Abstract
Mine tailings represent a great environmental concern due to their high contents of heavy metals. Cultivation analysis of microbiota of Tarnowskie Góry (Poland) mine tailing showed the occurrence of bacteria with colony-forming units as low as 5.7 × 104 per one gram of dried substrate. Among 110 bacterial isolates identified by a combination of MALDI-TOF mass spectrometry and 16S rRNA gene sequencing, phylum Actinobacteria was dominant, followed by Firmicutes and Proteobacteria. Extremely high levels of heavy-metal resistance were observed in Arthrobacter spp., particularly for zinc (500 mg/L), lead (1500 mg/L), and cadmium (1000 mg/L). On the other hand, Staphylococcus spp. showed high tolerance to several antibiotics tested, especially ampicillin, partly due to blaZ gene presence. Due to the occurrence of antibiotic-resistant bacteria, mine tailings are not the cause of heavy-metal contamination only, but also a source of antibiotic-resistant bacteria and thus may represent a serious risk for public health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Apori OS, Hanyabui E, Asiamah YJ (2018) Remediation technology for copper contaminated soil: a review. Asian J Soil Sci 1:1–7. https://doi.org/10.9734/ASRJ/2018/45322
Aslam F, Yasmin A, Thomas T (2018) Essential gene clusters identified in Stenotrophomonas MB339 for multiple metal/antibiotic resistance and xenobiotic degradation. Curr Microbiol 75:1484–1492. https://doi.org/10.1007/s00284-018-1549-2
Ballabio C, Panagos P, Lugato E, Huang JH, Orgiazzi A, Jones A, Fernández-Ugalde O, Borrelli P, Monatanarella L (2018) Copper distribution in European topsoils: An assessment based on LUCAS soil survey. Sci Total Environ 636:282–298. https://doi.org/10.1016/j.scitotenv.2018.04.268
Beattie RE, Henke W, Campa MF, Hazen TC, McAliley LR, Campbell JH (2018) Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biol Biochem 126:57–63. https://doi.org/10.1016/j.soilbio.2018.08.011
Biswas R, Halder U, Kabiraj A, Mondal A, Bandopadhyay R (2021) Overview on the role of heavy metals tolerance on developing antibiotic resistance in both Gram-negative and Gram-positive bacteria. Arch Microbiol 203:2761–2770. https://doi.org/10.1007/s00203-021-02275-w
Bruneel O, Mghazli N, Hakkou R, Dahmani I, Maltouf AF, Sbabou L (2017) In-depth characterization of bacterial and archaeal communities present in the abandoned Kettara pyrrhotite mine tailings (Morocco). Extremophiles 21:671–685. https://doi.org/10.1007/s00792-017-0933-3
Chauhan A, Pathak A, Jaswal R, Edwards B III, Chappell D, Ball C, Garcia-Sillas R, Stothard P, Seaman J (2018) Physiological and comparative genomic analysis of Arthrobacter sp. SRS-W-1–2016 provides insights on niche adaptation for survival in uraniferous soils. Genes 9:31. https://doi.org/10.3390/genes9010031
Chen Z, Pan Ch, Chen H, Guan X, Lin Z (2016) Biomineralization of Pb(II) into Pb-hydroxyapatite induced by Bacillus cereus 12–2 isolated from Lead-Zinc mine tailings. J Hazard Mater 301:531–537. https://doi.org/10.1016/j.jhazmat.2015.09.023
Cimermanova M, Pristas P, Piknova M (2021) Biodiversity of actinomycetes from heavy metal contaminated technosols. Microorganisms 9:1635. https://doi.org/10.3390/microorganisms9081635
de Bashan LE, Hernandez JP, Bashan Y, Maier RM (2010) Bacillus pumilus ES4: Candidate plant growth-promoting bacterium to enhance establishment of plants in mine tailings. Environ Exp Bot 69:343–352. https://doi.org/10.1016/j.envexpbot.2010.04.014
Domingues VS, de Souza MA, Queiroz JADL, ALL, dos Santos VL, (2020) Diversity of metal-resistant and tensoactive-producing culturable heterotrophic bacteria isolated from a copper mine in Brazilian Amazonia. Sci Rep 10:6171. https://doi.org/10.1038/s41598-020-62780-8
Duran N, Ozer B, Duran GG, Onlen Y, Demir C (2012) Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian J Med Res 132:389–396
Gao P, Sun X, Xiao E, Xu Z, Li B, Sun W (2019) Characterization of iron-metabolizing communities in soils contaminated by acid mine drainage from an abandoned coal mine in Southwest China. Environ Sci Pollut Res 26:9585–9598. https://doi.org/10.1007/s11356-019-04336-6
Gao T, Li H, He Y, Shen Y, Li G, Li X, Chen Y, Liu Y, Li C, Ji J, X, J, Chang C, (2021) The variations of bacterial community structures in tailing soils suffering from heavy metal contaminations. Water Air Soil Pollut 232:392. https://doi.org/10.1007/s11270-021-05338-2
Gołębiewski M, Deja-Sikora E, Cichosz M, Tretyn A, Wróbel B (2014) 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microb Ecol 67:635–647. https://doi.org/10.1007/s00248-013-0344-7
Govarthanan M, Lee KJ, Cho M, Kim JS, Kamala-Kannan S, Oh BT (2013) Significance of autochthonous Bacillus sp. KK1 on biomineralization of lead in mine tailings. Chemosphere 90:2267–2272. https://doi.org/10.1016/j.chemosphere.2012.10.038
Guo H, Nasir M, Lv J, Dai Y, Gao J (2017) Understanding the variation of microbial community in heavy metals contaminated soil using high throughput sequencing. Ecotoxicol Environ Saf 144:300–306. https://doi.org/10.1016/j.ecoenv.2017.06.048
Guo X, Xie C, Wang L, Li Q, Wang Y (2019) Biodegradation of persistent environmental pollutants by Arthrobacter sp. Environ Sci Pollut Res 26:8429–8443. https://doi.org/10.1007/s11356-019-04358-0
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1)
Hanbo Z, Changqun D, Qiyong S, Weimin R, Tao S, Lizhong Ch, Zhiwei Z, Bin H (2004) Genetic and physiological diversity of phylogenetically and geographically distinct groups of Arthrobacter isolated from lead–zinc mine tailings. FEMS Microbiol Ecol 49:333–341. https://doi.org/10.1016/j.femsec.2004.04.009
Hernandez-Soriano MC, Degryse F, Lombi E, Smolders E (2012) Manganese toxicity in barley is controlled by solution manganese and soil manganese speciation. Soil Sci Soc Am J 76:399. https://doi.org/10.2136/sssaj2011.0193
Huer M, Park SJ (2019) Identification of microbial profiles in heavy-metal-contaminated soil from full-length 16S rRNA reads sequenced by a PacBio System. Microorganisms 7:357. https://doi.org/10.3390/microorganisms7090357
Jędrzejczyk-Korycinska M, Rostański A (2015) Tereny o wysokiej zawartości metali ciężkich w podłożu na Górnym Śląsku. In: Wierzbicka M (ed) Ekotoksykologia. Rośliny, gleba, metale. Wydawnictwa Uniwersytetu Warszawskiego, Warszawa, pp.175–189 (in Polish)
Komijani M, Shamabadi NS, Shahin K, Eghbalpour F, Tahsili MR, Bahram M (2021) Heavy metal pollution promotes antibiotic resistance potential in the aquatic environment. Environ Pollut 274:116569. https://doi.org/10.1016/j.envpol.2021.116569
Kowalska M, Mikulski SZ, Sidorczuk M (2017) Zinc and lead mineral resources of Poland. In Majewska A (Ed) Mineral resources of Poland as seen by Polish Geological Survey
Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: a review. Appl Geochem 108:104388. https://doi.org/10.1016/j.apgeochem.2019.104388
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lee JH (2003) Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol 69:6489–6494. https://doi.org/10.1128/AEM.69.11.6489-6494.2003
Li S, Wu J, Huo Y, Zhao X, Xue L (2021) Profiling multiple heavy metal contamination and bacterial communities surrounding an iron tailing pond in Northwest China. Sci Total Environ 752:141827. https://doi.org/10.1016/j.scitotenv.2020.141827
Li M, Do H, Ding Y, Wang Y, Zhao Ch, Wu D, Zhan Ch (2022) The isolation and characterization of Glutamicibacter DC1 to induce carbonate precipitation of some heavy metals at low-temperature. Pol J Environ Stud 31:1693–1703. https://doi.org/10.15244/pjoes/142611
Lin YB, Wang XY, Li HF, Wang NN, Wang HX, Tang M, Wei GH (2011) Streptomyces zinciresistens sp. nov., a zinc-resistant actinomycete isolated from soil from a copper and zinc mine. Int J Syst Evol Microbiol 61:616–620. https://doi.org/10.1099/ijs.0.024018-0
Mahey S, Kumar R, Sharma M, Kumar V, Bhardwaj R (2020) A critical review on toxicity of cobalt and its bioremediation strategies. SN Appl Sci 2:1279. https://doi.org/10.1007/s42452-020-3020-9
Margesin R, Plaza GA, Kasenbacher S (2011) Characterization of bacterial communities at heavy-metal-contaminated sites. Chemosphere 82:1583–1588. https://doi.org/10.1016/j.chemosphere.2010.11.056
Martens J, Smolders E (2012) Zinc. In: Alloway, B. (Eds) Heavy Metals in Soils. Environmental Pollution, Springer, Dordrecht. Pp 465–493. https://doi.org/10.1007/978-94-007-4470-7_17
Metsalu T, Vilo J, Science C, Liivi J (2015) ClustVis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res 43:566–570. https://doi.org/10.1093/nar/gkv468
Navarro-Noya YE, Hernández-Mendoza E, Morales-Jiménez J, Jan-Roblero J, Martínez-Romero E, Hernández-Rodríguez C (2012) Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Appl Soil Ecol 62:52–60. https://doi.org/10.1016/j.apsoil.2012.07.011
Niewerth H, Schuldes J, Parschat K, Kiefer P, Vorholt JA, Daniel R, Fetzner S (2012) Complete genome sequence and metabolic potential of the quinaldine-degrading bacterium Arthrobacter sp. Rue61a. BMC Genom 13:534. https://doi.org/10.1186/1471-2164-13-534
Oliveira H (2012) Chromium as an environmental pollutant: Insights on induced plant toxicity. J Bot 2012:375843. https://doi.org/10.1155/2012/375843
Olsen JE, Christensen H, Aarestrup FM (2006) Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. J Antimicrob Chemother 57:450–460. https://doi.org/10.1093/jac/dki492
Onuoha SCh, Okafor CO, Aduo BC (2016) Antibiotic and heavy metal tolerance of bacterial pathogens isolated from agricultural soil. World J Medical Sci 13:236–241. https://doi.org/10.5829/idosi.wjms.2016.236.241
Pajak M, Blonska E, Szostak M, Gasiorek M, Pietrzykowski M, Urban O, Derbis P (2018) Restoration of vegetation in relation to soil properties of spoil heap heavily contaminated with heavy metals. Water Air Soil Pollut 229:392. https://doi.org/10.1007/s11270-018-4040-6
Palm GJ, Lederer T, Orth P, Saenger W, Takahashi M, Hinrichs HW, W, (2008) Specific binding of divalent metal ions to tetracycline and to the Tet repressor/tetracycline complex. J Biol Inorg Chem 13:1097–1110. https://doi.org/10.1007/s00775-008-0395-2
Paul T, Chakraborty A, Islam E, Mukherjee SK (2018) Arsenic bioremediation potential of arsenite-oxidizing Micrococcus sp. KUMAs15 isolated from contaminated soil. Pedosphere 28:299–310. https://doi.org/10.1016/S1002-0160(17)60493-4
Peciulyte D, Dirginciute-Volodkiene V (2009) Effect of long-term industrial pollution on soil microorganisms in deciduous forests situated along a pollution gradient next to a fertilizer factory. Ekologija 55:67–77. https://doi.org/10.2478/v10055-009-0008-6
Poole K (2017) At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 25:820–832. https://doi.org/10.1016/j.tim.2017.04.010
Raman NM, Asokan S, Shobana Sundari N, Ramasamy S (2017) Bioremediation of chromium(VI) by Stenotrophomonas maltophilia isolated from tannery effluent. Int J Environ Sci Technol 15:207–216. https://doi.org/10.1007/s13762-017-1378-z
Salzar MJ, Pignata ML (2014) Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation. J Geochem Explor 137:29–36. https://doi.org/10.1016/j.gexplo.2013.11.003
Sánchez-Castro I, Martínez-Rodríguez P, Abad MM, Descostes M, Merroun ML (2021) Uranium removal from complex mining waters by alginate beads doped with cells of Stenotrophomonas sp. Br 8: Novel perspectives for metal bioremediation. J Environ Manage 296:113411. https://doi.org/10.1016/j.jenvman.2021.113411
Sangthong C, Setkit K, Prapagdee B (2016) Improvement of cadmium phytoremediation after soil inoculation with a cadmium-resistant Micrococcus sp. Environ Sci Pollut Res 23:756–764. https://doi.org/10.1007/s11356-015-5318-5
Schwendener S, Perreten V (2022) The bla and mec families of β-lactam resistance genes in the genera Macrococcus Mammaliicoccus and Staphylococcus: an in-depth analysis with emphasis on Macrococcus. J Antimicrob Chemother dkac. https://doi.org/10.1093/jac/dkac107
Schumacher A, Vranken T, Malhotra A, Arts JJC, Habibovic P (2018) In vitro antimicrobial susceptibility testing methods: agar dilution to 3D tissue-engineered models. Eur J Clin Microbiol Infect Dis 37:187–208. https://doi.org/10.1007/s10096-017-3089-2
Shannon CE (1948) A mathematical theory of communication (Reprinted with correction). Bell Syst Tech J 27:379–423
Shtiza A, Swennen R, Tashko A (2005) Chromium and nickel distribution in soils, active river, overbank sediments and dust around the Burrel chromium smelter (Albania). J Geochem Explor 87:92–108. https://doi.org/10.1016/j.gexplo.2005.07.005
Sinegani AAS, Younessi N (2017) Antibiotic resistance of bacteria isolated from heavy metal-polluted soils with different land uses. J Glob Antimicrob Resist 10:247–255. https://doi.org/10.1016/j.jgar.2017.05.012
Singh J, Kalamdhad AS (2011) Effects of heavy metals on soil, plants, human health and aquatic life. Int J Res Chem Environ 1:15–21
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://journals.asm.org/doi/https://doi.org/10.1128/jb.173.2.697-703.1991
Wu D, Zhang Z, Gao Q, Ma Y (2018) Isolation and characterization of aerobic, culturable, arsenic-tolerant bacteria from lead–zinc mine tailing in southern China. World J Microbiol Biotechnol 34:177. https://doi.org/10.1007/s11274-018-2557-x
Zhang H, Ren W, Shao Q, Duan Ch (2007a) Genetic differentiation of Arthrobacter population from heavy metal-contaminated environment. Front Biol China 2:30–34. https://doi.org/10.1007/s11515-007-0005-7
Zhang HB, Yang MX, Shi W, Zheng Y, Sha T, Zha ZW (2007b) Bacterial diversity in mine tailings compared by cultivation and cultivation-independent methods and their resistance to lead and cadmium. Microb Ecol 54:705–712. https://doi.org/10.1007/s00248-007-9229-y
Zhang M, Chen L, Ye Ch, Yu X (2018) Co-selection of antibiotic resistance via copper shock loading on bacteria from a drinking water bio-filter. Environ Pollut 233:132–141. https://doi.org/10.1016/j.envpol.2017.09.084
Zhi Ch, QingYa Z, XiaoHong P, Zhang L, Xiong G (2014) Pb2+ tolerance and adsorption of Arthrobacter sp. 12–1 isolated from lead-zinc mine tailing dam. J Agric Biotechnol 22:1394–1401
Funding
This research was funded by Slovak Grant Agency VEGA (Grant No. 1/0779/21) and APVV (Slovak Research and Development Agency) Grant Agency (Grant No. SK-PL-18-0012). J.W., A.F., and S.M. acknowledge support from the Polish National Agency for Academic Exchange (Grant No. PPN/BIL/2018/1/00026/U/00001) and 11/020/BK_22/0088 Grant for Department of Metallurgy and Recycling, Silesian University of Technology, Poland.
Author information
Authors and Affiliations
Contributions
P.P., M.P. and J.S-K. designed the study and were responsible for project administration and funding acquisition. J.W., A.F. and M.S. performed the collection of samples and performed chemical analysis of substrate. L.N. and M.P. performed all biological experiments, L.N. and P.P. analyzed the sequence data. L.N., M.P. and P.P. wrote the paper with input from all authors. All authors discussed the results and contributed to the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no relevant financial or non-financial interests with respect to the work performed in the manuscript.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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.
About this article
Cite this article
Nosalova, L., Willner, J., Fornalczyk, A. et al. Diversity, heavy metals, and antibiotic resistance in culturable heterotrophic bacteria isolated from former lead–silver–zinc mine heap in Tarnowskie Gory (Silesia, Poland). Arch Microbiol 205, 26 (2023). https://doi.org/10.1007/s00203-022-03369-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03369-9