Exploration of bacterial strains with bioremediation potential for mercury and cyanide from mine tailings in “San Carlos de las Minas, Ecuador”

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Abstract

Ecuador is a developing country that relies on mining as a significant source of economic income every year; however, there needs to be more studies on the soil pollution caused by mining over time. Biological remediation as an alternative to the use of physical and chemical methods offers a more cost-effective and environmentally friendly means to counteract the negative impacts that the presence of heavy metals in mining tailings soils can cause. This study focused on soil sampling from the mining tailings of the San Carlos de las Minas sector, in the Zamora Chinchipe province in Ecuador, to find potential bacterial strains that can degrade two specific contaminants, mercury (Hg) and cyanide (CN^-). For this purpose, 68 soil subsamples were collected. pH, electrical conductivity, moisture, and the concentration of the contaminants were analyzed and measured. The initial concentration of CN^- was 0.14 mg/kg, and of Hg was 88.76 mg/kg. From the soil samples, eight bacterial strains were isolated, characterized at macroscopic and microscopic levels, and identified at the molecular level. The bacteria were then subjected to degradability tests for CN^- and Hg, obtaining interesting results. The degradation capacity of CN^- stood out for the strains Micrococcus aloeverae and Pseudomonas alcaliphila, and for the degradation of Hg, the strains Hydrogenophaga laconesensis and Micrococcus aloeverae were highlighted, achieving degradation percentages of up to 98.80%. These results emphasize the discovery of these bacterial species with potential use in cyanide and mercury remediation processes.

Keywords

bacterial bioremediation / contamination / mine tailings / cyanide / mercury

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References

[1] Betancourt O, Narváez A, Roulet M (2005) Small-scale gold mining in the Puyango River basin, southern Ecuador: A study of environmental impacts and human exposures. Ecohealth 2: 323-332. https://doi.org/10.1007/s10393-005-8462-4

[2] Counter SA, Buchanan LH, Ortega F, et al. (2002) Elevated blood mercury and neuro-otological observations in children of the Ecuadorian gold mines. J Toxicol Env Heal A 65: 149-163. https://doi.org/10.1080/152873902753396785

[3] Conde M (2017) Resistance to mining. A Review. Ecol Econ 132: 80-90. https://doi.org/10.1016/j.ecolecon.2016.08.025

[4] Hedrick DB, Peacock A, Stephen JR, et al. (2000) Measuring soil microbial community diversity using polar lipid fatty acid and denaturing gradient gel electrophoresis data. J Microbiol Meth 41: 235-248. https://doi.org/10.1016/S0167-7012(00)00157-3

[5] Chamba I, Rosado D, Kalinhoff C, et al. (2017) Erato polymnioides-A novel Hg hyperaccumulator plant in ecuadorian rainforest acid soils with potential of microbe-associated phytoremediation. Chemosphere 188: 633-641. https://doi.org/10.1016/j.chemosphere.2017.08.160

[6] Jing X, Lu T, Sun F, et al. (2023) Microbial transformation to remediate mercury pollution: Strains isolation and laboratory study. Int J Environ Sci Te 20: 3039-3048. https://doi.org/10.1007/s13762-022-04158-z

[7] Kannan SK, Mahadevan S, Krishnamoorthy R (2006) Characterization of a mercury-reducing Bacillus cereus strain isolated from the Pulicat Lake sediments, south east coast of India. Arch Microbiol 185: 202-211. https://doi.org/10.1007/s00203-006-0088-6

[8] Deng S, Zhang X, Zhu Y, et al. (2024) Recent advances in phyto-combined remediation of heavy metal pollution in soil. Biotechnol Adv 72. https://doi.org/10.1016/j.biotechadv.2024.108337

[9] Chen L, Zhang X, Zhang M, et al. (2022) Removal of heavy-metal pollutants by white rot fungi: Mechanisms, achievements, and perspectives. J Clean Prod 354. https://doi.org/10.1016/j.jclepro.2022.131681

[10] Purchase MDW, Castillo J, Arias AG, et al. (2024) First insight into the natural biodegradation of cyanide in a gold tailings environment enriched in cyanide compounds. Sci Total Environ 906: 167174. https://doi.org/10.1016/j.scitotenv.2023.167174

[11] Jabbar KA, Akhter G, Gabriel HF, et al. (2020) Anthropogenic effects of coal mining on ecological resources of the Central Indus basin, Pakistan. Int J Env Res Pub He 17: 1255. https://doi.org/10.3390/ijerph17041255

[12] Boerleider RZ, Roeleveld N, Scheepers PTJ (2017) Human biological monitoring of mercury for exposure assessment. AIMS Environ Sci 4: 251-276. https://doi.org/10.3934/environsci.2017.2.251

[13] Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5: 240-245. https://doi.org/10.1016/S1369-5274(02)00324-7

[14] Gao X, Wei M, Zhang X, et al. (2024) Copper removal from aqueous solutions by white rot fungus Pleurotus ostreatus GEMB-PO1 and its potential in co-remediation of copper and organic pollutants. Bioresource Technol 395. https://doi.org/10.1016/j.biortech.2024.130337

[15] Cao S, Duan M, Zhang X, et al. (2024) Bacterial community structure analysis of sludge from Taozi Lake and isolation of an efficient 17β-Estradiol (E2) degrading strain Sphingobacterium sp. GEMB-CSS-01. Chemosphere 355: 141806. https://doi.org/10.1016/j.chemosphere.2024.141806

[16] Narayanan M, Devarajan N, He Z, et al. (2020) Assessment of microbial diversity and enumeration of metal tolerant autochthonous bacteria from tailings of magnesite and bauxite mines. Mater Today Proc 33: 4391-4401. https://doi.org/10.1016/j.matpr.2020.07.652

[17] Mungla G, Facknath S, Lalljee B (2022) Assessing the potential of mechanical aeration combined with bioremediation process in soils and coastal sediments impacted by heavy metals. AIMS Environ Sci 9: 692-707. https://doi.org/10.3934/environsci.2022039

[18] Chen SC, Lin WH, Chien CC, et al. (2018) Development of a two-stage biotransformation system for mercury-contaminated soil remediation. Chemosphere 200: 266-273. https://doi.org/10.1016/j.chemosphere.2018.02.085

[19] Rodríguez MB, Piedra CAJ, Chiocchetti GDME, et al. (2016) The use of Saccharomyces cerevisiae for reducing mercury bioaccessibility. Toxicol Lett 258: S159. https://doi.org/10.1016/j.toxlet.2016.06.1604

[20] Ignatavičius G, Unsal MH, Busher PE, et al. (2022) Geochemistry of mercury in soils and water sediments. AIMS Environ Sci 9: 261-281. https://doi.org/10.3934/environsci.2022019

[21] Rivera AA, Hoyos SG, Buitrón G, et al. (2021) Biological treatment for the degradation of cyanide: A review. J Mater Res Technol 12: 1418-1433. https://doi.org/10.1016/j.jmrt.2021.03.030

[22] Almagro VML, Huertas MJ, Luque MM, et al. (2005) Bacterial degradation of cyanide and its metal complexes under alkaline conditions. Appl Environ Microb 71: 940-947. https://doi.org/10.1128/AEM.71.2.940-947.2005

[23] Standard Practices for Preserving and Transporting Soil Samples, ASTM International (2009) Ingenieía Civil en el Slavador. ASTM Designation D 4220-00, 2009. Available from: https://worldwidestandard.net/wp-content/uploads/2019/07/D-4220.pdf.

[24] Ministerio del Ambiente Ecuador (2015) Edición Especial N^o 387-Registro Oficial. 387: 17-18.

[25] EPA (2004) Method 9045D-soil and waste pH, EPA D.pdf, 2004. Available from: https://www.epa.gov/sites/default/files/2015-12/documents/9045d.pdf.

[26] EPA (1996) Method 9050A specific conductance, EPA, 1996. Available from: https://www.epa.gov/sites/default/files/2015-12/documents/9050a.pdf.

[27] American public health association (1997) By Authority Of. Available from: https://law.resource.org/pub/us/cfr/ibr/002/apha.method.4500-cn.1992.pdf.

[28] Yalkowsky S, He Y, Jain P (2010) Chemical abstracts service registry number (RN), Handbook of Aqueous Solubility Data , 2Eds., CRC Press, 1575-1608. https://doi.org/10.1201/EBK1439802458-6

[29] Tantray JA, Mansoor S, Wani RFC, et al. (2023) Gram staining of bacteria, Basic Life Sci Methods . https://doi.org/10.1016/B978-0-443-19174-9.00043-X

[30] Shields P, Cathcart L (2016) Motility test medium protocol. Am Soc Microbiol 214: 215.

[31] Ki JS, Zhang W, Qian PY (2009) Discovery of marine bacillus species by 16S rRNA and rpoB comparisons and their usefulness for species identification. J Microbiol Meth 77: 48-57. https://doi.org/10.1016/j.mimet.2009.01.003

[32] Polo CPL, Lebonguy AA, Boumba AEL, et al. (2022) Bacterial community diversity of a Congolese traditional fermented food, “Pandé”, revealed by Illumina Miseq^TM Sequencing of 16S rRNA Gene. Open J Appl Sci 12: 387-405. https://doi.org/10.4236/ojapps.2022.123027

[33] Gürtekin G, Aydar E (2023) Quantitative Mineralogy in characterization of historical tailings: A case from the abandoned Balya Pb-Zn mine, Western Turkey. Nat Resour Res 32: 195-212. https://doi.org/10.1007/s11053-022-10128-6

[34] Dinis ML, Fiúza A, Futuro A, et al. (2020) Characterization of a mine legacy site: an approach for environmental management and metals recovery. Environ Sci Pollut R 27: 10103-10114. https://doi.org/10.1007/s11356-019-06987-x

[35] Kagambega N, Sam U, Ouedraogo M (2023) Artisanal mining and soil quality in the Sudano-Sahelian climate: Case of the artisanal mining site of Yimiougou in Burkina Faso, West Africa. J Environ Prot 14: 1-15. https://doi.org/10.4236/jep.2023.141001

[36] Esshaimi M, EI Gharmali A, Berkhis F, et al. (2017) Speciation of heavy metals in the soil and the mining residues, in the zinclead Sidi Bou Othmane abandoned mine in Marrakech area. Linnaeus Eco-Tech 975-985. https://doi.org/10.15626/Eco-Tech.2010.102

[37] Nkongolo KK, Spiers G, Beckett P, et al. (2022) Inside old reclaimed mine tailings in Northern Ontario, Canada: A microbial perspective. Ecol Genet Genomics 23: 100118. https://doi.org/10.1016/j.egg.2022.100118

[38] Seney CS, Bridges CC, Aljic S, et al. (2020) Reaction of cyanide with Hg 0-contaminated gold mining tailings produces soluble mercuric cyanide complexes. Chem Res Toxicol 33: 2834-2844. https://doi.org/10.1021/acs.chemrestox.0c00211

[39] Johnson CA (2015) The fate of cyanide in leach wastes at gold mines: An environmental perspective. Appl Geochem 57: 194-205. https://doi.org/10.1016/j.apgeochem.2014.05.023

[40] Zhang C, Wang X, Jiang S, et al. (2021) Heavy metal pollution caused by cyanide gold leaching: A case study of gold tailings in central China. Environ Sci Pollut R 28: 29231-29240. https://doi.org/10.1007/s11356-021-12728-w

[41] Marshall BG, Veiga MM, da Silva HAM, et al. (2020) Cyanide contamination of the Puyango-Tumbes River caused by artisanal gold mining in Portovelo-Zaruma, Ecuador. Curr Env Hlth Rep 7: 303-310. https://doi.org/10.1007/s40572-020-00276-3

[42] Miserendino RA, Bergquist BA, Adler SE, et al. (2013) Challenges to measuring, monitoring, and addressing the cumulative impacts of artisanal and small-scale gold mining in Ecuador. Resour Policy 38: 713-722. https://doi.org/10.1016/j.resourpol.2013.03.007

[43] Yoon S, Kim DM, Yu S, et al. (2023) Metal(loid)-specific sources and distribution mechanisms of riverside soil contamination near an abandoned gold mine in Mongolia. J Hazard Mater 443: 130294. https://doi.org/10.1016/j.jhazmat.2022.130294

[44] Laker MC, Nortjé GP (2020) Review of existing knowledge on subsurface soil compaction in South Africa. Adv Agron 143-197. https://doi.org/10.1016/bs.agron.2020.02.004

[45] Rachman RM, Mangidi U, Trihadiningrum Y (2023) Solidification and stabilization of mercury-contaminated tailings in artisanal and small-scale gold mining using tras soil. J Degr Min Lands Manag 10: 4575. https://doi.org/10.15243/jdmlm.2023.104.4575

[46] Requelme MER, Ramos JFF, Angélica RS, et al. (2003) Assessment of Hg-contamination in soils and stream sediments in the mineral district of Nambija, Ecuadorian Amazon (example of an impacted area affected by artisanal gold mining). Appl Geochem 18: 371-381. https://doi.org/10.1016/S0883-2927(02)00088-4

[47] Estévez DR, Jácome GSY, Navarrete H (2023) Non-essential metal contamination in Ecuadorian agricultural production: A critical review. J Food Compos Anal 115: 104932. https://doi.org/10.1016/j.jfca.2022.104932

[48] Tapia CC, Vasco DC, Galarza AG, et al. (2023) Bioelectricity production from anaerobically treated leachate in microbial fuel cell using Delftia acidovorans spp. AIMS Environ Sci 10: 847-867. https://doi.org/10.3934/environsci.2023046

[49] Mishra S, Lin Z, Pang S, et al. (2021) Biosurfactant is a powerful tool for the bioremediation of heavy metals from contaminated soils. J Hazard Mater 418. https://doi.org/10.1016/j.jhazmat.2021.126253

[50] Mishra S, Chen S, Saratale GD, et al. (2021) Reduction of hexavalent chromium by Microbacterium paraoxydans isolated from tannery wastewater and characterization of its reduced products. J Water Process Eng 39. https://doi.org/10.1016/j.jwpe.2020.101748

[51] Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173: 170-177. https://doi.org/10.1007/s002039900127

[52] Park JM, Sewell BT, Benedik MJ (2017) Cyanide bioremediation: The potential of engineered nitrilases. Appl Microbiol Biot 101: 3029-3042. https://doi.org/10.1007/s00253-017-8204-x

[53] Almagro VML, Cabello P, Sáez LP, et al. (2018) Exploring anaerobic environments for cyanide and cyano-derivatives microbial degradation. Appl Microbiol Biot 102: 1067-1074. https://doi.org/10.1007/s00253-017-8678-6

[54] Mahendran R, Bs S, Thandeeswaran M, et al. (2020) Microbial (Enzymatic) degradation of cyanide to produce pterins as cofactors. Curr Microbiol 77: 578-587. https://doi.org/10.1007/s00284-019-01694-9

[55] Saim AK, Adu PCO, Amankwah RK, et al. (2021) Review of catalytic activities of biosynthesized metallic nanoparticles in wastewater treatment. Environ Technol Rev 10: 111-130. https://doi.org/10.1080/21622515.2021.1893831

[56] Chandrasekaran M, Paramasivan M (2024) Plant growth-promoting bacterial (PGPB) mediated degradation of hazardous pesticides: A review. Int Biodeter Biodegr 190: 105769. https://doi.org/10.1016/j.ibiod.2024.105769

[57] Qian J, Li D, Zhan G, et al. (2012) Simultaneous biodegradation of Ni-citrate complexes and removal of nickel from solutions by Pseudomonas alcaliphila. Bioresource Technol 116: 66-73. https://doi.org/10.1016/j.biortech.2012.04.017

[58] Majhi K, Let M, Halder U, et al. (2023) Copper adsorption ootentiality of bacillus stercoris GKSM6 and pseudomonas alcaliphila GKSM11 isolated from Singhbhum copper mines. Geomicrobiol J 40: 193-202. https://doi.org/10.1080/01490451.2022.2137603

[59] Mekuto L, Ntwampe SKO, Jackson VA (2015) Biodegradation of free cyanide and subsequent utilisation of biodegradation by-products by Bacillus consortia: Optimisation using response surface methodology. Environ Sci Pollut R 22: 10434-10443. https://doi.org/10.1007/s11356-015-4221-4

[60] Naguib MM, Khairalla AS, El-Gendy AO, et al. (2019) Isolation and characterization of mercury-resistant bacteria from wastewater sources in Egypt. Can J Microbiol 65: 308-321. https://doi.org/10.1139/cjm-2018-0379

[61] Matsui K, Yoshinami S, Narita M, et al. (2016) Mercury resistance transposons in Bacilli strains from different geographical regions. FEMS Microbiol Lett 363: fnw013. https://doi.org/10.1093/femsle/fnw013

[62] Chang CC, Lin LY, Zou XW, et al. (2015) Structural basis of the mercury(II)-mediated conformational switching of the dual-function transcriptional regulator MerR. Nucleic Acids Res 43: 7612-7623. https://doi.org/10.1093/nar/gkv681

[63] Sone Y, Uraguchi S, Takanezawa Y, et al. (2017) Cysteine and histidine residues are involved in Escherichia coli Tn21 MerE methylmercury transport. FEBS Open Bio 7: 1994-1999. https://doi.org/10.1002/2211-5463.12341

[64] Wahba HM, Lecoq L, Stevenson M, et al. (2016) Structural and biochemical characterization of a copper-binding mutant of the organomercurial lyase MerB: Insight into the key role of the active site aspartic acid in Hg-Carbon bond cleavage and metal binding specificity. Biochemistry 55: 1070-1081. https://doi.org/10.1021/acs.biochem.5b01298

[65] Gätjens DR, Schweizer PF, Jiménez KR, et al. (2022) Methylotrophs and hydrocarbon-degrading bacteria are key players in the microbial community of an abandoned century-old oil exploration well. Microb Ecol 83: 83-99. https://doi.org/10.1007/s00248-021-01748-1

[66] Pandit B, Moin A, Mondal A, et al. (2023) Characterization of a biofilm-forming, amylase-producing, and heavy-metal-bioremediating strain Micrococcus sp. BirBP01 isolated from oligotrophic subsurface lateritic soil. Arch Microbiol 205: 351. https://doi.org/10.1007/s00203-023-03690-x

[67] Mishra S, Lin Z, Pang S, et al. (2021) Recent advanced technologies for the characterization of xenobiotic-degrading microorganisms and microbial communities. Front Bioeng Biotech 9. https://doi.org/10.3389/fbioe.2021.632059