate degradation by oxygenated alkaline non-ammoniacal solutions. Min Eng 18(4):409–426

    Article  CAS  Google Scholar 

  • Senanayake G (2012) Gold leaching by copper (II) in ammoniacal thiosulphate solutions in the presence of. Hydromet 115:1–20

    Article  Google Scholar 

  • Senanayake G, Perera W, Nicol M (2003) Thermodynamic studies of the gold(III)/(I)/(0) redox system in ammonia-thiosulfate solutions at 25 °C. Vancouver, Canada, s.n., 158–168

  • Sessa C et al (2016) Investigation of the possible origins of sulfur in 19th century salted paper photographs by x-ray fluorescence spectroscopy. X-Ray Spectrom 45(3):176–184

    Article  CAS  Google Scholar 

  • Sevilla M, Diez N, Ferrero G, Fuertes A (2019) Sustainable supercapacitor electrodes produced by the activation of biomass with sodium thiosulfate. Energy Storage Mater 18:356–365

    Article  Google Scholar 

  • Shahak Y, Arieli B, Padan E, Hauska G (1992) Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett 299:127–130

    Article  CAS  Google Scholar 

  • Sharshar M et al (2020) Improving confirmed nanometric sulfur bioproduction using engineered Thioalkalivibrio versutus. Bioresour Technol 317:124018

    Article  CAS  Google Scholar 

  • Shevchenko T, Laitala K, Danko Y (2019) Understanding consumer E-waste recycling behavior: introducing a new economic incentive to increase the collection rates. Sustainability 11:2656

    Article  Google Scholar 

  • Sitando O et al (2018) A review of factors affecting gold leaching in non-ammoniacal thiosulfate solutions including degradation and in-situ generation of thiosulfate. Hydromet 178:151–175

    Article  CAS  Google Scholar 

  • Sorokin DY et al (2018) Sulfur respiration in a group of facultatively anaerobic natronoarchaea ubiquitous in hypersaline soda lakes. Front Microbiol 9:2359

    Article  Google Scholar 

  • Sorokin D, Kuenen J (2005) Haloalkaliphilic sulfur-oxidizing bacteria in soda lakes. FEMS Microbiol Rev 29(4):685–702

    Article  CAS  Google Scholar 

  • Sousa R et al (2021) A systematic review of sustainable gold extraction from raw ores using alternative leaching reagents. Extract Indus Soc 8(4):101018

    Google Scholar 

  • Southham G, Lengke M, Fairbrother L, Reith F (2009) The biogeochemistry of gold. Elements 5(5):303–307

    Article  Google Scholar 

  • Spasova I, Nicolova M, Veglio F, Groudev S (2006) Leaching of gold from a polymetallic sulphide ore, annual of the university of mining and geology “ST. IVAN RILSKI”. Geol Geophys 49(I):213–216

    Google Scholar 

  • Sun C, Zheng X, Kou J, Xing Y (2020) A review of gold extraction using noncyanide lixiviants: Fundamentals, advancements, and challenges toward alkaline sulfur-containing leaching agents. Int J Min Metall Mater 27:417–431

    Article  CAS  Google Scholar 

  • Suzuki I, Silver M (1966) The initial product and properties of the sulfur-oxidizing enzyme of thiobacilli. Biochim Biophys Acta 122(22):65428

    Google Scholar 

  • Tamazawa S et al (2012) Metagenomic and biochemical characterizations of sulfur oxidation metabolism in uncultured large sausage-shaped bacterium in hot spring microbial mats. PLoS ONE 7(11):e49793

    Article  CAS  Google Scholar 

  • Tang K, Baskaran V, Nemati M (2009) Bacteria of the sulphur cycle: An overview of microbiology, biokinetics and their role in petroleum and mining industries. Biochem Eng J 44(1):73–94

    Article  CAS  Google Scholar 

  • Tian H et al (2017) Compositions and abundances of sulfate-reducing and sulfur-oxidizing microorganisms in water-flooded petroleum reservoirs with different temperatures in China. Front Microb 8:143

    Article  Google Scholar 

  • Tourova T et al (2013) Analysis of community composition of sulfur-oxidizing bacteria in hypersaline and soda lakes using soxB as a functional molecular marker. FEMS Microbiol Ecol 84(2):280–289

    Article  CAS  Google Scholar 

  • Truper H, Fischer U (1982) Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis. Philosophical Trans Royal Soc B Biol Sci 298(1093):529–542

    Google Scholar 

  • Valdés J et al (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BCM Genomics 9:597

    Article  Google Scholar 

  • Van den Bosch P, van Beusekom O, Buisman C, Janssen A (2007) Sulfide oxidation at halo-alkaline conditions in a fed-batch bioreactor. Biotechnol Bioeng 97(5):1053–1063

    Article  Google Scholar 

  • Van Den Bosch P, Sorokin D, Buisman C, Janssen A (2008) The effect of pH on thiosulfate formation in a biotechnological process for the removal of hydrogen sulfide from gas streams. Environ Sci Technol 42:2637–2642

    Article  Google Scholar 

  • van den Ende F, van Gemerden H (1993) Sulfide oxidation under oxygen limitation by a Thiobacillus thioparus isolated from a marine microbial mat. FEMS Microbiol Ecol 13:69–78

    Article  Google Scholar 

  • van Aswegen P, van Niekerk J, Olivier W (2007) The BIOXTM process for the treatment of refractory gold concentrates. In: Rawlings D, Johnson D (eds) Biomining. Springer-Verlag, Berlin Heidelberg, pp 1–33

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vestola E et al (2010) Acid bioleaching of solid waste materials from copper, steel and recycling industries. Hydromet 103(1–4):74–794

    Article  CAS  Google Scholar 

  • Vijayakumar S (2012) Potential applications of cyanobacteria in industrial effluents-a review. J Bioremediat Biodegradation 154(3). https://doi.org/10.4172/2155-6199.1000154

  • Visscher P, Taylor B (1993) A new mechanism for the aerobic catabolism of dimethyl sulfide. Appl Environ Microbiol 59:3784–3789

    Article  CAS  Google Scholar 

  • Wang R (2002) Two’s company, three’s a crowd: Can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    Article  CAS  Google Scholar 

  • Wang J et al (2019) A novel biological sulfur reduction process for mercury-contaminated wastewater treatment. Water Res 160:288–295

    Article  CAS  Google Scholar 

  • Wan R, Levier K (2003) Solution chemistry factors for gold thiosulfate heap leaching. Int J Miner Process 72:311–322

    Article  CAS  Google Scholar 

  • West-Sells P, Ji J, Hackl R (2003) A process for counteracting the detrimental effect of tetrathionate on resin gold adsorption from thiosulfate leachates. Warrendale, TMS, pp 245–256

    Google Scholar 

  • Xia Y, Lü C, Hou N (2017) Sulfide production and oxidation by heterotrophic bacteria under aerobic conditions. ISME J 11:2754–2766

    Article  CAS  Google Scholar 

  • Xie F, Chen J, Wang J, Wang W (2021) Review of gold leaching in thiosulfate-based solutions. Trans Nonferrous Met Soc China 31(11):3506–3529

    Article  CAS  Google Scholar 

  • Xin Y et al (2020) The heterotrophic bacterium cupriavidus pinatubonensis JMP134 oxidizes sulfide to sulfate with thiosulfate as a key intermediate. Appl Environ Microbiol 86(22):e01835–e01820

    Article  CAS  Google Scholar 

  • Xin Y, Liu H, Cui F, Liu H, Xun L (2016) Recombinant Escherichia coli with sulfide:quinone oxidoreductase and persulfide dioxygenase rapidly oxidises sulfide to sulfite and thiosulfate via a new pathway. Sci Rep 12:5123–5136

    Google Scholar 

  • Xu B et al (2017) A review of thiosulfate leaching of gold: focus on thiosulfate consumption and gold recovery from pregnant solution. Metals 7(6):222

    Article  Google Scholar 

  • Xu X, Chen C, Guo H (2016) Characterization of a newly isolated strain Pseudomonas sp. C27 for sulfide oxidation. Reaction kinetics and stoichiometry. Sci Rep 6:21032

    Article  CAS  Google Scholar 

  • Yin H et al (2014) Whole-genome sequencing reveals novel insights into sulfur oxidation in the extremophile Acidithiobacillus thiooxidans. BMC Microbiol 14:179

    Article  Google Scholar 

  • Yong X, Schoonen M (1995) The stability of thiosulfate in the presence of pyrite in low-temperature aqueous solutions. Geochim Cosmochim Acta 59(22):4605–4622

    Article  Google Scholar 

  • Yoo K, Kim H (2012) Development of ammoniacal leaching processes; a review. J Korean Inst Resour Recycling 21(5):3–17

    Article  Google Scholar 

  • Zhang Y et al (2020) Complete genome sequence of acidithiobacillus ferrooxidans YNTRS-40, a strain of the ferrous iron- and sulfur-oxidizing acidophile. Microorganisms 8(1):2

    Article  CAS  Google Scholar 

  • Zhang H, Jeffery M (2010) A kinetic study of rearrangement and degradation reactions of tetrathionate and trithionate in near-neutral solutions. Inorg Chem 49:10273–10282

    Article  CAS  Google Scholar 

  • Zhang X, Senanayake G (2016) A review of ammoniacal thiosulfate leaching of gold: an update useful for further research in non-cyanide gold lixiviants. Miner Process Extr Metall Rev 37(6):385–411

    Article  CAS  Google Scholar 

  • Zhang M, Dugbartey G, Juriasingani S, Sener A (2021) Hydrogen sulfide metabolite, sodium thiosulfate: clinical applications and underlying molecular mechanisms. Int J Mol Sci 22(12):6452

    Article  CAS  Google Scholar 

  • Zhao F et al (2008) Activated carbon cloth as anode for sulfate removal in a microbial fuel cell. Environ Sci Technol 42(13):4971–4976

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) and Newmont Corp. through the Collaborative Research and Development Grant Program CRDPJ.523048–17.

Author information

Authors and Affiliations

Authors

Contributions

James McNeice performed the literature search, data analysis, and drafted the work. Harshit Mahandra critically revised and edited the work. Ahmad Ghahreman provided the funding and supervision for James McNeice and edited the work.

Corresponding author

Correspondence to James McNeice.

Ethics declarations

Conflict of interest

The authors have no competing interests to declare that are relevant to the content of this article.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McNeice, J., Mahandra, H. & Ghahreman, A. Biogenesis of thiosulfate in microorganisms and its applications for sustainable metal extraction. Rev Environ Sci Biotechnol 21, 993–1015 (2022). https://doi.org/10.1007/s11157-022-09630-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-022-09630-3

Keywords

Navigation