Abstract
Selenium (SeNPs) and tellurium nanoparticles (TeNPs) were synthesized by green technology using the three new bacterial marine isolates (strains PL 2476, AF 2469 and G 2451). Isolates were classified as Pseudoalteromonas shioyasakiensis according to 16S rRNA sequence analysis, morphological characteristics, and biochemical reactions. The bioreduction processes of isolates were studied in comparison with the previously described Alteromonas macleodii (strain 2328). All strains exhibited significant tolerance to selenite and tellurite up to 1000 µg/mL. A comparative analysis of the bioreduction processes of the isolates demonstrated that the strains have a high rate of reduction processes. Characterization of biogenic red SeNPs and black TeNPs using scanning electron microscopy (SEM), EDX analysis, Dynamic Light Scattering, and micro-Raman Spectroscopy revealed that all the isolates form stable spherical selenium and tellurium nanoparticles whose size as well as elemental composition depend on the producer strain. Nanoparticles of the smallest size (up to 100 nm) were observed only for strain PL 2476. Biogenic SeNPs and TeNPs were also characterized and tested for their antimicrobial, antifouling and cytotoxic activities. Significant antimicrobial activity was shown for nanoparticles at relatively high concentrations (500 and 1000 µg/mL), with the antimicrobial activity of TeNPs being more significant than SeNPs. In contrast, against cell cultures (breast cancer cells (SkBr3) and human dermal fibroblasts (HDF) SeNPs showed greater toxicity than tellurium nanoparticles. Studies have demonstrated the high antifouling effectiveness of selenium and tellurium nanoparticles when introduced into self-polishing coatings. According to the results obtained, the use of SeNPs and TeNPs as antifouling additives can reduce the concentration of leachable biocides used in coatings, reducing the pressure on the environment.
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References
Abo EMM, Al-Hagar OEA, Abdelkhalek ES, Sidkey NM (2018) Synthesis and investigations on tellurium myconanoparticles. Biotechnol Rep 18:e00247. https://doi.org/10.1016/j.btre.2018.e00247
Adam N, Schmitt C, De Bruyn L, Knapen D, Blust R (2015) Aquatic acute species sensitivity distributions of ZnO and CuO nanoparticles. Sci Total Environ 526:233–242
Alagesan V, Venugopal S (2019) Green synthesis of selenium nanoparticle using leaves extract of withania somnifera and its biological applications and photocatalytic activities. BioNanoScience 9:105–116
Ali I, Peng C, Khan ZM, Naz I, Sultan M, Ali M, Abbasi IA, Islam T, Ye T (2019) Overview of microbes based fabricated biogenic nanoparticles for water and wastewater treatment. J Environ Manage 230:128–150. https://doi.org/10.1016/j.jenvman.2018.09.073
Barnaby S, Frayne S, Fath K, Banerjee I (2011) Growth of Se nanoparticles on kinetin assemblies and their biocompatibility studies. Soft Mater 9:313–334. https://doi.org/10.1080/1539445X.2010.516302
Beleneva IA, Efimova KV, Eliseikina MG, Svetashev VI, Orlova TY (2019) The tellurite-reducing bacterium Alteromonas macleodii from a culture of the toxic dinoflagellate Prorocentrum foraminosum. Helyon 5:e02435. https://doi.org/10.1016/j.heliyon.2019.e02435
Bondarenko OM, Heinlaan M, Sihtmäe M, Ivask A, Kurvet I, Joonas E, Jemec A, Mannerström M, Heinonen T, Rekulapelly R, Singh S, Zou J, Pyykkö I, Drobne D, Kahru A (2016) Multilaboratory evaluation of 15 bioassays for (eco)toxicity screening and hazard ranking of engineered nanomaterials: FP7 project NANOVALID. Nanotoxicology 10(9):1229–1242. https://doi.org/10.1080/17435390.2016.1196251
Borghese R, Borsetti F, Foladori P, Ziglio G, Zannoni D (2004) Effects of the metalloid oxyanion tellurite (TeO32−) on growth characteristics of the phototrophic bacterium Rhodobacter capsulatus. Appl Environ Microbiol 70:6595–6602. https://doi.org/10.1128/AEM.70.11.6595-6602.2004
Buchs B, Evangelou MVH, Winkel LHE, Lenz M (2013) Colloidal properties of nanoparticular biogenic selenium govern environmental fate and bioremediation effectiveness. Environ Sci Technol 47:2401–2407. https://doi.org/10.1021/es304940s
Castro L, Li J, González F, Muñoz JA, Blázquez ML (2020) Green synthesis of tellurium nanoparticles by tellurate and tellurite reduction using Aeromonas hydrophila under different aeration conditions. Hydrometallurgy 196:105415. https://doi.org/10.1016/j.hydromet.2020.105415
Churchill HOH, Salamo GJ, Yu S-Q, Hironaka T, Hu X, Stacy J, Shih I (2017) Toward single atom chains with exfoliated tellurium. Nanoscale Res Lett 12:488. https://doi.org/10.1186/s11671-017-2255-x
Clinical and laboratory standards institute (CLSI), 2006. Methods for antimicrobial disk susceptibility testing of bacteria isolated from aquatic animals; approved guideline. CLSI, Document M42-A. Wayne, Pennsylvania; ISBN 1-56238-611-5.
Cremonini E, Zonaro E, Donini M, Lampis S, Boaretti M, Dusi S, Melotti P, Lleo M, Vallini G (2016) Biogenic selenium nanoparticles: characterization, antimicrobial activity and effects on human dendritic cells and fibroblasts. Microb Biotechnol 9:758–771
Cruz MD, Mi G, Webster TJ (2018) Synthesis and characterization of biogenic selenium nanoparticles with antimicrobial properties made by Staphylococcus aureus, methicillin-resistant Staphylococcus aureus (MRSA), Escherichia coli, and Pseudomonas aeruginosa. J Biomed Mater Res A 106:1400–1412
Cruz DM, Tien-Street W, Zhang B, Huang X, Crua AV, Nieto-Argüello A, Cholula-Díaz JL, Martínez L, Huttel Y, González MU, García-Martín JM, Webster TJ (2019) Citric juice-mediated synthesis of tellurium nanoparticles with antimicrobial and anticancer properties. Green Chem 21:1982–1988. https://doi.org/10.1039/C9GC00131J
Debieux CM, Dridge EJ, Mueller CM, Splatt P, Paszkiewicz K, Knight I, Florance H, Love J, Titball RW, Lewis RJ, Richardson DJ, Butler CS (2011) A bacterial process for selenium nanospehere assembly. Proc Natl Acad Sci USA 108:13480–13485
Deng Z, Zhang Y, Yue J, Tang F, Wei Q (2007) Green and orange CdTe quantum dots as effective pH-sensitive fluorescent probes for dual simultaneous and independent detection of viruses. J Phys Chem B 111:12024–12031. https://doi.org/10.1021/jp074609z
Dobias J, Suvorova EI, Bernier-Latmani R (2011) Role of proteins in controlling selenium nanoparticle size. Nanotechnology 22:195605
Faramarzi MA, Sadighi A (2013) Insights into biogenic and chemical production of inorganic nanomaterials and nanostructures. Adv Colloid Interface Sci 189–190:1–20. https://doi.org/10.1016/j.cis.2012.12.001
Fellowes JW, Pattrick RA, Lloyd JR, Charnock JM, Coker VS, Mosselmans JF, Weng TC, Pearce CI (2013) Ex situ formation of metal selenide quantum dots using bacterially derived selenide precursors. Nanotechnology 24:145603
Fernandez-Llamosas H, Castro L, Blazquez M, Diaz E, Carmona M (2017) Speeding up bioproduction of selenium nanoparticles by using vibrio natriegens as microbial factory. Sci Rep 7:16046
Forootanfar H, Mahboubeh A, Maryam N, Mitra M, Bagher A, Ahmad S (2014) Antioxidant and cytotoxic effect of biologically synthesized selenium nanoparticles in comparison to selenium dioxide. J Trace Elem Med Biol 28:75–79. https://doi.org/10.1016/j.jtemb.2013.07.005
Forootanfar H, Amirpour-Rostami S, Jafari M, Forootanfar A, Yousefizadeh Z, Shakibaie M (2015) Microbial-assisted synthesis and evaluation the cytotoxic effect of tellurium nanorods. Mater Sci Eng 49:183–189. https://doi.org/10.1016/j.msec.2014.12.078
Gambardella C, Mesarič T, Milivojević T, Sepčić K, Gallus L, Carbone S, Ferrando S, Faimali M (2014) Effects of selected metal oxide nanoparticles on Artemia salina larvae: evaluation of mortality and behavioural and biochemical responses. Environ Monit Assess 186:4249–4259. https://doi.org/10.1007/s10661-014-3695-8
Gupta N, Voloshinov VB, Knyazev GA, Kulakova LA (2011) Optical transmission of single crystal tellurium for application in acousto-optic cells. J Optics 13:055702. https://doi.org/10.1088/2040-8978/13/5/055702
Horie M, Fujita K, Kato H, Endoh S, Nishio K, Komaba LK, Nakamura A, Miyauchi A, Kinugasa S, Hagihara Y, Niki E, Yoshida Y, Iwahashi H (2012) Association of the physical and chemical properties and the cytotoxicity of metal oxide nanoparticles: metal ion release, adsorption ability and specific surface area. Metallomics 4:350–360
Husen A, Siddiqi KS (2014) Plants and microbes assisted selenium nanoparticles: characterization and application. J Nanobiotechnol 12:28. https://doi.org/10.1186/s12951-014-0028-6
Jain R, Dominic D, Jordan N, Rene ER, Weiss S, van Hullebusch ED, Hübner R, Lens PNL (2016) Preferential adsorption of Cu in a multi-metal mixture onto biogenic elemental selenium nanoparticles. Chem Eng J 284:917–925. https://doi.org/10.1016/j.cej.2015.08.144
Kamnev AA, Mamchenkova PV, Dyatlova YA, Tugarova AV (2017) FTIR spectroscopic studies of selenite reduction by cells of the rhizobacterium Azospirillum brasilense Sp7 and the formation of selenium nanoparticles. J Mol Struct 1140:106–112. https://doi.org/10.1016/j.molstruc.2016.12.003
Khanh VN, Hau TN, Gyu MH, Young HK (2019) Kinetics of microbial selenite reduction by novel bacteria isolated from activated sludge. J Environ Manage 236:746–754. https://doi.org/10.1016/j.jenvman.2019.02.012
Kim DH, Kanaly RA, Hur HG (2012) Biological accumulation of tellurium nanorod structures via reduction of tellurite by Shewanella oneidensis MR-1. Biores Technol 125:127–131. https://doi.org/10.1016/j.biortech.2012.08.129
Koketsu T, Paul B, Wu C, Kraehnert R, Huang Y, Strasser P (2016) A lithium–tellurium rechargeable battery with exceptional cycling stability. J Appl Electrochem 46:627–633. https://doi.org/10.1007/s10800-016-0959-8
Kora AJ, Rastogi L (2016) Biomimetic synthesis of selenium nanoparticles by Pseudomonas aeruginosa ATCC 27853: an approach for conversion of selenite. J Environ Manag 181:231–236
Lampis S, Zonaro E, Bertolini C, Cecconi D, Monti F, Micaroni M, Turner RJ, Butler CS, Vallini G (2017) Selenite biotransformation and detoxification by Stenotrophomonas maltophilia SeITE02: Novel clues on the route to bacterial biogenesis of selenium nanoparticles. J Hazard Mat 324:3–14. https://doi.org/10.1016/j.jhazmat.2016.02.035
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 4:3735. https://doi.org/10.1038/srep03735
Libralato G, Prato E, Migliore L, Cicero AM, Manfra L (2016) A review of toxicity testing protocols and endpoints with Artemia spp. Ecol Ind 69:35–49. https://doi.org/10.1016/j.ecolind.2016.04.017
Luyts K, Napierska D, Nemery B, Hoet PHM (2013) How physico-chemical characteristics of nanoparticles cause their toxicity: complex and unresolved interrelations. Environ Sci 15:23–38. https://doi.org/10.1039/C2EM30237C
Molina RC, Burra R, Pérez-Donoso JM, Elias AO, Muñoz C, Montes RA, Chasteen TG, Vasquez CC (2010) Simple, fast, and sensitive method for quantification of tellurite in culture media. Appl Environ Microbiol 76:4901–4904. https://doi.org/10.1128/AEM.00598-10
Mousavi-Kamazani M, Rahmatolahzadeh R, Shobeiri SA, Beshkar F (2017) Sonochemical synthesis, formation mechanism, and solar cell application of tellurium nanoparticles. Ultrason Sonochem 39:233–239. https://doi.org/10.1016/j.ultsonch.2017.04.031
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
Notter DA, Mitrano DM, Nowack B (2014) Are nanosized or dissolved metals more toxic in the environment? A Meta-Analysis. Environ Toxicol Chem 33:2733–2739. https://doi.org/10.1002/etc.2732
Prakash NT, Sharma N, Prakash R, Raina KK, Fellowes J, Pearce CI, Lloyd JR, Pattrick RAD (2009) Aerobic microbial manufacture of nanoscale selenium: exploiting nature’s bio-nanomineralization potential. Biotechnol Lett 31:1857–1862. https://doi.org/10.1007/s10529-009-0096-0
Presentato A, Piacenza E, Darbandi A, Anikovskiy M, Cappelletti M, Zannoni D, Turne RJ (2018) Assembly, growth and conductive properties of tellurium nanorods produced by Rhodococcus aetherivorans BCP1. Sci Rep 8:3923. https://doi.org/10.1038/s41598-018-22320-x
Qiu J, Li N, Lu Z, Yang Y, Ma Y, Niu L, He J, Liu W (2016) Conversion of nornicotine to 6-hydroxy-nornicotine and 6-hydroxy-myosmine by Shinella sp. strain HZN7. Appl Microbiol Biotechnol 100:10019–10029. https://doi.org/10.1007/s00253-016-7805-0
Rajaee Behbahani S, Iranbakhsh A, Ebadi M, Majd A, Ardebili ZO (2020) Red elemental selenium nanoparticles mediated substantial variations in growth, tissue differentiation, metabolism, gene transcription, epigenetic cytosine DNA methylation, and callogenesis in bittermelon (Momordica charantia); an in vitro experiment. PLoS ONE 15:e0235556
Selmani A, Ulm L, Kasemets K, Kurvet I, Erceg I, Barbir R, Pem B, Santini P, Marion ID, Vinković T, Krivohlavek A, Sikirić MD, Kahru A, Vrček IV (2020) Stability and toxicity of differently coated selenium nanoparticles under model environmental exposure settings. Chemosphere 250:126265. https://doi.org/10.1016/j.chemosphere.2020.126265
Shoeibi S, Mashreghi M (2017) Biosynthesis of selenium nanoparticles using Enterococcus faecalis and evaluation of their antibacterial activities. J Trace Elem Med Biol 39:135–139
Srivastava N, Mukhopadhyay M (2013) Biosynthesis and structural characterization of selenium nanoparticles mediated by Zooglea ramigera. Powder Technol 244:26–29. https://doi.org/10.1016/j.powtec.2013.03.050
Srivastava P, Nikhil EVR, Bragança JM, Braganca JM, Kowshik M (2015) Anti-bacterial TeNPs biosynthesized by haloarcheaon Halococcus salifodinae BK3. Extremophiles 19:875–884. https://doi.org/10.1007/s00792-015-0767-9
Tam K, Ho CT, Lee JH, Lai M, Chang CH, Rheem Y, Chen W, Hur HG, Myung NV (2010) Growth mechanism of amorphous selenium nanoparticles synthesized by Shewanella sp. HN-41. Biosci Biotechnol Biochem 74:696–700. https://doi.org/10.1271/bbb.90454
Tan LC, Nancharaiah YV, Lu S, van Hullebusch ED, Gerlach R, Lens PNL (2018) Biological treatment of selenium-laden wastewater containing nitrate and sulfate in an upflow anaerobic sludge bed reactor at pH 5.0. Chemosphere 211:684–693
Tugarova AV, Mamchenkova PV, Dyatlova YA, Kamnev AA (2018) FTIR and Raman spectroscopic studies of selenium nanoparticles synthesised by the bacterium Azospirillum thiophilum. Spectrochim Acta A 192:458–463. https://doi.org/10.1016/j.saa.2017.11.050
Turner RJ, Borghese R, Zannoni D (2012) Microbial processing of tellurium as a tool in biotechnology. Biotechnol Adv 30:954–963. https://doi.org/10.1016/j.biotechadv.2011.08.018
Vahidi H, Kobarfard F, Alizadeh A, Saravanan M, Barabadi H (2021) Green nanotechnology-based tellurium nanoparticles: exploration of their antioxidant, antibacterial, antifungal and cytotoxic potentials against cancerous and normal cells compared to potassium tellurite. Inorg Chem Commun 124:108385. https://doi.org/10.1016/j.inoche.2020.108385
Vaigankar DC, Dubey SK, Mujawar SY, D’Costa A, Shyama SK (2018) Tellurite biotransformation and detoxification by Shewanella baltica with simultaneous synthesis of tellurium nanorods exhibiting photo-catalytic and anti-biofilm activity. Ecotoxicol Environ Saf 165:516–526. https://doi.org/10.1016/j.ecoenv.2018.08.111
Wadhwani SA, Shedbalkar UU, Singh R, Chopade BA (2016) Biogenic selenium nanoparticles: current status and future prospects. Appl Microbiol Biotechnol 100:2555–2566. https://doi.org/10.1007/s00253-016-7300-7
Wadhwani SA, Gorain M, Banerjee P, Shedbalkar UU, Singh R, Kundu GC, Chopade BA (2017) Green synthesis of selenium nanoparticles using Acinetobacter sp. SW30: optimization, characterization and its anticancer activity in breast cancer cells. Int J Nanomed 12:6841–6855. https://doi.org/10.2147/IJN.S139212
Wang T, Yang L, Zhang B, Liu J (2010) Extracellular biosynthesis and transformation of selenium nanoparticles and application in H2O2 biosensor. Colloids Surf B 80:94–102. https://doi.org/10.1016/j.colsurfb.2010.05.041
Wang X, Liu G, Zhou J, Wang J, Jin R, Lv H (2011) Quinone-mediated reduction of selenite and tellurite by Escherichia coli. Bioresour Technol 102:3268–3271. https://doi.org/10.1016/j.biortech.2010.11.078
Wang Z, Bu Y, Zhao Y, Zhang Z, Liu L, Zhou H (2018) Morphology-tunable tellurium nanomaterials produced by the tellurite-reducing bacterium Lysinibacillus sp. ZYM-1. Environ Sci Pollut Res 25:20756–20768. https://doi.org/10.1007/s11356-018-2257-y
Wang L, Li C, Huang Q, Fu X (2019) Biofunctionalization of selenium nanoparticles with a polysaccharide from Rosa roxburghii fruit and their protective effect against H2O2-induced apoptosis in INS-1 cells. Food Funct 10:539–553
Wen H, Zhong J, Shen B, Gan T, Fu C, Zhu Z, Li R, Yang X (2013) Comparative study of the cytotoxicity of the nanosized and microsized tellurium powders on HeLa cells. Front Biol 8:444–450. https://doi.org/10.1007/s11515-013-1266-y
Wu S, Li T, Xia X, Zhou Z, Zheng S, Wang G (2019) Reduction of tellurite in Shinella sp. WSJ-2 and adsorption removal of multiple dyes and metals by biogenic tellurium nanorods. Int Biodeter Biodegrad 144:104751. https://doi.org/10.1016/j.ibiod.2019.104751
Xia X, Zhou Z, Wu S, Wang D, Zheng S, Wang G (2018) Adsorption removal of multiple dyes using biogenic selenium nanoparticles from an Escherichia coli strain overexpressed selenite reductase CsrF. Nanomaterials 8:234. https://doi.org/10.3390/nano8040234
Xu C, Guo Y, Qiao L, Ma L, Cheng Y, Roman A (2018) Biogenic synthesis of novel functionalized selenium nanoparticles by Lactobacillus casei ATCC 393 and its protective effects on intestinal barrier dysfunction caused by enterotoxigenic Escherichia coli K88. Front Microbiol 9:1129
Yadav V, Sharma N, Prakash R, Raina K, Bharadwaj L, Prakash NT (2008) Generation of selenium containing nano-structures by soil bacterium, Pseudomonas aeruginosa. Biotechnol 7:299–304. https://doi.org/10.3923/BIOTECH.2008.299.304
Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Organ Coat 5(2):75–104
Zambonino C, Quizhpe EM, Jaramillo FE, Rahman A, Vispo SN, Jeffryes C, Dahoumane SA (2021) Greens synthesis of selenium and tellurium nanoparticles: current trends, Biological properties and biomedical applications. Int J Mol Sci 22:989. https://doi.org/10.3390/ijms22030989
Zare B, Faramarzi MA, Sepehrizadeh Z, Shakibaie M, Rezaie S, Shahverdi AR (2012) Biosynthesis and recovery of rod-shaped tellurium nanoparticles and their bactericidal activities. Mater Res Bull 47:3719–3725. https://doi.org/10.1016/j.materresbull.2012.06.034
Zhang W, Chen Z, Liu H, Zhang Y, Gao P, Li D (2011) Biosynthesis and structural characteristics of selenium nanoparticles by Pseudomonas alcaliphila. Colloids Surf B 88:196–201. https://doi.org/10.1016/j.colsurfb.2011.06.031
Zonaro E, Lampis S, Turner RJ, Qazi SJS, Vallini G (2015) Biogenic selenium and tellurium nanoparticles synthesized by environmental microbial isolates efficaciously inhibit bacterial planktonic cultures and biofilms. Front Microbiol 6:584. https://doi.org/10.3389/fmicb.2015.00584
Acknowledgements
The authors wish to thank colleagues from the Russian-Vietnamese Tropical Research and Technology Center in Nha Trang (Vietnam) for invaluable assistance during field experiments. The authors also express their great appreciation to Corresponding Member of RAS S.Yu. Bratskaya for kindly providing cancer cell cultures.
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BI and KU conceived the idea, designed the study, performed most of the experiments, interpreted the data and wrote the manuscript. IN carried out the SEM analysis with EDX-ray spectroscopy. KA carried out DNA extraction, PCR amplification and 16rRNA sequencing and processed the resulting data. BA carried out flow cytometric analyses. AG performed Raman spectroscopy. EV secured the funding, supervised the project and revised the manuscript. All authors read and approved the manuscript.
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Beleneva, I.A., Kharchenko, U.V., Kukhlevsky, A.D. et al. Biogenic synthesis of selenium and tellurium nanoparticles by marine bacteria and their biological activity. World J Microbiol Biotechnol 38, 188 (2022). https://doi.org/10.1007/s11274-022-03374-6
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DOI: https://doi.org/10.1007/s11274-022-03374-6