Skip to main content

Advertisement

Log in

Assessment of biotoxicity of Cu nanoparticles with respect to probiotic strains of microorganisms and representatives of the normal flora of the intestine of broiler chickens

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Copper nanoparticle Cu (d = 55 ± 15 nm) and CuO nanoparticles (d = 90 ± 10 nm) were used in the studies (OOO Platina, Russia). Using the method of pure cultures, we extracted Lactobacillus, Enterococcus, and Enterobacterium from the intestines of broilers. Additionally, strains of Bacillus subtilis 10641 and Bifidobacterium were involved in probiotic strains. The data obtained in the course of the study testify to the insignificant biotoxicity of copper nanoparticles with respect to representatives of the genera Lactobacillus (30 to 15 μg/ml) and Bifidobacterium (30 μg/ml), with the most sensitive bacteria being the genus Lactobacillus, for which a concentration of 7.5 μg/ml was subinhibitory. The second stage was the study using method of agar wells. In the course of the experiment, we obtained results confirming the data of the research by the serial dilution method. In this case, as in the first case, the data indicate the insignificant biotoxicity of copper nanoparticles in relation to representatives of the genera Lactobacillus and Bifidobacterium. We have studied the bioaccumulating ability of microorganisms of the studied metals. In all the studies carried out, as in the first series of experiments, representatives of the genera Lactobacillus and Bifidobacterium with the lowest bioaccumulative ability were the most sensitive to copper nanoparticles and were 3.1 and 8.2%, respectively. The use of nanoparticles as a component of the fodder additive in small concentrations does not adversely affect not only the probiotic strains, but also the main representatives of the normoflora (Lactobacillus, Enterococcus, and Enterobacterium) of the poultry, the positive effect of the copper nanoparticles being directly related to low level of dissociation of nanoparticles, since biologically active ions will be released much more slowly, thereby creating a prolonged effect of exposure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmadi F, Ebrahimnezhad Y, Sis NM, Ghalehkandi JG (2013) The effects of zinc oxide nanoparticles on performance, digestive organs and serum lipid concentrations in broiler chickens during starter period. Int J Biosci 7(23):23–29. https://doi.org/10.12692/ijb/3.7

    Article  Google Scholar 

  • Auffan, M, Flahaut, E, Thill A, Mouchet F, Carriere M, Gauthier L, Bottero JY (2011) Ecotoxicology: nanoparticle reactivity and living organisms. In Nanoethics and nanotoxicology, Springer Berlin Heidelberg, рр. 325–357

  • Beveridge TJ, Murray RG (1980) Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol 141(2):876–887

    CAS  Google Scholar 

  • Bogoslovskaya OA, Sizova EA, Polyakova VS, Miroshnikov SA, Leipunsky IO, Olkhovskaya IP, Glushchenko NN (2009) Investigation of the safety of the introduction of copper nanoparticles with different physicochemical characteristics into the animal organism. Vestnik OGU 2:124–127

    Google Scholar 

  • Chen M, Yamamuro S, Farrell D, Majetich SA (2003) Gold-coated iron nanoparticles for biomedical applications. J Appl Phys 93(10):7551–7553

  • Churilov GI, Ivanycheva Y, Ampleev LE, Nazarova A, Zheglov T, Polishchuk S (2009) Introduction to the diet of rabbits wikis grown using ultrafine cobalt powders. Krolikovodstvo i zverovodstvo 1:16–17

    Google Scholar 

  • Claudio DM, Rojasa R (2006) Copper accumulation by bacteria and transfer to scallop larvae. Mar Pollut Bull 52(3):293–300

    Article  CAS  Google Scholar 

  • Ezhkov AM, Yapparov AK, Motina TY, Yapparov IA, Yezhkov VO (2015) Quality of meat of broiler chickens using the feed additive of nanosized bentonite. Glavnyj zootekhnik 1:45–49

    Google Scholar 

  • Folmanis GE, Kovalenko LV (2006) Biologically active iron nanopowders. MGOU Publishing House, Moscow

    Google Scholar 

  • Fondevila M, Herrer R, Casallas MC, Abecia L, Ducha JJ (2009) Silver nanoparticles as potential antimicrobial additive for weaned pigs. Anim Feed Sci Technol 150:259–269. https://doi.org/10.1016/j.anifeedsci.2008.09.003

    Article  CAS  Google Scholar 

  • Galagudza MM, Korolev DV, Sonin DL, Aleksandrov IV, Postnov VN, Papayan GV, Shlyakhto EV (2010) Passive directed delivery of drugs to the ischemic myocardium using silica nanoparticles. Rossijskie nanotekhnologii 11-12:125–130

    Google Scholar 

  • Glushchenko NN, Bogoslovskaya OA, Olkhovskaya IP (2006) Comparative toxicity of salts and metal nanoparticles and their biological effect. Proceedings of the Academy of Industrial Ecology 3:46–47

  • Glushchenko NN, Bogoslovskaya OA, Baitukalov TA, Olkhovskaya IP (2008) Nanoparticles of metals in bioelementology. Mikroehlementy v medicine 1-2:52

    Google Scholar 

  • Gusev AI (2005) Nanomaterials, nanostructures, nanotechnologies. Moscow, Fizmatlit

    Google Scholar 

  • Hussain N, Jaitley V, Florence AT (2001) Recent advances in the understanding of uptake of microparticles across the gastrointestinal lymphatics. Adv Drug Deliv Rev 50:107–142

    Article  CAS  Google Scholar 

  • Isajkina EY, Sizentsov AN, Bunina AU, Shablo AS, Ovsyannikova DC (2015) Study of the bioaccumulating ability of probiotic preparations for the intoxication of laboratory animals with copper. Izvestia ОGAU 1(51):147–149

    Google Scholar 

  • Kasemets K, Ivask A, Dubourguier HC, Kahru A (2009) Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol in Vitro 23(6):1116–1122

    Article  CAS  Google Scholar 

  • Kaweeteerawat C, Chang CH, Roy KR, Liu R, Li R, Toso D, Zhou ZH (2015) Cu nanoparticles have different impacts in Escherichia coli and Lactobacillus brevis than their microsized and ionic analogues. ACS Nano 9(7):7215–7225

    Article  CAS  Google Scholar 

  • Kensova R, Blazkova I, Vaculovicova M, Milosavljevic V, Blazkova L, Hynek D, Kopel P, Novotna M, Zehnalek J, Pohanka M, Trnkova L, Adam V, Kizek R (2015) The effect of cadmium ions and cadmium nanoparticles on chicken embryos and evaluation of organ accumulation. Int J Electrochem Sci 10:3623–3634

    CAS  Google Scholar 

  • Kim JH, Cho H, Ryu SE, Choi MU (2000) Effects of metal ions on the activity of protein tyrosine phosphatase VHR: highly potent and reversible oxidative inactivation by Cu2+ ion. Arch Biochem Biophys 382(1):72–80

    Article  CAS  Google Scholar 

  • Koch AM, Reynolds F, Merkle HP, Weissleder R, Josephson L (2005) Transport of surface-modified nanoparticles through cell monolayers. Chem bio chem 6(2):337–345

    Article  CAS  Google Scholar 

  • Kvan OB, Rusakova EA, Sizentsov AN, Kataev VY (2014) Effect of probiotic drugs on the content of toxic elements in the body of laboratory animals. Vestnik OGU 6(167):64–66

    Google Scholar 

  • Liang X, Sun M, Li L, Qiao R, Chen K, Xiao Q, Xu F (2012) Preparation and antibacterial activities of polyaniline/Cu0.05Zn0.95O nanocomposites. Dalton Trans 41(9):2804–2811

    Article  CAS  Google Scholar 

  • Lin YE, Vidic RD, Stout JE, McCartney CA, Yu VL (1998) Inactivation of Mycobacterium avium by copper and silver ions. Water Res 32(7):1997–2000

    Article  CAS  Google Scholar 

  • Makarov DV (2014) Forecast of the development of the world market of nanopowders. Vestnik KRAUNC Fiziko-matematicheskie nauki 1:97–102

    Google Scholar 

  • Maynard AD (2006) Nanotechnology: a research strategy for addressing risk. Woodrow Wilson International Center for Scholars, Washington, DC, USA

    Google Scholar 

  • Mroczek-Sosnowska N, Łukasiewicz M, Wnuk A, Sawosz E, Niemiec J, Skot A, Jaworski S, Chwalibog A (2016) In ovo administration of copper nanoparticles and copper sulfate positively influences chicken performance. J Sci Food Agric 96:3058–3062. https://doi.org/10.1002/jsfa.7477

    Article  CAS  Google Scholar 

  • Niazi JH, Gu MB (2009) Toxicity of metallic nanoparticles in microorganism—a review. In Atmospheric and biological environmental monitoring, Ed. Y. J. Kim, Ed. Springer Science+Business Media

  • Ognik K, Sembratowicz I, Cholewińska E, Wlazło Ł, Nowakowicz-Dębek B, Szlązak R, Tutaj K (2016) The effect of chemically-synthesized silver nanoparticles on performance and the histology and microbiological profile of the jejunum in chickens. Ann Anim Sci 16:439–450. https://doi.org/10.1515/aoas-2015-0067

    Article  CAS  Google Scholar 

  • Peshkov SA, Sizentsov AN, Nikiyan AN, Kobzev GI (2015) Study of the bioaccumulation of heavy metals by bacteria of the genus Bacillus using X-ray fluorescence analysis and atomic force microscopy. Sovremennye problemy nauki i obrazovanija 4:50–53

    Google Scholar 

  • Pineda LM, Chwalibog A, Sawosz E, Lauridsen C, Engberg RM, Elnif J, Hotowy A, Sawosz F, Ali A, Gao Y, Moghaddam HS (2012a) Effect of silver nanoparticles on growth performance, metabolism and microbial profile of broiler chickens. Arch Anim Nutr 66:416–429. https://doi.org/10.1080/1745039X.2012.710081

    Article  CAS  Google Scholar 

  • Pineda L, Sawosz E, Hotowy A, Elnif J, Sawosz F, Ali A, Chwalibog A (2012b) Effect of nanoparticles of silver and gold on metabolic rate and development of broiler and layer embryos. Comp Biochem Physiol A Mol Integr Physiol 161(3):315–319

  • Presnyak AR (2015) The use of micronutrient nanoparticles is a promising direction in the production of chicken broilers. Molodoj uchenyj 5(2):40–42

    Google Scholar 

  • Refaie AM, Ghazal MN, Easa FM, Barakat SA, Ge Y, Wh E (2015) Nano-copper as a new growth promoter in the diet of growing New Zealand white rabbits. Egypt J Rabbit Sci 25(1):39–57

    Google Scholar 

  • Rohner F, Ernst FO, Arnold M, Hilbe M, Biebinger R, Ehrensperger F, Pratsinis SE, Langhans W, Hurrell RF, Zimmermann MB (2007) Synthesis, characterization, and bioavailability in rats of ferric phosphate nanoparticles. J Nutr 137(3):614–619

    Article  CAS  Google Scholar 

  • Ruparelia JP, Chatterjee AK, Duttagupta SP, Mukherji S (2008) Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomater 4(3):707–716

    Article  CAS  Google Scholar 

  • Sahoo SK, Labhasetwar V (2003) Nanotech approaches to drug delivery and imaging. Drug Discov Today 73:1112–1120. https://doi.org/10.1016/S1359-6446(03)02903-9

    Article  CAS  Google Scholar 

  • Santos A, Mauro MS, Diaz DM (2006) Prebiotics and their long-term influence on the microbial populations of the mouse bowel. Food Microbiol 23:498–503. https://doi.org/10.1016/j.fm.2005.07.004

    Article  CAS  Google Scholar 

  • Sawosz E, Binek M, Grodzik M, Zieliska M, Sysa P, Szmidt M, Niemiec T, Chwalibog A (2007) Influence of hydrocolloidal silver nanoparticles on gastrointestinal microflora and morphology of enterocytes of quails. Arch Anim Nutr 61:444–451. https://doi.org/10.1080/17450390701664314

    Article  CAS  Google Scholar 

  • Schwegmann H, Frimmel FH (2010) Nanoparticles: interaction with microorganisms. In: Frimmel FH, Niessner R (eds) Nanoparticles in the water cycle. Springer, Berlin, Germany

    Google Scholar 

  • Sizentsov AN, Barysheva ES, Babushkina AE (2015) The ability of probiotic preparations based on bacteria of the genus Bacillus to bioaccumulate heavy metal ions in the body of laboratory animals. Russ Immunol J 9(2):753–755

    Google Scholar 

  • Sizentsov AN, Kvan OV, Babushkina АЕ, Исайкина Isajkina EY (2016) Bioaccumulative ability of bacteria of the genus Bacillus against lead ions under in vitro and in vivo conditions. Izvestia ОGAU 2(58): С.186–188

  • Sizova EA (2010) Mineral composition and morphofunctional aspects of liver reorganization in the enteral method of introducing copper nanoparticles such as CU10X. Vestnik Orenburgskogo gosudarstvennogo universiteta 6:92–94

    Google Scholar 

  • Sizova EA, Korolev VL, Makaev SA, Miroshnikova EP, Shakhov VA (2016) Morpho-biochemical indicators of blood in broilers when correcting the diet with salts and nanoparticles Cu. Sel'skohozyajstvennaya biologiya 6:903–911

    Article  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336. https://doi.org/10.1016/0891-5849(94)00159-H

    Article  CAS  Google Scholar 

  • Taylor AA, Marcus IM, Guysi RL, Walker SL (2015) Metal oxide nanoparticles induce minimal phenotypic changes in a model colon gut microbiota. Environ Eng Sci 32:602–612. https://doi.org/10.1089/ees.2014.0518

    Article  CAS  Google Scholar 

  • Tsao N, Luh TY, Chou CK, Chang TY, Wu JJ, Liu CC, Lei HY (2002) In vitro action of carboxyfullerene. J Antimicrob Chemother 49(4):641–649

    Article  CAS  Google Scholar 

  • Vishnyakov AI, Ushakov AS, Lebedev SV (2011) Features of bone marrow hematopoiesis when copper nanoparticles are introduced per os and intramuscularly. Vestnik myasnogo skotovodstva 54:96–102

    Google Scholar 

  • Wang Z, Li N, Zhao J, White JC, Qu P, Xing B (2012) CuO nanoparticle interaction with human epithelial cells: cellular uptake, location, export, and genotoxicity. Chem Res Toxicol 25(7):1512–1521

    Article  CAS  Google Scholar 

  • Wang С, Wang MQ, Ye SS, Tao WJ, Du YJ, Wang C (2011) Effects of copper-loaded chitosan nanoparticles on growth and immunity in broilers. Poult Sci 90(10):2223–2228. https://doi.org/10.3382/ps.2011-01511

    Article  CAS  Google Scholar 

  • Yapparov AH, Aliev SA, Yapparov IA, Ezhkova AM, Degtyareva IA, Yezhkov VO (2014) Scientific substantiation of obtaining nanostructured and nanocomposite materials and technology of their use in agriculture. Kazan': Centr innovacionnyh tekhnologij

  • Yausheva EV, Miroshnikov SA, Kosyan DB, Sizova ЕА (2016) Nanoparticles in combination with amino acids change productive and immunological indicators of broiler chicken. Agric Biol 51:912–920. https://doi.org/10.15389/agrobiology.2016.6.912eng

    Article  Google Scholar 

  • Yausheva EV, Miroshnikov SA, Kvan OV (2013a) On the understanding of the biological effect of metal nanoparticles. Voprosy biologicheskoj, medicinskoj i farmacevticheskoj himii 9:54–56

    Google Scholar 

  • Yausheva EV, Zelepukhin AG, Ryabov NI, Kvan OV, Ramensky VA, Zaveryukha AK, Sirazetdinov FK (2013b) Investigation of metal nanoparticles as a source of microelements for animals. Sovremennye problemy nauki i obrazovaniya 5:470

    Google Scholar 

  • Yoon K, Hoon Byeon J, Park JH, Hwang J (2007) Susceptibility constants of Escherichia coli and Bacillus subtilis to silver and copper nanoparticles. Sci Total Environ 373(2–3):572–575

    Article  CAS  Google Scholar 

Download references

Funding

This research was carried out with the financial support of the Russian Ministry of Science and Education as part of the base part of the state task to carry out research projects in the Orenburg State University (No. 6.6811.2017/Ch).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Irina Aleksandrovna Gavrish.

Ethics declarations

The studies were carried out under the conditions of the experimental and biological clinic of the Orenburg State University on broiler chickens (Smena 8). Experimental studies were conducted in accordance with the instructions recommended by the Russian Regulations, 1987, and “The Guide for the Care and Use of Laboratory Animals (National Academy Press Washington, D.C. 1996).”

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sizentsov, A.N., Kvan, O.V., Miroshnikova, E.P. et al. Assessment of biotoxicity of Cu nanoparticles with respect to probiotic strains of microorganisms and representatives of the normal flora of the intestine of broiler chickens. Environ Sci Pollut Res 25, 15765–15773 (2018). https://doi.org/10.1007/s11356-018-1761-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-1761-4

Keywords

Navigation