Abstract
Bioreduction of selenium oxyanions to elemental selenium is ubiquitous; elucidating the properties of this biogenic elemental selenium (BioSe) is thus important to understand its environmental fate. In this study, the magnetic properties of biogenic elemental selenium nanospheres (BioSe-Nanospheres) and nanorods (BioSe-Nanorods) obtained via the reduction of selenium(IV) using anaerobic granular sludge taken from an upflow anaerobic sludge blanket (UASB) reactor treating paper and pulp wastewater were investigated. The study indicated that the BioSe nanomaterials have a strong paramagnetic contribution with some ferromagnetic component due to the incorporation of Fe(III) (high-spin and low-spin species) as indicated by electron paramagnetic resonance (EPR). The paramagnetism did not saturate up to 50,000 Oe at 5 K, and the hysteresis curve showed the coercivity of 100 Oe and magnetic moment saturation around 10 emu. X-ray photoelectron spectroscopy (XPS) and EPR evidenced the presence of Fe(III) in the nanomaterial. Signals for Fe(II) were observed neither in EPR nor in XPS ruling out its presence in the BioSe nanoparticles. Fe(III) being abundantly present in the sludge likely got entrapped in the extracellular polymeric substances (EPS) coating the biogenic nanomaterials. The presence of Fe(III) in BioSe nanomaterial increases the mobility of Fe(III) and may have an effect on phytoplankton growth in the environment. Furthermore, as supported by the literature, there is a potential to exploit the magnetic properties of BioSe nanomaterials in drug delivery systems as well as in space refrigeration.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All the data generated in this study has been included in this article.
References
Ali A, Zafar H, Zia M, ul Haq I, Phull AR, Ali JS, Hussain A (2016) Synthesis, characterization, applications, and challenges of iron oxide nanoparticles. Nanotechnol Sci Appl 9:49–67. https://doi.org/10.2147/NSA.S99986
Amweg EL, Stuart DL, Weston DP (2003) Comparative bioavailability of selenium to aquatic organisms after biological treatment of agricultural drainage water. Aquat Toxicol 63:13–25. https://doi.org/10.1016/S0166-445X(02)00110-8
Chudobova D, Cihalova K, Dostalova S, Ruttkay-Nedecky B, Merlos Rodrigo MA, Tmejova K, Kopel P, Nejdl L, Kudr J, Gumulec J, Krizkova S, Kynicky J, Kizek R, Adam V (2014) Comparison of the effects of silver phosphate and selenium nanoparticles on Staphylococcus aureus growth reveals potential for selenium particles to prevent infection. FEMS Microbiol Lett 351:195–201. https://doi.org/10.1111/1574-6968.12353
Coey JMD (2010) Magnetism and magnetic materials. Cambridge University Press, Cambridge
Dessì P, Jain R, Singh S, Seder-Colomina M, van Hullebusch ED, Rene ER, Ahammad SZ, Carucci A, Lens PNL (2016) Effect of temperature on selenium removal from wastewater by UASB reactors. Water Res 94:146–154. https://doi.org/10.1016/j.watres.2016.02.007
Drewniak L, Sklodowska A (2013) Arsenic-transforming microbes and their role in biomining processes. Environ Sci Pollut Res 20:7728–7739. https://doi.org/10.1007/s11356-012-1449-0
Edler E, Stein M (2014) Spin-state-dependent properties of an iron(III) hydrogenase mimic. Eur J Inorg Chem 2014:3587–3599. https://doi.org/10.1002/ejic.201402295
Fatoki OS, Mathabatha S (2001) An assessment of heavy metal pollution in the East London and Port Elizabeth harbours. Water SA 27:233–240. https://doi.org/10.4314/wsa.v27i2.4997
Fennel K, Abbott MR, Spitz YH, Richman JG, Nelson DM (2003) Impacts of iron control on phytoplankton production in the modern and glacial Southern Ocean. Deep Res Part II Top Stud Oceanogr 50:833–851. https://doi.org/10.1016/S0967-0645(02)00596-9
Fernández-Martínez A, Charlet L (2009) Selenium environmental cycling and bioavailability: a structural chemist point of view. Rev Environ Sci Biotechnol 8:81–110. https://doi.org/10.1007/s11157-009-9145-3
Finotelli PV, Morales MA, Rocha-Leão MH, Baggio-Saitovitch EM, Rossi AM (2004) Magnetic studies of iron(III) nanoparticles in alginate polymer for drug delivery applications. Mater Sci Eng C 24:625–629. https://doi.org/10.1016/j.msec.2004.08.005
Gao S, Tanji KK, Peters DW, Herbel MJ (2000) Water selenium speciation and sediment fractionation in a California flow-through wetland system. J Environ Qual 29:1275–1283. https://doi.org/10.2134/jeq2000.00472425002900040034x
George S, Pokhrel S, Xia T, Gilbert B, Ji Z, Schowalter M, Rosenauer A, Damoiseaux R, Bradley KA, Mädler L, Nel AE (2010) Use of a rapid cytotoxicity screening approach to engineer a safer zinc oxide nanoparticle through iron doping. ACS Nano 4:15–29. https://doi.org/10.1021/nn901503q
Golubkina NA, Folmanis GE, Tananaev IG (2012) Comparative evaluation of selenium accumulation by Allium species after foliar application of selenium nanoparticles, sodium selenite and sodium selenate. Dokl Biol Sci 444:176–179. https://doi.org/10.1134/S0012496612030076
Hauksdóttir HL, Webster TJ (2018) Selenium and iron oxide nanocomposites for magnetically-targeted anti-cancer applications. J Biomed Nanotechnol 14:510–525. https://doi.org/10.1166/jbn.2018.2521
Hiemstra T, van Riemsdijk WH (2006) Biogeochemical speciation of Fe in ocean water. Mar Chem 102:181–197. https://doi.org/10.1016/j.marchem.2006.03.008
Hu T, Li H, Li J, Zhao G, Wu W, Liu L, Wang Q, Guo Y (2018) Absorption and bio-transformation of selenium nanoparticles by wheat seedlings (Triticumaestivum L.). Front. Plant Sci 9:597. https://doi.org/10.3389/fpls.2018.00597
Huber F, Schild D, Vitova T, Rothe J, Kirsch R, Schäfer T (2012) U(VI) removal kinetics in presence of synthetic magnetite nanoparticles. Geochim Cosmochim Acta 96:154–173. https://doi.org/10.1016/j.gca.2012.07.019
Jain R, Gonzale-Gil G, Singh V et al (2014) Biogenic selenium nanoparticles: production, characterization and challenges. In: Biotechnology Volume 10: Nanobiotechnology, Studium Press LLC, pp 365–394
Jain R, Jordan N, Schild D, van Hullebusch ED, Weiss S, Franzen C, Farges F, Hübner R, Lens PNL (2015a) Adsorption of zinc by biogenic elemental selenium nanoparticles. Chem Eng J 260:855–863. https://doi.org/10.1016/j.cej.2014.09.057
Jain R, Jordan N, Weiss S, Foerstendorf H, Heim K, Kacker R, Hübner R, Kramer H, van Hullebusch ED, Farges F, Lens PNL (2015b) Extracellular polymeric substances govern the surface charge of biogenic elemental selenium nanoparticles. Environ Sci Technol 49:1713–1720. https://doi.org/10.1021/es5043063
Jain R, Matassa S, Singh S, van Hullebusch ED, Esposito G, Lens PNL (2016) Reduction of selenite to elemental selenium nanoparticles by activated sludge. Environ Sci Pollut Res 23:1193–1202. https://doi.org/10.1007/s11356-015-5138-7
Jain R, Jordan N, Tsushima S, Hübner R, Weiss S, Lens PNL (2017) Shape change of biogenic elemental selenium nanomaterials from nanospheres to nanorods decreases their colloidal stability. Environ Sci Nano 4:1054–1063. https://doi.org/10.1039/c7en00145b
Khalilov RI, Nasibova AN, Serezhenkov VA, Ramazanov MA, Kerimov MK, Garibov AA, Vanin AF (2011) Accumulation of magnetic nanoparticles in plants grown on soils of Apsheron peninsula. Biophysics (Oxf) 56:316–322. https://doi.org/10.1134/S000635091102014X
Krastev PB, Gunnlaugsson HP, Nomura K, Bharuth-Ram K, Qi B, Masenda H, Mølholt TE, Naidoo D, Ólafsson S, Martín-Luengo AT, Unzueta I, Johnston K, Schell J, Gislason HP (2020) Local increase of the Curie temperature in Mn/Fe implanted Y3Fe5O12 (YIG). Appl Radiat Isot 160:2–6. https://doi.org/10.1016/j.apradiso.2020.109121
Kumar N, Krishnani KK, Singh NP (2018) Comparative study of selenium and selenium nanoparticles with reference to acute toxicity, biochemical attributes, and histopathological response in fish. Environ Sci Pollut Res 25:8914–8927. https://doi.org/10.1007/s11356-017-1165-x
Lenz M, Enright AM, O’Flaherty V, van Aelst AC, Lens PNL (2009) Bioaugmentation of UASB reactors with immobilized Sulfurospirillum barnesii for simultaneous selenate and nitrate removal. Appl Microbiol Biotechnol 83:377–388. https://doi.org/10.1007/s00253-009-1915-x
Levasseur S, Frank M, Hein JR, Halliday AN (2004) The global variation in the iron isotope composition of marine hydrogenetic ferromanganese deposits: Implications for seawater chemistry? Earth Planet Sci Lett 224:91–105. https://doi.org/10.1016/j.epsl.2004.05.010
Li L, Yan M (2020) Recent progresses in exploring the rare earth based intermetallic compounds for cryogenic magnetic refrigeration. J Alloys Compd 823:153810. https://doi.org/10.1016/j.jallcom.2020.153810
Li J, Struzhkin VV, Mao HK, Shu J, Hemley RJ, Fei Y, Mysen B, Dera P, Prakapenka V, Shen G (2004) Electronic spin state of iron in lower mantle perovskite. Proc Natl Acad Sci U S A 101:14027–14030. https://doi.org/10.1073/pnas.0405804101
Li DB, Cheng YY, Wu C, Li WW, Li N, Yang ZC, Tong ZH, Yu HQ (2014) Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm. Sci Rep 4:1–7. https://doi.org/10.1038/srep03735
Li D, An Q, Wu Y, Li JQ, Pan C (2020) Foliar application of selenium nanoparticles on celery stimulates several nutrient component levels by regulating the α-linolenic acid pathway. ACS Sustain Chem Eng 8:10502–10510. https://doi.org/10.1021/acssuschemeng.0c02819
Ling L, Zhang WX (2014) Structures of Pd-Fe(0) bimetallic nanoparticles near 0.1 nm resolution. RSC Adv 4:33861–33865. https://doi.org/10.1039/c4ra04311a
Luna H, Baêta B, Aquino S, Rodríguez Susa M (2014) EPS and SMP dynamics at different heights of a submerged anaerobic membrane bioreactor (SAMBR). Process Biochem 49:2241–2248. https://doi.org/10.1016/j.procbio.2014.09.013
Lv J, Christie P, Zhang S (2019) Uptake, translocation, and transformation of metal-based nanoparticles in plants: recent advances and methodological challenges. Environ Sci Nano 6:41–59. https://doi.org/10.1039/C8EN00645H
Mal J, Veneman WJ, Nancharaiah YV, van Hullebusch ED, Peijnenburg WJGM, Vijver MG, Lens PNL (2017) A comparison of fate and toxicity of selenite, biogenically, and chemically synthesized selenium nanoparticles to zebrafish (Danio rerio) embryogenesis. Nanotoxicology 11:87–97. https://doi.org/10.1080/17435390.2016.1275866
Malhotra N, Chen JR, Sarasamma S, Audira G, Siregar P, Liang ST, Lai YH, Lin GM, Ger TR, Hsiao CD (2019) Ecotoxicity assessment of Fe3O4 magnetic nanoparticle exposure in adult zebrafish at an environmental pertinent concentration by behavioral and biochemical testing. Nanomaterials 9:873. https://doi.org/10.3390/nano9060873
Mazur M, Pogány L, Brachňaková B, Šalitroš I (2020) A variable-temperature Q- and X-band EPR study of spin-crossover iron(III) Schiff base complex. Chem Pap 74:3683–3692. https://doi.org/10.1007/s11696-019-00781-2
Mohite BV, Koli SH, Patil SV (2018) Heavy metal stress and its consequences on exopolysaccharide (EPS)-producing Pantoea agglomerans. Appl Biochem Biotechnol 186:199–216. https://doi.org/10.1007/s12010-018-2727-1
Nancharaiah YV, Lens PNL (2015) Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev 79:61–80. https://doi.org/10.1128/mmbr.00037-14
Pal A, Shirodkar SN, Gohil S, Ghosh S, Waghmare UV, Ayyub P (2013) Multiferroic behavior in elemental selenium below 40 K: effect of electronic topology. Sci Rep 3:1–7. https://doi.org/10.1038/srep02051
Park H, Ayala P, Deshusses MA et al (2008) Electrodeposition of maghemite (γ-Fe2O3) nanoparticles. Chem Eng J 139:208–212. https://doi.org/10.1016/j.cej.2007.10.025
Pradel N, Fuduche M, Ollivier B (2016) Magnetotactic bacteria population in a pristine French Atlantic lagoon. Environ Sci Pollut Res 23:691–697. https://doi.org/10.1007/s11356-015-5322-9
Qin T, Chen J, Wang D, Hu Y, Zhang J, Wang M, Qiu S, Gao Z, liu R, Yu Y, Huang Y, Wang Q, Wang Q (2013) Selenylation modification can enhance immune-enhancing activity of Chinese angelica polysaccharide. Carbohydr Polym 95:183–187. https://doi.org/10.1016/j.carbpol.2013.02.072
Roessler MM, Salvadori E (2018) Principles and applications of EPR spectroscopy in the chemical sciences. Chem Soc Rev 47:2534–2553. https://doi.org/10.1039/c6cs00565a
Roest K, Heilig HGHJ, Smidt H, de Vos WM, Stams AJM, Akkermans ADL (2005) Community analysis of a full-scale anaerobic bioreactor treating paper mill wastewater. Syst Appl Microbiol 28:175–185. https://doi.org/10.1016/j.syapm.2004.10.006
Sand W, Gehrke T (2006) Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria. Res Microbiol 157:49–56. https://doi.org/10.1016/j.resmic.2005.07.012
Schulz-Vogt HN, Pollehne F, Jürgens K, Arz HW, Beier S, Bahlo R, Dellwig O, Henkel JV, Herlemann DPR, Krüger S, Leipe T, Schott T (2019) Effect of large magnetotactic bacteria with polyphosphate inclusions on the phosphate profile of the suboxic zone in the Black Sea. ISME J 13:1198–1208. https://doi.org/10.1038/s41396-018-0315-6
Shankramma K, Yallappa S, Shivanna MB, Manjanna J (2016) Fe2O3 magnetic nanoparticles to enhance S. lycopersicum (tomato) plant growth and their biomineralization. Appl Nanosci 6:983–990. https://doi.org/10.1007/s13204-015-0510-y
Staicu LC, van Hullebusch ED, Lens PNL, Pilon-Smits EAH, Oturan MA (2015) Electrocoagulation of colloidal biogenic selenium. Environ Sci Pollut Res 22:3127–3137. https://doi.org/10.1007/s11356-014-3592-2
Stock T, Rother M (2009) Selenoproteins in Archaea and Gram-positive bacteria. Biochim Biophys Acta, Gen Subj 1790:1520–1532. https://doi.org/10.1016/j.bbagen.2009.03.022
Stoll S, Schweiger A (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J Magn Reson 178:42–55. https://doi.org/10.1016/j.jmr.2005.08.013
Tan LC, Nancharaiah YV, van Hullebusch ED, Lens PNL (2016) Selenium: environmental significance, pollution, and biological treatment technologies. Biotechnol Adv 34:886–907. https://doi.org/10.1016/j.biotechadv.2016.05.005
Tapia JM, Muñoz JA, González F, Blázquez ML, Ballester A (2011) Mechanism of adsorption of ferric iron by extracellular polymeric substances (EPS) from a bacterium Acidiphilium sp. Water Sci Technol 64:1716–1722. https://doi.org/10.2166/wst.2011.649
Temesghen W, Sherwood PMA (2002) Analytical utility of valence band X-ray photoelectron spectroscopy of iron and its oxides, with spectral interpretation by cluster and band structure calculations. Anal Bioanal Chem 373:601–608. https://doi.org/10.1007/s00216-002-1362-3
Usov NA, Liubimov BY (2012) Dynamics of magnetic nanoparticle in a viscous liquid: application to magnetic nanoparticle hyperthermia. J Appl Phys 112:02. https://doi.org/10.1063/1.4737126
Vicente AI, Joseph A, Ferreira LP, de Deus Carvalho M, Rodrigues VHN, Duttine M, Diogo HP, Minas da Piedade ME, Calhorda MJ, Martinho PN (2016) Dynamic spin interchange in a tridentate Fe(III) Schiff-base compound. Chem Sci 7:4251–4258. https://doi.org/10.1039/c5sc04577k
Vignola F, Borges DLG, Curtius AJ, Welz B, Becker-Ross H (2010) Simultaneous determination of Cd and Fe in sewage sludge by high-resolution continuum source electrothermal atomic absorption spectrometry with slurry sampling. Microchem J 95:333–336. https://doi.org/10.1016/j.microc.2010.01.014
Vlasov A, Guillemette J, Gervais G, Szkopek T (2017) Magnetic refrigeration with paramagnetic semiconductors at cryogenic temperatures. Appl Phys Lett 111:14. https://doi.org/10.1063/1.4994536
Wang H, Zhang J, Yu H (2007) Elemental selenium at nano size possesses lower toxicity without compromising the fundamental effect on selenoenzymes: Comparison with selenomethionine in mice. Free Radic Biol Med 42:1524–1533. https://doi.org/10.1016/j.freeradbiomed.2007.02.013
Wang Y, Liu Y, Wendler E, Hübner R, Anwand W, Wang G, Chen X, Tong W, Yang Z, Munnik F, Bukalis G, Chen X, Gemming S, Helm M, Zhou S (2015) Defect-induced magnetism in SiC: interplay between ferromagnetism and paramagnetism. Phys Rev B - Condens Matter Mater Phys 92:1–11. https://doi.org/10.1103/PhysRevB.92.174409
Wang Q, Mejía Jaramillo A, Pavon JJ, Webster TJ (2016) Red selenium nanoparticles and gray selenium nanorods as antibacterial coatings for PEEK medical devices. J Biomed Mater Res - Part B Appl Biomater 104:1352–1358. https://doi.org/10.1002/jbm.b.33479
Winkel LHE, Johnson CA, Lenz M, Grundl T, Leupin OX, Amini M, Charlet L (2012) Environmental selenium research: from microscopic processes to global understanding. Environ Sci Technol 46:571–579. https://doi.org/10.1021/es203434d
Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, Schoenfeld D, Meng H, Lin S, Wang X, Wang M, Ji Z, Zink JI, Mädler L, Castranova V, Lin S, Nel AE (2011) Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano 5:1223–1235. https://doi.org/10.1021/nn1028482
Yue X, Guo W, Li X, Zhou H, Wang R (2016) Core-shell Fe3O4@MIL-101(Fe) composites as heterogeneous catalysts of persulfate activation for the removal of Acid Orange 7. Environ Sci Pollut Res 23:15218–15226. https://doi.org/10.1007/s11356-016-6702-5
Zandvoort MH, van Hullebusch ED, Gieteling J, Lens PNL (2006) Granular sludge in full-scale anaerobic bioreactors: trace element content and deficiencies. Enzym Microb Technol 39:337–346. https://doi.org/10.1016/j.enzmictec.2006.03.034
Zhang Y, Zahir ZA, Frankenberger WT (2003) Factors affecting reduction of selenate to elemental selenium in agricultural drainage water by Enterobacter taylorae. J Agric Food Chem 51:7073–7078. https://doi.org/10.1021/jf0304019
Zhang J, Wang H, Bao Y, Zhang L (2004) Nano red elemental selenium has no size effect in the induction of seleno-enzymes in both cultured cells and mice. Life Sci 75:237–244. https://doi.org/10.1016/j.lfs.2004.02.004
Acknowledgments
The authors express gratitude to Dr YM Frappart (University of Paris Descartes, France) for his help in EPR data recording.
Funding
The design of the study and collection of data was supported through Erasmus Mundus Joint Doctorate Environmental Technologies for Contaminated Solids, Soils, and Sediments (ETeCoS3) (FPA no. 2010-0009). The analysis and interpretation of data and writing of the manuscript were supported by the fellowship provided by the Ministry of Human Resource Development (MHRD), Government of India, to the first author to pursue her PhD.
Author information
Authors and Affiliations
Contributions
RD carried out data analysis and interpretation. RD critically analyzed the data and wrote the manuscript with support from AG. NJ, SW, and DS carried out XPS experiments. EG and SG carried out EPR and magnetism experiments, respectively. RJ conceptualized the study and prepared samples for analysis with support from NJ and SW. PL supervised the study.
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Additional information
Responsible Editor: Santiago V. Luis
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOC 44 kb)
Rights and permissions
About this article
Cite this article
Dixit, R., Gupta, A., Jordan, N. et al. Magnetic properties of biogenic selenium nanomaterials. Environ Sci Pollut Res 28, 40264–40274 (2021). https://doi.org/10.1007/s11356-020-11683-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11683-2