The presented study proposes an efficient utilization of a common Thymus serpyllum L. (wild thyme) plant as a highly potent biosorbent of Cu(II) and Pb(II) ions and the efficient interaction of the copper-laden plant with two opportunistic bacteria. Apart from biochars that are commonly used for adsorption, here we report the direct use of native plant, which is potentially interesting also for soil remediation. The highest adsorption capacity for Cu(II) and Pb(II) ions (qe = 12.66 and 53.13 mg g-1, respectively) was achieved after 10 and 30 min of adsorption, respectively. Moreover, the Cu-laden plant was shown to be an efficient antibacterial agent against the bacteria Escherichia coli and Staphylococcus aureus, the results being slightly better in the former case. Such an activity is enabled only via the interaction of the adsorbed ions effectively distributed within the biological matrix of the plant with bacterial cells. Thus, the sustainable resource can be used both for the treatment of wastewater and, after an effective embedment of metal ions, for the fight against microbes.

Central European Institute of Technology Brno University of Technology Purkyňova 656 123 612 00 Brno Czech Republic

Chair of Building Materials and Construction Chemistry Technische Universität Berlin Gustav Meyer Allee 25 13355 Berlin Germany

Faculty of Chemical Technology and Engineering The West Pomeranian University of Technology in Szczecin Piastów Avenue 42 71 065 Szczecin Poland

Faculty of Mathematics and Physics Charles University Ke Karlovu 3 121 16 Prague 2 Czech Republic

Institute of Biology University of Szczecin ul Wąska 13 71 415 Szczecin Poland

Institute of Geotechnics Slovak Academy of Sciences Watsonova 45 040 01 Košice Slovakia

Zobrazit více v PubMed

Ibrahim D, Froberg B, Wolf A, Rusyniak DE. Heavy metal poisoning: clinical presentations and pathophysiology. Clin Lab Med. 2006;26:67–97. doi: 10.1016/j.cll.2006.02.003. PubMed DOI

Mudhoo A, Garg VK, Wang SB. Removal of heavy metals by biosorption. Environ Chem Lett. 2012;10:109–117. doi: 10.1007/s10311-011-0342-2. DOI

Wan MW, Kan CC, Rogel BD, Dalida MLP. Adsorption of copper(II) and lead(II) ions from aqueous solution on chitosan-coated sand. Carbohydr Polym. 2010;80:891–899. doi: 10.1016/j.carbpol.2009.12.048. DOI

Moore MR. Haematological effects of lead. Sci Total Environ. 1988;71:419–431. doi: 10.1016/0048-9697(88)90214-8. PubMed DOI

Adriano DC. Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. 2. New York: Springer; 2001.

Awual MR, Yaita T, El-Safty SA, Shiwaku H, Suzuki S, Okamoto Y. Copper(II) ions capturing from water using ligand modified a new type mesoporous adsorbent. Chem Eng J. 2013;221:322–330. doi: 10.1016/j.cej.2013.02.016. DOI

Schmuhl R, Krieg HM, Keizer K. Adsorption of Cu(II) and Cr(VI) ions by chitosan: kinetics and equilibrium studies. Water SA. 2001;27:1–7. doi: 10.4314/wsa.v27i1.5002. DOI

Guerrero-Jimenez M, Calahorro C, Rojas LG. Wilson disease and psychiatric symptoms: a brief case report. Gen Psychiat. 2019;32:4e100066. doi: 10.1136/gpsych-2019-100066. PubMed DOI PMC

European Parliament, Council of the European Union (2020) Directive (EU) 2020/2184 of the European Parliament and of the Council of 16 December 2020 on the quality of water intended for human consumption. Offi J Eur Union L 435:1–62

Czikkely M, Neubauer E, Fekete I, Ymeri P, Fogarassy C. Review of heavy metal adsorption processes by several organic matters from wastewaters. Water-Sui. 2018;10:1377. doi: 10.3390/w10101377. DOI

Beni AA, Esmaeili A. Biosorption, an efficient method for removing heavy metals from industrial effluents: a review. Environ Technol Innov. 2020;17:100503. doi: 10.1016/j.eti.2019.100503. DOI

Mariana M, Khalil HPSA, Mistar EM, Yahya EB, Alfatah T, Danish M, Amayreh M. Recent advances in activated carbon modification techniques for enhanced heavy metal adsorption. J Water Process Eng. 2021;43:102221. doi: 10.1016/j.jwpe.2021.102221. DOI

Ahmad T, Danish M. A review of avocado waste-derived adsorbents: characterizations, adsorption characteristics, and surface mechanism. Chemosphere. 2022;296:134036. doi: 10.1016/j.chemosphere.2022.134036. PubMed DOI

Duan CT, Zhao N, Yu XL, Zhang XY, Xu J. Chemically modified kapok fiber for fast adsorption of Pb2+, Cd2+, Cu2+ from aqueous solution. Cellulose. 2013;20:849–860. doi: 10.1007/s10570-013-9875-9. DOI

Chen JY, Sun LF, Negulescu II, Xu BG. Fabrication and evaluation of regenerated cellulose/nanoparticle fibers from lignocellulosic biomass. Biomass Bioenerg. 2017;101:1–8. doi: 10.1016/j.biombioe.2017.03.024. DOI

Kapoor RT, Danish M, Singh RS, Rafatullah M, Khalil HPSA. Exploiting microbial biomass in treating azo dyes contaminated wastewater: mechanism of degradation and factors affecting microbial efficiency. J Water Process Eng. 2021;43:102255. doi: 10.1016/j.jwpe.2021.102255. DOI

Baláž M. Environmental mechanochemistry: recycling waste into materials using high-energy ball milling. London: Springer; 2021.

Elangovan R, Philip L, Chandraraj K. Biosorption of hexavalent and trivalent chromium by palm flower (Borassus aethiopum) Chem Eng J. 2008;141:99–111. doi: 10.1016/j.cej.2007.10.026. DOI

Witek-Krowiak A, Szafran RG, Modelski S. Biosorption of heavy metals from aqueous solutions onto peanut shell as a low-cost biosorbent. Desalination. 2011;265:126–134. doi: 10.1016/j.desal.2010.07.042. DOI

Moyo M, Guyo U, Mawenyiyo G, Zinyama NP, Nyamunda BC. Marula seed husk (Sclerocarya birrea) biomass as a low cost biosorbent for removal of Pb(II) and Cu(II) from aqueous solution. J Ind Eng Chem. 2015;27:126–132. doi: 10.1016/j.jiec.2014.12.026. DOI

Kafle A, Timilsina A, Gautam A, Adhikari K, Bhattarai A, Aryal N. Phytoremediation: mechanisms, plant selection and enhancement by natural and synthetic agents. Environ Adv. 2022;8:100203. doi: 10.1016/j.envadv.2022.100203. DOI

Witek-Krowiak A. Analysis of temperature-dependent biosorption of Cu2+ ions on sunflower hulls: kinetics, equilibrium and mechanism of the process. Chem Eng J. 2012;192:13–20. doi: 10.1016/j.cej.2012.03.075. DOI

Jarić S, Mitrović M, Pavlović P. Review of ethnobotanical, phytochemical, and pharmacological study of thymus serpyllum L. Evidence Based Complement Altern Med. 2015;2015:101978. doi: 10.1155/2015/101978. PubMed DOI PMC

Jovanovic AA, Dordevic VB, Zdunic GM, Pljevljakusic DS, Savikin KP, Godevac DM, Bugarski BM. Optimization of the extraction process of polyphenols from Thymus serpyllum L. herb using maceration, heat- and ultrasound-assisted techniques. Sep Purif Technol. 2017;179:369–380. doi: 10.1016/j.seppur.2017.01.055. DOI

Nikolić M, Glamočlija J, Ferreira ICFR, Calhelha RC, Fernandes T, Marković T, Marković D, Giweli A, Soković M. Chemical composition, antimicrobial, antioxidant and antitumor activity of Thymus serpyllum L., Thymus algeriensis Boiss. and Reut and Thymus vulgaris L. essential oils. Ind Crops Prod. 2014;52:183–190. doi: 10.1016/j.indcrop.2013.10.006. DOI

Figas A, Tomaszewska-Sowa M, Kobierski M, Sawilska AK, Klimkowska K. Hazard of contamination with heavy metals in Thymus serpyllum L. Herbs from rural areas. Agriculture. 2021;11:375. doi: 10.3390/agriculture11040375. DOI

Littera P, Urik M, Sevc J, Kolencik M, Gardosova K. The potential of thymus serpyllum biomass for removal of antimony(Iii) from aqueous environment. Fresenius Environ Bull. 2011;20:2959–2963.

Harikishore Kumar Reddy D, Vijayaraghavan K, Kim JA, Yun YS. Valorisation of post-sorption materials: opportunities, strategies, and challenges. Adv Colloid Interface Sci. 2017;242:35–58. doi: 10.1016/j.cis.2016.12.002. PubMed DOI

Staroń P, Pszczółka K, Chwastowski J, Banach M. Sorption behavior of Arachis hypogaea shells against Ag+ ions and assessment of antimicrobial properties of the product. Environ Sci Pollut Res. 2020;27:19530–19542. doi: 10.1007/s11356-020-08464-2. PubMed DOI PMC

Zavareh S, Zarei M, Darvishi F, Azizi H. As(III) adsorption and antimicrobial properties of Cu-chitosan/alumina nanocomposite. Chem Eng J. 2015;273:610–621. doi: 10.1016/j.cej.2015.03.112. DOI

Mahltig B, Soltmann U, Haase H. Modification of algae with zinc, copper and silver ions for usage as natural composite for antibacterial applications. Mater Sci Eng C. 2013;33:979–983. doi: 10.1016/j.msec.2012.11.033. PubMed DOI

Lagergren S. Zur Theorie der sogenannten Adsorption gelöster Stoffe, Kungliga Svenska Vetenskapsakademiens. Handlingar. 1898;24:1–39.

Ho YS, Wase DAJ, Forster CF. Kinetic studies of competitive heavy metal adsorption by sphagnum moss peat. Environ Technol. 1996;17:71–77. doi: 10.1080/09593331708616362. DOI

Freundlich HMF. Uber die adsorption in Losungen. Z Phys Chem. 1906;57:385–470.

Langmuir I. The constitution and fundamental properties of solids and liquids part I solids. J Am Chem Soc. 1916;38:2221–2295. doi: 10.1021/ja02268a002. DOI

Yankovych H, Novoseltseva V, Kovalenko O, Behunova DM, Kanuchova M, Vaclavikova M, Melnyk I. New perception of Zn(II) and Mn(II) removal mechanism on sustainable sunflower biochar from alkaline batteries contaminated water. J Environ Manag. 2021;292:112757. doi: 10.1016/j.jenvman.2021.112757. PubMed DOI

Martinez M, Miralles N, Hidalgo S, Fiol N, Villaescusa I, Poch J. Removal of lead(II) and cadmium(II) from aqueous solutions using grape stalk waste. J Hazard Mater. 2006;133:203–211. doi: 10.1016/j.jhazmat.2005.10.030. PubMed DOI

Zou ZM, Tang YL, Jiang CH, Zhang JS. Efficient adsorption of Cr(VI) on sunflower seed hull derived porous carbon. J Environ Chem Eng. 2015;3:898–905. doi: 10.1016/j.jece.2015.02.025. DOI

Cui SH, Zhang R, Peng YT, Gao X, Li Z, Fan BB, Guan CY, Beiyuan J, Zhou YY, Liu J, Chen Q, Sheng J, Guo LL. New insights into ball milling effects on MgAl-LDHs exfoliation on biochar support: a case study for cadmium adsorption. J Hazard Mater. 2021;416:11126258. doi: 10.1016/j.jhazmat.2021.126258. PubMed DOI

Leng L, Xiong Q, Yang L, Li H, Zhou Y, Zhang W, Jiang S, Li H, Huang H. An overview on engineering the surface area and porosity of biochar. Sci Total Environ. 2021;763:144204. doi: 10.1016/j.scitotenv.2020.144204. PubMed DOI

Bhattacharyya KG, Sen Gupta S. Adsorption of Fe(III) from water by natural and acid activated clays: studies on equilibrium isotherm, kinetics and thermodynamics of interactions. Adsorpt J Int Adsorpt Soc. 2006;12:185–204. doi: 10.1007/s10450-006-0145-0. DOI

Ucer A, Uyanik A, Aygun SF. Adsorption of Cu(II), Cd(II), Zn(II), Mn(II) and Fe(III) ions by tannic acid immobilised activated carbon. Sep Purif Technol. 2006;47:113–118. doi: 10.1016/j.seppur.2005.06.012. DOI

Cruz-Olivares J, Perez-Alonso C, Barrera-Diaz C, Lopez G, Balderas-Hernandez P. Inside the removal of lead(II) from aqueous solutions by De-Oiled Allspice Husk in batch and continuous processes. J Hazard Mater. 2010;181:1095–1101. doi: 10.1016/j.jhazmat.2010.05.127. PubMed DOI

Huang XX, Liu YG, Liu SB, Tan XF, Ding Y, Zeng GM, Zhou YY, Zhang MM, Wang SF, Zheng BH. Effective removal of Cr(VI) using beta-cyclodextrin-chitosan modified biochars with adsorption/reduction bifuctional roles. RSC Adv. 2016;6:94–104. doi: 10.1039/c5ra22886g. DOI

Huang YH, Hsueh CL, Huang CP, Su LC, Chen CY. Adsorption thermodynamic and kinetic studies of Pb(II) removal from water onto a versatile Al2O3-supported iron oxide. Sep Purif Technol. 2007;55:23–29. doi: 10.1016/j.seppur.2006.10.023. DOI

Liu LL, Luo XB, Ding L, Luo SL. Application of nanotechnology in the removal of heavy metal from water. Amsterdam: Elsevier; 2019.

Bayo J. Kinetic studies for Cd(II) biosorption from treated urban effluents by native grapefruit biomass (Citrus paradisi L.): the competitive effect of Pb(II), Cu(II) and Ni(II) Chem Eng J. 2012;191:278–287. doi: 10.1016/j.cej.2012.03.016. DOI

Ivanova L, Vassileva P, Detcheva A. Studies on copper(II) biosorption using a material based on the plant Thymus vulgaris L. Mater Today Proc. 2022;61:1237–1242. doi: 10.1016/j.matpr.2022.02.040. DOI

Kumar R, Kumar Joshi H, Vishwakarma MC, Sharma H, Joshi SK, Bhandari NS. Biosorption of copper and lead ions onto treated biomass Myrica esculenta: isotherms and kinetics studies. Environ Nanotechnol Monitor Manag. 2023;19:100775. doi: 10.1016/j.enmm.2022.100775. DOI

Hazarika L, Shah KK, Baruah G, Bharali RK. Kinetic and equilibrium studies on bioadsorption of copper and lead by water hyacinth (Eichhornia crassipes) plant powder. Vietnam J Chem. 2023;61:238–252. doi: 10.1002/vjch.202200138. DOI

Castanho NRCM, De Oliveira RA, Batista BL, Freire BM, Lange C, Lopes AM, Jozala AF, Grotto D. Comparative study on lead and copper biosorption using three bioproducts from edible mushrooms residues. J Fungi. 2021;7:441. doi: 10.3390/jof7060441. PubMed DOI PMC

Jonglertjunya W. Biosorption of lead(II) and copper(II) from aqueous solution. Chiang Mai J Sci. 2008;35:69–81.

Afolabi FO, Musonge P, Bakare BF. Bio-sorption of copper and lead ions in single and binary systems onto banana peels. Cogent Eng. 2021;8:1886730. doi: 10.1080/23311916.2021.1886730. PubMed DOI PMC

Lee ME, Park JH, Chung JW. Comparison of the lead and copper adsorption capacities of plant source materials and their biochars. J Environ Manag. 2019;236:118–124. doi: 10.1016/j.jenvman.2019.01.100. PubMed DOI

Sienkiewicz M, Lysakowska M, Ciećwierz J, Denys P, Kowalczyk E. Antibacterial activity of thyme and lavender essential oils. Med Chem. 2011;7:674–689. doi: 10.2174/157340611797928488. PubMed DOI

Galovičová L, Borotová P, Valková V, Vukovic NL, Vukic M, Terentjeva M, Štefániková J, Ďúranová H, Kowalczewski PŁ, Kačániová M. Thymus serpyllum essential oil and its biological activity as a modern food preserver. Plants. 2021;10:1416. doi: 10.3390/plants10071416. PubMed DOI PMC

Mahaninia MH, Rahimian P, Kaghazchi T. Modified activated carbons with amino groups and their copper adsorption properties in aqueous solution. Chin J Chem Eng. 2015;23:50–56. doi: 10.1016/j.cjche.2014.11.004. DOI

Forgionny A, Acelas NY, Ocampo-Perez R, Padilla-Ortega E, Leyva-Ramos R, Florez E. Understanding mechanisms in the adsorption of lead and copper ions on chili seed waste in single and multicomponent systems: a combined experimental and computational study. Environ Sci Pollut Res. 2021;28:23204–23219. doi: 10.1007/s11356-020-11721-z. PubMed DOI

Xu L, Liu YN, Wang JG, Tang Y, Zhang Z. Selective adsorption of Pb2+ and Cu2+ on amino-modified attapulgite: kinetic, thermal dynamic and DFT studies. J Hazard Mater. 2021;404:10124140. doi: 10.1016/j.jhazmat.2020.124140. PubMed DOI

Shafeeyan MS, Daud W, Houshmand A, Shamiri A. A review on surface modification of activated carbon for carbon dioxide adsorption. J Anal Appl Pyrolysis. 2010;89:143–151. doi: 10.1016/j.jaap.2010.07.006. DOI

Luiz JM, Nunes RS. Synthesis, characterization, and thermal behavior of amidosulfonates of transition metals in air and nitrogen atmosphere. Eclet Quím. 2020;45:32–39. doi: 10.26850/1678-4618eqj.v45.4.2020.p32-39. DOI

Basu M, Guha AK, Ray L. Adsorption of lead on cucumber peel. J Cleaner Prod. 2017;151:603–615. doi: 10.1016/j.jclepro.2017.03.028. DOI

Sheng PX, Ting YP, Chen JP, Hong L. Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: characterization of biosorptive capacity and investigation of mechanisms. J Colloid Interface Sci. 2004;275:131–141. doi: 10.1016/j.jcis.2004.01.036. PubMed DOI

Lu HL, Zhang WH, Yang YX, Huang XF, Wang SZ, Qiu RL. Relative distribution of Pb2+ sorption mechanisms by sludge-derived biochar. Water Res. 2012;46:854–862. doi: 10.1016/j.watres.2011.11.058. PubMed DOI

Smith M, Scudiero L, Espinal J, McEwen JS, Garcia-Perez M. Improving the deconvolution and interpretation of XPS spectra from chars by ab initio calculations. Carbon. 2016;110:155–171. doi: 10.1016/j.carbon.2016.09.012. DOI

Wang J, Liu TL, Huang QX, Ma ZY, Chi Y, Yan JH. Production and characterization of high quality activated carbon from oily sludge. Fuel Process Technol. 2017;162:13–19. doi: 10.1016/j.fuproc.2017.03.017. DOI

Taylor JA, Perry DL. An X-ray photoelectron and electron energy loss study of the oxidation of lead. J Vac Sci Technol, A. 1984;2:771–774. doi: 10.1116/1.572569. DOI

Rondon S, Sherwood PMA. Core level and valence band spectra of PbO by XPS. Surf Sci Spectra. 1998;5:97–103. doi: 10.1116/1.1247866. DOI

Laajalehto K, Smart RS, Ralston J, Suoninen E. STM and XPS investigation of reaction of galena in air. Appl Surf Sci. 1993;64:29–39. doi: 10.1016/0169-4332(93)90019-8. DOI

Biesinger MC. Advanced analysis of copper X-ray photoelectron spectra. Surf Interface Anal. 2017;49:1325–1334. doi: 10.1002/sia.6239. DOI

Li D, Wang GN, Cheng LM, Wang CP, Mei XF. Engineering the self-assembly induced emission of copper nanoclusters as 3D nanomaterials with mesoporous sphere structures by the crosslinking of Ce3+ ACS Omega. 2018;3:14755–14765. doi: 10.1021/acsomega.8b02204. PubMed DOI PMC

Liu R, Zuo L, Huang XR, Liu SM, Yang GY, Li SY, Lv CY. Colorimetric determination of lead(II) or mercury(II) based on target induced switching of the enzyme-like activity of metallothionein-stabilized copper nanoclusters. Microchim Acta. 2019;186:250. doi: 10.1007/s00604-019-3360-6. PubMed DOI

Cui XQ, Fang SY, Yao YQ, Li TQ, Ni QJ, Yang XE, He ZL. Potential mechanisms of cadmium removal from aqueous solution by Canna indica derived biochar. Sci Total Environ. 2016;562:517–525. doi: 10.1016/j.scitotenv.2016.03.248. PubMed DOI

Vincent M, Duval RE, Hartemann P, Engels-Deutsch M. Contact killing and antimicrobial properties of copper. J Appl Microbiol. 2018;124:1032–1046. doi: 10.1111/jam.13681. PubMed DOI

Verma RS, Padalia RC, Saikia D, Chauhan A, Krishna V, Sundaresan V. Chemical composition and antimicrobial activity of the essential oils isolated from the herbage and aqueous distillates of two thymus species. J Essent Oil Bear Plants. 2016;19:936–943. doi: 10.1080/0972060x.2014.935071. DOI

Scheutz F, Strockbine NA (2015) Escherichia. In: Trujillo ME, Dedysh P, DeVos B, Hedlund P, Kämpfer P, Rainey FA, Whitman WB (eds) Bergey’s manual of systematics of archaea and bacteria

Schleifer K, Bell JA (2015) Staphylococcus. In: Trujillo ME, Dedysh P, DeVos B, Hedlund P, Kämpfer P, Rainey FA, Whitman WB (eds) Bergey’s manual of systematics of archaea and bacteria