{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T18:50:56Z","timestamp":1789152656652,"version":"build-2803163510"},"reference-count":61,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2024,12,23]],"date-time":"2024-12-23T00:00:00Z","timestamp":1734912000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Higher Education of the Russian Federation"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>This paper presents the results of microbial corrosion tests on M0-grade copper under conditions simulating a geological repository for radioactive waste at the Yeniseisky site (Krasnoyarsk Krai, Russia). The work used a microbial community sampled from a depth of 450 m and stimulated with glucose, hydrogen and sulfate under anaerobic conditions. It was shown that the maximum corrosion rate, reaching 9.8 \u00b5m\/y, was achieved with the addition of sulfate (1 g\/L) with the participation of microorganisms from the families Desulfomicrobiaceae, Desulfovibrionaceae and Desulfuromonadaceae. It was noted that the most important factor leading to copper corrosion was the accumulation of hydrogen sulfide during the activation of sulfate-reducing microorganisms of the genera Desulfomicrobium, Desulfovibrio and Desulfuromonas. During the development of the microbial community under these conditions, the content of copper can have a significant toxic effect at a concentration of more than 250 mg\/L.<\/jats:p>","DOI":"10.3390\/biology13121086","type":"journal-article","created":{"date-parts":[[2024,12,23]],"date-time":"2024-12-23T02:39:56Z","timestamp":1734921596000},"page":"1086","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Microbial Corrosion of Copper Under Conditions Simulating Deep Radioactive Waste Disposal"],"prefix":"10.3390","volume":"13","author":[{"given":"Elena","family":"Abramova","sequence":"first","affiliation":[{"name":"Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, 119071 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0661-2169","authenticated-orcid":false,"given":"Natalia","family":"Shapagina","sequence":"additional","affiliation":[{"name":"Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, 119071 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8018-6287","authenticated-orcid":false,"given":"Grigoriy","family":"Artemiev","sequence":"additional","affiliation":[{"name":"Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, 119071 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6920-4659","authenticated-orcid":false,"given":"Alexey","family":"Safonov","sequence":"additional","affiliation":[{"name":"Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, 119071 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Apted, M.J., and Ahn, J. (2017). Geological Repository Systems for Safe Disposal of Spent Nuclear Fuels and Radioactive Waste, Woodhead Publishing. [1st ed.].","DOI":"10.1016\/B978-0-08-100642-9.00001-3"},{"key":"ref_2","first-page":"7","article-title":"Geological disposal of radioactive wastes\u2013concept, status and trends","volume":"32","author":"Chapman","year":"2006","journal-title":"J. Iber. Geol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jnucmat.2008.06.001","article-title":"Overview of European concepts for high-level waste and spent fuel disposal with special reference waste container corrosion","volume":"379","author":"Bennett","year":"2008","journal-title":"J. Nucl. Mater."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1016\/j.apgeochem.2008.02.014","article-title":"Site descriptive modelling during characterization for a geological repository for nuclear waste in Sweden","volume":"23","author":"Andersson","year":"2008","journal-title":"Appl. Geochem."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1007\/s11665-014-1332-x","article-title":"Effect of mixed-species biofilm on copper surfaces in cooling water system","volume":"24","author":"Cansever","year":"2015","journal-title":"J. Mater. Eng. Perform."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"C63","DOI":"10.1149\/1.2772085","article-title":"Corrosion of Copper by Water","volume":"10","author":"Hultquist","year":"2007","journal-title":"Electrochem. Solid-State Lett."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1108\/00035590410512735","article-title":"Pitting corrosion of copper in chloride solutions","volume":"51","author":"Sherif","year":"2004","journal-title":"Anti-Corros. Method. M"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"389","DOI":"10.5006\/1.3280482","article-title":"Corrosion mechanisms and products of copper in aqueous solutions at various pH values","volume":"53","author":"Feng","year":"1997","journal-title":"Corrosion"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1080\/1478422X.2016.1271161","article-title":"Effect of chloride on Cu corrosion in anaerobic sulphide solutions","volume":"52","author":"Chen","year":"2017","journal-title":"Corros. Eng. Sci. Technol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1016\/j.corsci.2014.07.009","article-title":"Corrosion of copper and steel alloys in a simulated underground storage-tank sump environment containing acid-producing bacteria","volume":"87","author":"Sowards","year":"2014","journal-title":"Corros. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.ibiod.2007.06.001","article-title":"Microbiologically induced corrosion of copper pipes in low-pH water","volume":"61","author":"Reyes","year":"2008","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Ruiz-Fresneda, M.A., Martinez-Moreno, M.F., Povedano-Priego, C., Morales-Hidalgo, M., Jroundi, F., and Merroun, M.L. (2023). Impact of microbial processes on the safety of deep geological repositories for radioactive waste. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1134078"},{"key":"ref_13","unstructured":"(2017). \u201cExamples of Some Materials Vulnerable to MIC\u201d in Microbiologically Influenced Corrosion-An Engineering Insight, Springer. [2nd ed.]. Chapter 8."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"59","DOI":"10.3390\/cmd1010005","article-title":"An electrochemist perspective of microbiologically influenced corrosion","volume":"1","author":"Blackwood","year":"2018","journal-title":"Corros. Mater. Degrad."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.corsci.2018.08.055","article-title":"Investigation of the mechanism and characteristics of copper corrosion by sulfate reducing bacteria","volume":"144","author":"Dou","year":"2018","journal-title":"Corros. Sci."},{"key":"ref_16","first-page":"1","article-title":"Microbiologically influenced corrosion of copper and its alloys\u2014A review","volume":"84","author":"Javed","year":"2016","journal-title":"Corros. Prev. Control."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.copbio.2004.05.001","article-title":"Biocorrosion: Towards understanding interactions between biofilms and metals","volume":"15","author":"Beech","year":"2004","journal-title":"Curr. Opin. Biotechnol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1016\/j.apsusc.2016.11.086","article-title":"Corrosion of copper in oxygen-deficient groundwater with and without deep bedrock micro-organisms: Characterisation of microbial communities and surface processes","volume":"396","author":"Rajala","year":"2017","journal-title":"Appl. Surf. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1515\/corrrev-2019-0108","article-title":"Microbiologically influenced corrosion: A review of the studies conducted on buried pipelines","volume":"38","author":"Spark","year":"2020","journal-title":"Corros. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"108993","DOI":"10.1016\/j.corsci.2020.108993","article-title":"Distinguishing two different microbiologically influenced corrosion (MIC) mechanisms using an electron mediator and hydrogen evolution detection","volume":"177","author":"Wang","year":"2020","journal-title":"Corros. Sci."},{"key":"ref_21","unstructured":"Puigdomenech, I., and Taxen, C. (2000). Thermodynamic Data For Copper. Implications for the Corrosion of Copper Under Repository Conditions, Swedish Nuclear Fuel and Waste Management Company. SKB-TR-00-13."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1080\/08927019609378310","article-title":"Effects of arthrobacter sp., acidovorax delafieldii, and bacillus megaterium colonisation on copper solvency in a laboratory reactor","volume":"9","author":"Davidson","year":"2009","journal-title":"J. Bioadhesion Biofilm Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Chen, Z., Dou, W., Chen, S., Pu, Y., and Xu, Z. (2022). Influence of nutrition on Cu corrosion by Desulfovibrio vulgaris in anaerobic environment. Bioelectrochemistry, 144.","DOI":"10.1016\/j.bioelechem.2021.108040"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Amendola, R., and Acharjee, A. (2022). Microbiologically Influenced Corrosion of Copper and Its Alloys in Anaerobic Aqueous Environments: A Review. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.806688"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"253","DOI":"10.2113\/gselements.12.4.253","article-title":"The Russian strategy of using crystalline rock as a repository for nuclear waste","volume":"12","author":"Laverov","year":"2016","journal-title":"Elements"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1007\/s10666-023-09893-2","article-title":"Radionuclide Migration From an Underground Radioactive Waste Repository Under the Influence of Tectonic Fault Emergence: The Nizhnekanskiy Massif (Siberia, Russia) Example","volume":"28","author":"Malkovsky","year":"2023","journal-title":"Environ. Model. Assess."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"85","DOI":"10.25283\/2587-9707-2022-2-85-99","article-title":"Borehole RW Disposal Concept and Prospects of its Implementation in Russia","volume":"2","author":"Kochkin","year":"2022","journal-title":"Radioact. Waste"},{"key":"ref_28","unstructured":"Gupalo, T.A. (2003). Development of a Comprehensive Plan for Scientific Research, Exploration, and Design: Creation of an Underground Radioactive Waste Isolation Facility at the Nizhnekansky Rock Massif, VNIPIpromtechnologii. ISTC 2377 Project Report."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"106931","DOI":"10.1016\/j.enggeo.2022.106931","article-title":"Biological factors affecting the evolution of safety barrier materials in the yeniseisky deep geological repository","volume":"312","author":"Abramova","year":"2023","journal-title":"Eng. Geol."},{"key":"ref_30","unstructured":"(2017). Standard Test Method for Evaluating Degree of Rusting on Painted Steel Surfaces (Standard No. ASTM D610-01). SSPC-VIS-2."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"124491a","DOI":"10.1016\/j.envpol.2024.124491","article-title":"Microbial influence in Spanish bentonite slurry microcosms: Unveiling a-year long geochemical evolution and early-stage copper corrosion related to nuclear waste repositories","volume":"358","author":"Mumford","year":"2024","journal-title":"Environ. Pollut."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"7496","DOI":"10.1128\/AEM.02413-15","article-title":"Anaerobic growth of Corynebacterium glutamicum via mixed-acid fermentation","volume":"81","author":"Michel","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"131940","DOI":"10.1016\/j.jhazmat.2023.131940","article-title":"Impact of compacted bentonite microbial community on the clay mineralogy and copper canister corrosion: A multidisciplinary approach in view of a safe Deep Geological Repository of nuclear wastes","volume":"458","author":"Mumford","year":"2023","journal-title":"J. Hazard. Mater."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/BF00689356","article-title":"Inhibition of methanogenesis by sulphate reducing bacteria competing for transferred hydrogen","volume":"117","author":"Abram","year":"1978","journal-title":"Arch. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4326","DOI":"10.1111\/1462-2920.15614","article-title":"Genomic characterization of three novel Desulfobacterota classes expand the metabolic and phylogenetic diversity of the phylum","volume":"23","author":"Murphy","year":"2021","journal-title":"Environ. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"115951","DOI":"10.1016\/j.watres.2020.115951","article-title":"Corroding copper and steel exposed to intermittently flowing tap water promote biofilm formation and growth of Legionella pneumophila","volume":"183","author":"Veenendaal","year":"2020","journal-title":"Water Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.ibiod.2014.04.008","article-title":"Microbial community analysis of anaerobic bio-corrosion in different ORP profiles","volume":"95","author":"Chang","year":"2014","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.clay.2019.04.025","article-title":"Interactions between microorganisms and clay minerals: New insights and broader applications","volume":"177","author":"Li","year":"2019","journal-title":"Appl. Clay Sci."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Abramova, E., Popova, N., Artemiev, G., Zharkova, V., Zakharova, E., and Safonov, A. (2022). Characteristics and Rates of Microbial Processes in Clays of Different Mineral and Elemental Composition in Relation to Safety Prediction for ESB Clay Materials. Appl. Sci., 12.","DOI":"10.3390\/app12041843"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Ershov, B. (2022). Natural radioactivity and chemical evolution on the early earth: Prebiotic chemistry and oxygenation. Molecules, 27.","DOI":"10.3390\/molecules27238584"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1089\/ast.2007.0150","article-title":"Radiolytic Hydrogen and Microbial Respiration in Subsurface Sediments","volume":"7","author":"Blair","year":"2007","journal-title":"Astrobiology"},{"key":"ref_42","first-page":"820172","article-title":"Impact of \u03b3-irradiation on biofilm-formation by corrosion-relevant heterotrophic bacteria","volume":"5","author":"Boretska","year":"2020","journal-title":"Nauk. Dopovidi NUBiP Ukr."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"\u010cernou\u0161ek, T., \u0160evc\u016f, A., Shrestha, R., Steinov\u00e1, J., Kokinda, J., and Vizelkov\u00e1, K. (2021). Microbially influenced corrosion of container material. The Microbiology of Nuclear Waste Disposal, Elsevier.","DOI":"10.1016\/B978-0-12-818695-4.00006-X"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1080\/09593330.2017.1310934","article-title":"Evaluation of methanogenic microbial electrolysis cells under closed\/open circuit operations","volume":"39","author":"Luo","year":"2018","journal-title":"Environ. Technol."},{"key":"ref_45","first-page":"319","article-title":"Hydrogenophaga, a new genus of hydrogen-oxidizing bacteria that includes Hydrogenophaga flava comb. nov. (formerly Pseudomonas flava), Hydrogenophaga palleronii (formerly Pseudomonas palleronii), Hydrogenophaga pseudoflava (formerly Pseudomonas pseudoflava and Pseudomonas carboxydoflava), and Hydrogenophaga taeniospiralis (Formerly Pseudomonas taeniospiralis)","volume":"39","author":"Willems","year":"1989","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1007\/BF00549357","article-title":"Physiology of a Methanobacterium strain AZ","volume":"111","author":"Zehnder","year":"1977","journal-title":"Arch. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2048","DOI":"10.1039\/C5EE00866B","article-title":"Does it have to be carbon? Metal anodes in microbial fuel cells and related bioelectrochemical systems","volume":"8","author":"Baudler","year":"2015","journal-title":"Energy Environ. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3755","DOI":"10.1016\/S0013-4686(01)00657-0","article-title":"Initial and Later Stages of Anodic Oxide Formation on Cu, Chemical Aspects, Structure and Electronic Properties","volume":"46","author":"Strehblow","year":"2001","journal-title":"Electrochim. Acta"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1134\/S2070205123700260","article-title":"Physicochemical Features of Biocorrosion of Copper and Products Based on It by Microfungi","volume":"59","author":"Belov","year":"2023","journal-title":"Prot. Met. Phys. Chem. Surf."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1149\/1.2425445","article-title":"Copper Corrosion: I. Thermodynamic Aspects","volume":"109","author":"Ives","year":"1962","journal-title":"J. Electrochem. Soc."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1149\/1.2425446","article-title":"Copper Corrosion: II. Kinetic Studies","volume":"109","author":"Ives","year":"1962","journal-title":"J. Electrochem. Soc."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1149\/1.2425448","article-title":"Copper Corrosion: IV. The Effects of Saline Additions","volume":"109","author":"Ives","year":"1962","journal-title":"J. Electrochem. Soc."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1690","DOI":"10.1002\/maco.202313757","article-title":"The transition from used fuel container corrosion under oxic conditions to corrosion in an anoxic environment","volume":"74","author":"Guo","year":"2023","journal-title":"Mater. Corros."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Dou, W., Pu, Y., Han, X., Song, Y., Chen, S., and Gu, T. (2020). Corrosion of Cu by a sulfate reducing bacterium in anaerobic vials with different headspace volumes. Bioelectrochemistry, 133.","DOI":"10.1016\/j.bioelechem.2020.107478"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"142117","DOI":"10.1016\/j.jclepro.2024.142117","article-title":"A new perspective on the mechanism of swift corrosion perforation of copper in solutions containing sulfate-reducing bacteria","volume":"451","author":"Qian","year":"2024","journal-title":"J. Clean. Prod."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1080\/1478422X.2017.1296224","article-title":"Insights from post-test examination of three packages from the MiniCan test series of coppercast iron canisters for geological disposal of spent nuclear fuel: Impact of the presence and density of bentonite clay","volume":"52","author":"Johansson","year":"2017","journal-title":"Corros. Eng. Sci. Technol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1002\/bit.10575","article-title":"Quantification of toxic and inhibitory impact of copper and zinc on mixed cultures of sulfate-reducing bacteria","volume":"82","author":"Utgikar","year":"2003","journal-title":"Biotechnol. Bioeng."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1111\/j.1574-6976.1994.tb00083.x","article-title":"Copper resistance mechanisms in bacteria and fungi","volume":"14","author":"Cervantes","year":"1994","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"271","DOI":"10.2113\/gsecongeo.59.2.271","article-title":"Syngenesis of sulfide ores; sulfate-reducing bacteria and copper toxicity","volume":"59","author":"Temple","year":"1964","journal-title":"Econ. Geol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1007\/s11434-011-4397-z","article-title":"Effects of sulfide on sulfate reducing bacteria in response to Cu(II), Hg(II) and Cr(VI) toxicity","volume":"56","author":"Sheng","year":"2011","journal-title":"Chin. Sci. Bull."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1134\/S0003683822090022","article-title":"Microbial Processes in Engineering Clay Materials and Biocidal Additives to Prevent them","volume":"58","author":"Abramova","year":"2022","journal-title":"Appl. Biochem. Microbiol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/12\/1086\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:58:07Z","timestamp":1760115487000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/12\/1086"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,23]]},"references-count":61,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["biology13121086"],"URL":"https:\/\/doi.org\/10.3390\/biology13121086","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,23]]}}}