Abstract
This study reports the terrestrial ecotoxicity of the spherical gold nanoparticles with size of 14 ± 3 nm and the negative surface charge of −33 ± 3 mV synthesized by the biomass of Streptomyces rimosus. The impact of these gold nanoparticles on the size and structure of microbial communities in the garden soil was analyzed by the enumeration of culturable soil microorganisms and community level physiological profiles (CLPP). Treatment effects on soil enzymatic activities for β-glucosidase, urease, alkaline phosphatase, and dehydrogenase were followed. Toxicity towards soil microorganisms involved in carbon and nitrogen transformation was determined. The data obtained in this study demonstrate that the biogenic gold nanoparticles up to the concentration of 33 mg kg −1 do not affect the soil processes and can be classified as “not harmful.”
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Abellan MA, Baena CW, Morote FAG, Cordoba MIP, Perez DC, Lucas-Borja ME (2011) Influence of the soil storage method on soil enzymatic activities in Mediterranean forest soils. For Syst 20:379–388
Antisari LV, Carbone S, Gatti A, Vianello G, Nannipieri P (2013) Toxicity of metal oxide (CeO2, Fe3O4, SnO2) engineered nanoparticles on soil microbial biomass and their distribution in soil. Soil Biol Biochem 60:87–94
Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR (2009) Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634–641
Baumann J, Köser J, Arndt D, Filser J (2014) The coating makes the difference: Acute effects of iron oxide nanoparticles on Daphnia magna. Sci Total Environ 484:176–184
Bhatt I, Tripathi BN (2011) Interaction of engineered nanoparticles with various components of the environment and possible strategies for their risk assessment. Chemosphere 82:308–317
Casida L Jr, Klein D, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–377
Chander K, Brookes PC, Harding SA (1995) Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam. Soil Biol Biochem 27:1409–1421
Diegoli S, Manciulea AL, Begum S, Jones IP, Lead JR, Preece JA (2008) Interaction between manufactured gold nanoparticles and naturally occurring organic macromolecules. Sci Total Environ 402:51–61
Dinesh R, Anandaraj M, Srinivasan V, Hamza S (2012) Engeenered nanoparticles in the soil and their potential implications to microbial activity. Geoderma 173–174:19–27
Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:3–11
Fenglerowa W (1965) Simple method for counting Azotobacter in soil samples. Acta Microbiol Pol 14:203–206
Frąc M, Oszust K, Lipiec J (2012) Community level physiological profiles (CLPP), characterization and microbial activity of soil amended with dairy sewage sludge. Sensors 12:3253–3268
Galindo TPS, Pereira R, Freitas AC, Santos-Rocha TAP, Rasteiro MG, Antunes F, Rodrigues D, Soares AMVM, Gonçalves F, Duarte AC, Lopes I (2013) Toxicity of organic and inorganic nanoparticles to four species of white-rot fungi. Sci Total Environ 458–460:290–297
García A, Delgado L, Torŕ JA, Casals E, González E, Puntes V, Font X, Carrera J, Sánchez A (2012) Effect of cerium dioxide, titanium dioxide, silver, and gold nanoparticles on the activity of microbial communities intended in wastewater treatment. J Hazard Mater 199–200:64–72
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole carbon source utilization. Appl Environ Microbiol 57:2351–2359
Goodman CM, McCusker CD, Yilmaz T, Rotello VM (2004) Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjug Chem 2004(15):897–900
Guo SE, Wang E (2007) Synthesis and electrochemical applications of gold nanoparticles. Anal Chim Acta 598:181–192
Haiss W, Thanh NT, Aveyard J, Fernig DG (2007) Determination of size and concentration of gold nanoparticles from UV–vis spectra. Anal Chem 79:4215–4221
Hänsch M, Emmerling C (2010) Effects of silver nanoparticles on the microbiota and enzyme activity in soil. J Plant Nutr Soil Sci 173:554–558
Hattori R, Hattori T (1980) Sensitivity to salts and organic compounds of soil bacteria isolated on diluted media. J Gen Appl Microbiol 26:1–14
Hinojosa MB, Carreira JA, García-Ruíz R, Dick RP (2004) Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biol Biochem 36:1559–1568
Hristozov D, Malsch I (2009) Hazards and risks of engineered nanoparticles for the environment and human health. Sustainability 1:1161–1194
Huang X, Neretina S, El-Sayed MA (2009) Gold nanorods: from synthesis and properties to biological and biomedical applications. Adv Mater 21:4880–4910
ISO (2002) ISO guideline 17155: Soil Quality. Determination of Abundance and Activity of Soil Microflora Using Respiration Curves. International Organization for Standardization, Geneva
Johnson D, Leake JR, Lee JA, Campbell CD (1998) Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands. Environ Pollut 103:239–250
Jones WJ, Ananyeva ND (2001) Correlations between pesticide transformation rate and microbial respiration activity in soil of different ecosystems. Biol Fertil Soils 33:477–483
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination or ammonium. Biol Fertil Soils 6:68–72
Kandeler E, Stemmer M, Klimanek EM (1999) Response of soil microbial biomass, urease and xylanase within particle size fraction to long-term soil management. Soil Biol Biochem 31:205–211
Kathiresan K, Alikunhi NM, Pathmanaban SM, Nabikhan A, Kandasamy S (2010) Analysis of antimicrobial silver nanoparticles synthesized by coastal strains of Escherichia coli and Aspergillus niger. Can J Microbiol 56:1050–1059
Klain SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851
Maliszewska I (2011) Microbial synthesis of metal nanoparticles. In: M. Rai M & Duran N (ed) Metal nanoparticles in microbiology Springer-Verlag Berlin Heidelberg, p 153–176
Maliszewska I (2013) Microbial mediated synthesis of gold nanoparticles: preparation, characterization and cytotoxicity studies. Dig J Nanomater Bios 8:1123–1131
Maliszewska-Kordybach B, Smeeczak B (2003) Habitat function of agricultural soils as affected by heavy metals and polycyclic aromatic hydrocarbons contamination. Environ Int 28:719–728
Merdzan V, Domingos RF, Monteiro CE, Hadiou M, Wilkinson KJ (2014) The effects of different coatings on zinc oxide nanoparticles and their influence on dissolution and bioaccumulation by the green alga, C. reinhartii. Sci Total Environ 488–489:316–324
Mulder EG, Antheumisse J (1963) Morphologie, physiologie et ecologie des Arthrobacter. Ann Inst Pasteur 105:46–74
Nagaraja P, Kumar MH, Yathirajan H, Prakash J (2003) Highly sensitive reaction of nitrate with brucine and 3-methyl-2-benzothiazolinone hydrazone hydrochloride for the determination of nitrate in environmental samples. Anal Sci 19:961–963
Narayanan KB, Sakthivel N (2008) Coriander leaf mediated biosynthesis of gold nanoparticles. Mater Lett 62:4588–4590
Nath D, Banerjee P (2013) Green nanotechnology – a new hope for medical biology. Environ Toxicol Pharmacol 36:997–1014
Nogueira V, Lopes I, Rocha-Santos T, Santos AL, Rasteiro GM, Antunes F, Gonçalves F, Soares AM, Cunha A, Almeida A, Gomes NC, Pereira R (2012) Impact of organic and inorganic nanomaterials in the soil microbial community structure. Sci Total Environ 424:344–350
OECD (2000a) Guideline for Testing of Chemicals 216, Soil Microorganisms: Nitrogen Transformation Test. Organization for Economic Cooperation and Development, Paris
OECD (2000b) Guideline for Testing of Chemicals 217, Soil Microorganisms: Carbon Transformation Test. Organization for Economic Cooperation and Development, Paris
Pereira R, Rocha-Santos TAP, Antunes FE, Rasteiro MG, Ribeiro R, Gonçalves F, Soares AM, Lopes I (2011) Screening evaluation of the ecotoxicity and genotoxicity of soils contaminated with organic and inorganic nanoparticles: the role of ageing. J Hazard Mater 194:345–354
Peric B, Sierra J, Martí E, Cruañas R, Garau MA (2014) A comparative study of the terrestrial ecotoxicity of selected protic and aprotic ionic liquids. Chemosphere 12, doi: 10.1016/j.chemosphere.2014.02.043
Philip D (2009) Honey mediated green synthesis of gold nanoparticles. Spectrochim Acta A 73:650–653
Prem LK, Kumar S, Srivastava AK, Sharma AK (2013) Myconanotechnology in agriculture: a perspective. World J Microbiol Biotechnol 29:191–207
Priyadarshini E, Pradhan N, Sukla LB, Panda PK, Mishra BK (2013) Biogenic synthesis of floral-shaped gold nanoparticles using a novel strain, Talaromyces flavus. Ann Microbiol. doi:10.1007/s13213-013-0744-4
Quester K, Avalos-Borja M, Castro-Longoria E (2013) Biosynthesis and microscopic study of metallic nanoparticles. Micron 54–55:1–27
Radada K, Al-Shraimb M, Moldzioc R, Rauschc WD (2012) Recent advances in benefits and hazards of engineered nanoparticles. Environ Toxicol Pharmacol 34:661–672
Ros M, Goberna M, Pascual JA, Klammer S, Insam H (2008) 16S rDNA analysis reveals low microbial diversity in community level physiological profile assays. J Microbiol Methods 72:221–226
Sadowski Z, Maliszewska I (2011) Applications of gold nanoparticles : current trends and future prospects. In: M. Rai M and Duran N (ed) Metal Nanoparticles in Microbiology. Springer-Verlag Berlin Heidelberg, p 225–248
Shah V, Belozerova I (2009) Influence of metal nanoparticles on the soil microbial community and germination of lettuce seeds. Water Air Soil Pollut 197:143–148
Sperling RA, Gil PR, Zhang F, Zanella M, Parak WJ (2008) Biological applications of gold nanoparticles. Chem Soc Rev 37:1896–1908
Sukul P (2006) Enzymatic activities and microbial biomass in soil as influenced by metalaxyl residues. Soil Biol Biochem 38:320–326
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Biol Biochem 1:301–307
Tong Z, Bischoff M, Gnies L, Applegate B, Turco RF (2007) Impact of fullerene (C60) on a soil microbial community. Environ Sci Technol 41:2985–2991
United Nations (2006) Globally Harmonized System of classification and labeling of chemicals. UN/SCEGHS/12/INF5. New York, USA
Yen HJ, Hsu SH, Tsai CL (2009) Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 13:1553–1561
Zaborowska M, Wyszkowska J, Kucharski J (2006) Microbial activity in zinc contaminated soil of different pH. Pol J Environ Stud 15:569–574
Acknowledgments
This work was partially financed by a statutory activity subsidy from the Polish Ministry of Science and Higher Education (PMSHE) for the Faculty of Chemistry of Wrocław University of Technology, NCN grant (NN507515058). I would like to thank Marta Pacia for technical support in carrying out the experimental work and Prof. J. Sołoducho (Wrocław University of Technology) for helpful consultation on the manuscript.
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Maliszewska, I. Effects of the biogenic gold nanoparticles on microbial community structure and activities. Ann Microbiol 66, 785–794 (2016). https://doi.org/10.1007/s13213-015-1158-2
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DOI: https://doi.org/10.1007/s13213-015-1158-2