Biosynthesis and effects of copper nanoparticles on plants

Environ Chem Lett DOI 10.1007/s10311-017-0615-5 REVIEW Biosynthesis and effects of copper nanoparticles on plants Ramesh Chand Kasana1 • Nav Raten Panwar1 • Ramesh Kumar Kaul2 Praveen Kumar3 • Received: 14 February 2017 / Accepted: 21 February 2017 Ó Springer International Publishing Switzerland 2017 Abstract Copper nanoparticles have improved properties compared to the bulk copper material. Copper nanoparticles indeed find applications in gas sensors, heat transfer fluids, catalysis, solar energy and batteries. Antibacterial and antifungal activities of copper nanoparticles find applications in the agriculture and healthcare sectors. Nonetheless, careless use of copper nanoparticles may cause environmental pollution and health effects. Here we review the biosynthesis of copper nanoparticles using plant materials, named phytosynthesis, and micro-organisms. We also discuss the effect of copper nanoparticles on crops and pathogenic micro-organisms. Copper nanoparticles varying in sizes from 5 to 295 nm have been synthesized using leaf extracts and latex from plants, and using bacteria and fungi. Biosynthesized copper nanoparticles show good antimicrobial activity inhibiting the growth of pathogenic bacteria and pathogenic fungi. Copper nanoparticles enhance the germination and growth of some plants at lower concentrations, whereas high concentrations result in retarded growth. & Ramesh Chand Kasana [email protected] 1 Division of Natural Resources and Environment, ICARCentral Arid Zone Research Institute, Jodhpur, Rajasthan 342003, India 2 Division of Plant Improvement, Propagation and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, Rajasthan 342003, India 3 Division of Integrated Land Use Management and Farming System, ICAR-Central Arid Zone Research Institute, Jodhpur, Rajasthan 342003, India Keywords Copper nanoparticles
Biosynthesis
Antimicrobial activity
Pathogenic micro-organisms
Agriculture crops
Phytosynthesis Introduction Increasing agriculture production in economized way without polluting the environment is a global challenge. Agriculture and healthcare sectors have witnessed great strides during recent past; still, many developing countries face the threat of food/healthcare insecurity (Husen and Siddiqi 2014). Exploiting the latest innovations in the field of nanobiotechnology, researchers are trying to develop alternative antimicrobial agents including cationic polymers, metal nanoparticles and antimicrobial peptides against drug resistance micro-organisms (Ren et al. 2009; Ahamed et al. 2014). In agriculture, nanotechnology has found wider applications in post-harvest storage of food products, but its application in improving crop productivity is recent one. At present attention is being paid to increase the crop yield through nanotechnological interventions by enhancing plant growth and reducing the impact of abiotic and biotic stresses. Copper an essential micronutrient being incorporated into many proteins and enzymes has a significant role in the health and nutrition of plants. Copper has an outstanding electrical conductivity, good catalytic behaviour and surface enhanced Raman scattering activity; hence, copper nanoparticles have attracted the attention of researches for using it as an essential component in the future nanodevices (Chandra et al. 2014). Copper nanoparticles have also gained importance due to their widespread applications as antimicrobials, in gas sensors, electronics and coating on textiles, batteries, solar energy conversion tools and high- 123 Environ Chem Lett temperature superconductors (Chen et al. 2012). Copper nanoparticles effectively inhibit growth of many pathogens such as Staphylococcus aureus, Bacillus subtilis, Escherichia coli, Shigella dysenteriae, Salmonella typhi, Klebsiella pneumoniae (Cioffi et al. 2005; Abboud et al. 2014; Ahamed et al. 2014; Sutradhar et al. 2014; Naika et al. 2015) and are being used as antibacterial additive for food packaging applications (Longano et al. 2012). Antifungal activity shown by copper nanoparticles against various plant pathogenic fungi makes them a good candidate for plant disease management (Giannousi et al. 2013; Kanhed et al. 2014; Shende et al. 2015; Bramhanwade et al. 2016). Despite many valuable uses of nanoparticles, the fate and effect of nanoparticles on environment are a matter of concern (Schilling et al. 2010; Song et al. 2015). The potential risks associated with production and application of copper nanoparticles therefore need to be investigated before releasing them into public domain. This article is an abridged version of the chapter published by Kasana et al. 2016 (Chapter 5: Copper Nanoparticles in Agriculture: Biological Synthesis and Antimicrobial Activity) in the book series Sustainable Agriculture Reviews (http://www. springer.com/series/8380). Phytosynthesis of copper nanoparticles Phytosynthesis of copper nanoparticles have been carried out by using various plants and salts of copper such as copper acetate, copper sulphate and copper nitrate. Starting with copper acetate as substrate, copper nanoparticles of 15 and 40 nm were synthesized by using Calotropis procera latex and flowers broth of Aloe vera (Harne et al. 2012; Karimi and Mohsenzadeh 2015). Addition of Centella asiatica leaves extract to copper acetate formed copper nanoparticles ranging from 2 to 5 lm (Devi and Singh 2014). Phytosynthesis of copper nanoparticles ranging from 5 to 93 nm using copper sulphate and leaf extract from Syzygium aromaticum, Tabernaemontana divaricate, Vitis vinifera, brown alga Bifurcaria bifurcata extract and fruit juice of Citrus medica has been achieved (Subhankari and Nayak 2013; Sivaraj et al. 2014; Angrasan and Subbaiya 2014; Abboud et al. 2014; Shende et al. 2015; Nagaonkar et al. 2015). Copper oxide nanoparticles of 110–280 nm were synthesized by adding copper sulphate to flowers extract of Cassia alata (Jayalakshmi and Yogamoorthi 2014). Using copper nitrate and extract from tea leaf, coffee powder, Andean blackberry fruit and leaf resulted in the synthesis of copper oxide nanoparticles ranging from 50 to 100 nm (Sutradhar et al. 2014; Kumar et al. 2015). Copper nanoparticles of 5–10 nm were obtained by using Gloriosa 123 superba extract and cupric nitrate (Naika et al. 2015). Detailed list of various plant materials and salts used for phytosynthesis of copper nanoparticles, synthesis method and averages size of nanoparticles are summarized in Table 1. Biosynthesis of copper nanoparticles using microorganisms Micro-organisms serve as a good source for biosynthesis of nanoparticles because of biochemical diversity, easy and fast cultivation under laboratory conditions. Various approaches used for biosynthesis of nanoparticles utilizing microbes are shown in Fig. 1. Bacterium belonging to the genus Serratia isolated from an insect Stibara species was first micro-organism reported for synthesis of copper nanoparticles of 10–30 nm using 5 mM copper sulphate (Hasan et al. 2008). Spherical copper nanoparticles of 8–15 nm were produced by Pseudomonas stutzeri (Varshney et al. 2010), whereas quasi-spherical nanoparticles ranging from 10 to 40 nm were produced by Escherichia coli and Morganella morganii (Singh et al. 2010; Ramanathan et al. 2013). Copper nanoparticles of 79–295 nm were produced by using copper sulphate and extracellular metabolites from Penicillium aurantiogriseum, P. citrinum and P. waksmanii (Honary et al. 2012). Copper nanoparticles of 24.5 and 87.5 nm were produced by using dead biomass of Hypocrea lixii and Trichoderma koningiopsis, respectively (Salvadori et al. 2013, 2014). Copper nanoparticle with average size of 49 nm were synthesized by using culture supernatant from Pseudomonas fluorescens MTCC103 and Salmonella typhimurium (Shantkriti and Rani 2014; Ghorbani et al. 2015). Copper/copper oxide nanoparticles of 5–20 nm were synthesized by using a fungus Stereum hirsutum and copper salts (Cuevas et al. 2015). An overview of concentration of salts, micro-organisms and biosynthesis conditions is given in Table 2. Above review clearly brought out that by using various plant materials and micro-organisms, both fungi and bacteria copper nanoparticles of different shape and size have been synthesized. Though the nanoparticles can be synthesized by using extracts from various plants, more emphasis should be placed on microbial synthesis keeping in mind that commercial biosynthesis using plant extracts is not a viable strategy due to requirement of large quantity of raw material. Micro-organisms can be grown and multiplied under the laboratory conditions; moreover, they can be manipulated and operated for optimal production of nanoparticles, making micro-organisms more suitable for commercial production of copper nanoparticles. Cu(NO3)2 Gloriosa superba L. extract 0.1 M Cu(NO3)2 5 mM Cu(CH3COO)2 Aloe vera flowers broth Solanum tuberosum starch extract 100 mM CuSO4 Citrus medica Linn fruit juice 0.001 M Cu(NO3)2 1 mM CuSO4 Bifurcaria bifurcata (Alga) extract Garcinia mangostana leaf extract 54 nm Added extract to CuSO4 and heated at 50 °C 1% Cu(CH3COO)2 Centella asiatica leaf extract 1 mM CuSO4 Cu(NO3)2 Tea leaf extract/or coffee powder extract Cu(NO3)2 1.0 mM CuSO4 Cassia alata flowers extract Citrus medica fruit extract 1 mM CuSO4 Vitis vinifera leaf extract Rubus glaucus Benth. fruit/leaf extract 5–10 nm Added extract to Cu(NO3)2 and incubated at 400 °C for 3–4 min CuSO4 Tabernaemontana divaricate leaf extract Added Cu(NO3)2 to extract with stirring Added extract to Cu(NO3)2 and kept on water bath at 70 °C Added extract to Cu(NO3)2 with stirring at 75–80 °C Added extract to Cu(CH3COO)2 and incubated at 50 °C in a steam bath 54 nm 26.51 nm 43.3/52.5 nm 40 nm 33 nm Added juice to CuSO4 and heated at 60–100 °C Alishah et al. (2016) Prabhu et al. (2015) Kumar et al. (2015) Nagaonkar et al. (2015) Naika et al. (2015) Karimi and Mohsenzadeh (2015) Shende et al. (2015) Abboud et al. (2014) Devi and Singh (2014) 2–5 lm 5–45 nm Sutradhar et al. (2014) Jayalakshmi and Yogamoorthi (2014) Angrasan and Subbaiya (2014) Sivaraj et al. (2014) Subhankari and Nayak (2013) Harne et al. (2012) References 50–100 nm 110–280 nm – 46 nm 5–40 nm Added extract to CuSO4 with constant stirring at 100–120 °C Added extract to Cu(CH3COO)2 under constant stirring Extract and Cu(NO3)2 subjected to microwave heating at 540 W for 7–8 min Added CuSO4 to extract under stirring and incubated at 80 °C Added extract to CuSO4 and incubated in darkroom Added extract to CuSO4 under constant stirring Added extract to CuSO4 and incubated for 1 h 0.001 M CuSO4 Syzygium aromaticum extract 15 nm Added latex to Cu(CH3COO)2 with shaking 3.0 mM Cu(CH3COO)2 Calotropis procera L. latex Size Synthesis conditions Salt and concentration Name of the plant material Table 1 Phytosynthesis of copper nanoparticles: various plant materials used to synthesize copper nanoparticles of different size form various salts are summarized below Environ Chem Lett 123 Environ Chem Lett Fig. 1 Microbial synthesis of copper nanoparticles is carried out by one of these methods: (1) to micro-organisms growing in growth medium copper salt is added; (2) to microbial biomass taken in water copper salt is added; (3) to extracellular secretion from micro- organisms copper salt is added. Then incubation is done at a suitable temperature. Synthesized nanoparticles as observed using particles size analyser and transmission electron microscope Antimicrobial activity of copper nanoparticles inhibitory concentration of copper nanoparticles ranged from 31.25 to 250 lg/ml against Escherichia coli, Enterococcus faecalis, Pseudomonas aeruginosa, Shigella flexneri, Salmonella typhimurium, Proteus vulgaris, Staphylococcus aureus and Klebsiella pneumoniae (Ahamed et al. 2014). Gloriosa superba synthesized copper nanoparticles of 5–10 nm exhibited antibacterial activity against Klebsiella aerogenes, Pseudomonas desmolyticum, Escherichia coli and Staphylococcus aureus (Naika et al. 2015). Using 20 ll of copper nanoparticles of 33 nm synthesized by Citrus medica showed inhibitory activity against Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Propionibacterium acnes and Salmonella typhi (Shende et al. 2015), while 100 ll of copper nanoparticles of 26.51 nm synthesized using Garcinia mangostana at 0.2–1.0 lg/ml concentrations showed antibacterial activity against Escherichia coli and Staphylococcus aureus (Prabhu et al. 2015). Monodisperse copper nanoparticles of 50 nm have minimum inhibitory concentration ranging between 1.875 and 3.75 lg/ml against standard and clinical strains of Staphylococcus, including methicillin-resistant Staphylococcus aureus, and Candida species (Kruk et al. 2015). Copper oxide nanoparticles of 54 nm synthesized using Solanum tuberosum showed This section deals with antimicrobial activity studies conducted using different concentrations of copper nanoparticles against human pathogenic bacteria belonging to various genera and species. Using 100 ll of copper oxide nanoparticles of 46 nm synthesized by Tabernaemontana divaricate at concentration of 50 ug/ml in well plate method showed 17 mm zone of inhibition against urinary tract pathogen Escherichia coli (Sivaraj et al. 2014). Twenty microlitre of copper nanoparticles of 5–45 nm synthesized using brown alga Bifurcaria bifurcata showed inhibition zone of 14 and 16 mm, respectively, against Enterobacter aerogenes and Staphylococcus aureus (Abboud et al. 2014). Copper oxide nanoparticles synthesized by tea leaf or coffee powder extract exhibited inhibition zone of 5–16 mm against Shigella dysenteriae, Vibrio cholerae, Streptococcus pneumoniae, Staphylococcus aureus and Escherichia coli at concentration from 1 to 200 lg/ disc (Sutradhar et al. 2014). Using 40 ll of Vitis vinifera synthesized copper nanoparticles showed inhibition zone from 8 to 18 mm against Bacillus subtilis, Escherichia coli, Klebsiella pneumoniae, Salmonella typhi and Staphylococcus aureus (Angrasan and Subbaiya 2014). Minimum 123 Pellet (8 g) from 15 days grown culture was put in water and incubated under shaking for 24 h. After addition of salts to supernatant again incubated under shaking Grew in broth and then supernatant was added to Cu(NO3)2 318, 750, 1000 ppm CuSO4 100 mg/l CuSO4 100 mg/l CuCl2 1 mM CuSO4 1, 3 and 5 mM CuSO4 1 mM CuSO4 5 mM CuCl2, Cu(NO3)2 and CuSO4 1 mM Cu(NO3)2 Pseudomonas fluorescens Trichoderma koningiopsis Hypocrea lixii Pseudomonas stutzeri Penicillium aurantiogriseum, P. citrinum, P. waksmanii Escherichia coli Stereum hirsutum Salmonella typhimurium Grew in citrate medium for 15 h under shaking. Suspended 30 g biomass in 100 ml CuSO4 and incubated under shaking Grew in broth for 10 days then to 100 ml supernatant added 100 ml of CuSO4 49 nm 5–20 nm spherical 10–40 nm quasi-spherical 79–295 nm spherical Ghorbani et al. (2015) Cuevas et al. (2015) Singh et al. (2010) Honary et al. (2012) Varshney et al. (2010) 8–15 nm spherical Grew in broth for 24 h and 0.1 g biomass was added to 100 ml CuSO4. Incubated under shaking Salvadori et al. (2013) 24.5 nm spherical Grew in broth for 5 days under shaking, then pellet dried at 50 °C was ground to obtain uniformly sized particles Salvadori et al. (2014) Shantkriti and Rani (2014) Hasan et al. (2008) 87.5 nm spherical 49 nm spherical and hexagonal 10–30 nm Ramanathan et al. (2013) References Dried pellets from 5 days grown culture was used to synthesize copper nanoparticles utilizing CuSO4 Grew in broth under shaking and suspended 1 g biomass in 20 ml of CuSO4. Incubate under shaking Grew in broth for 24 h and to pellet added CuSO4. Incubate under shaking 1, 3, 5, 7 and 10 mM CuSO4 Serratia 19.2 nm quasi-spherical After 24 h of growth added CuSO4 and incubated at 37 °C under shaking 5 mM CuSO4 Morganella morganii Particle size and shape Synthesis conditions Salt and concentration Micro-organism Table 2 Biosynthesis of copper nanoparticles by micro-organisms: bacteria and fungi synthesizing copper nanoparticles of different size and shape form various salts are summarized below Environ Chem Lett 123 Environ Chem Lett minimum inhibitory concentration and minimum bactericidal concentration ranging between 200 and 1000 lg/ml against Bacillus cereus, Enterococcus, Escherichia coli, Pseudomonas aeruginosa, Shigella sonnei and Staphylococcus epidermidis (Alishah et al. 2016). Good antimicrobial activity shown by copper nanoparticles against the pathogenic bacteria belonging to various genera and species suggests their use as antimicrobial agent. Copper nanoparticles with antimicrobial activity can be employed for the production of a broad range of polymer/copper nanocomposites to be used in the preparation of antibacterial paints/coatings for application in household, biomedical and aerospace industries. Furthermore, copper nanoparticles embedded into polymer matrix can be employed in the food packaging for delaying of deterioration, shelf life extension, maintaining quality and safety of packaged food. Impact of copper nanoparticle on agriculture crops The impact of nanoparticles on plants is depended on many parameters starting from composition, concentration, size and physical to chemical properties of nanoparticles as well as plant species under study (Shalaby et al. 2016). Metaland metal oxide-based nanomaterials act as mediators of DNA damage in living organisms, but the molecular mechanisms by which damage occurs are poorly studied (Atha et al. 2012). Under controlled laboratory conditions, copper nanoparticles at different concentrations from 200 to 1000 mg/l negatively impacted the growth of plant seedling of Phaseolus radiates and Triticum aestivum (Lee et al. 2008). Copper oxide nanoparticle inhibited the growth of Raphanus sativus, Lolium perenne, and Lolium rigidum (Atha et al. 2012). Seed germination in Glycine max and Cicer arietinum occurred up to 2000 ppm of copper oxide nanoparticles of \50 nm, but the root growth was prevented above 500 ppm (Adhikari et al. 2012). At 50–500 mg/l copper oxide nanoparticles reduced the growth of Glycine max in 1/2 strength Murashige and Skoog medium (Nair and Chung 2014a). Copper oxide nanoparticles at concentration above 2 mg/l showed significant reduction in plant biomass and total chlorophyll content of Arabidopsis thaliana. However, there was increase in anthocyanin, lipid peroxidation and amino acid proline content at concentrations above 5 mg/l (Nair and Chung 2014b). Copper nanoparticles up to 20 lg/ml increased mitotic index of actively dividing cells in Allium cepa with gradual decline in mitotic index as the concentration increased (Nagaonkar et al. 2015). Copper oxide nanoparticles showed significant increase in germination, shoot and root length in deteriorated 123 (artificially aged) seeds of maize hybrid cv. Hema (Maithreyee and Gowda 2015). Application of copper nanoparticles ranging from 0.2 to 1.0 ppm blended in Murashige and Skoog medium resulted in significant increase in various agronomic parameters of wheat, but concentration above 2 ppm showed deleterious effects. However, soil application of copper nanoparticles at concentrations from 10 to 30 ppm in pots significantly increased growth and yield of wheat (Hafeez et al. 2015). Exposing germinating seedlings of chickpea and Oryza sativa to copper oxide nanoparticles above 50 mg/l resulted in toxic response (Nair and Chung 2015; Costa and Sharma 2016). Copper oxide nanoparticles at concentrations above 10 mg/l significantly inhibited the growth of transgenic and conventional cotton. However, copper oxide nanoparticles enhanced the expression of the exogenous gene encoding for Bt toxin protein in leaves and roots at low concentrations of 10 mg/l, providing insect resistance in Bt cotton (Van et al. 2016). Exposure of aquatic macrophyte Lemna gibba plants to copper oxide nanoparticles resulted in inhibition of photosynthetic activity (Perreault et al. 2014). From the review of the literature on impact of copper nanoparticle on plants, it is clear that barring few examples copper nanoparticles do not have much effect on germination and growth of plants. However, studies on effect of copper nanoparticles gain importance for exploring the nanoparticles for diseases management without impacting the plant growth. Disease management using copper nanoparticles Many fungal and bacterial pathogens cause diseases in agriculture crops leading to yield losses. The antimicrobial activity shown by copper nanoparticles against broad range of pathogenic micro-organisms both bacteria and fungi has created interest in assessing the role of nanoparticles for disease control in agriculture. Studies carried on in vitro antifungal activity of copper nanoparticles reported the maximum antifungal activity against Curvularia lunata MTCC 2030 followed by Alternaria alternata MTCC6572, Fusarium oxysporum MTCC1755 and Phoma destructive DBT66 (Kanhed et al. 2014). Copper nanoparticles synthesized using Citrus medica also demonstrated inhibitory activity against plant pathogenic fungi, Fusarium culmorum, F. oxysporum and F. graminearum (Shende et al. 2015). In another study, copper nanoparticles showed maximum antifungal activity against Fusarium equiseti with 25 mm zone of inhibition followed by F. oxysporum and F. culmorum (Bramhanwade et al. 2016). Copper nanoparticles of 20–50 nm at a concentration of 450 ppm could inhibit 93.98% growth of the Fusarium sp after 9 days of incubation (Viet et al. 2016). Copper-based fungicide has been used in Environ Chem Lett disease prevention and treatment in many plant species (Borkow and Gabbay 2005). Field studies under protected cultivation using three different copper-based nanoparticles of similar sizes, i.e. 11–14 nm and shapes, Cu2O, CuO and Cu/Cu2O, respectively, against Phytophthora infestans on Lycopersicon esculentum showed that copper-based nanoparticles were more effective than the four registered copper-based agrochemicals. Along with the promising efficacy, it was also found that copper-based nanoparticles did not induce any permanent damage/deleterious effect to the plants (Giannousi et al. 2013). In exploring copper nanoparticles for disease management, it is the beginning which has to go long way for protecting the plants from various diseases in sustainable manner. Conclusion The diverse properties, applications and production economics make copper nanoparticles as one of the important nanomaterials among others. Synthesis of copper nanoparticles can be carried out by physical and chemical methods, but in recent past biological methods are being preferred due to the ease in production and environmental concerns. The biosynthesized copper nanoparticles have shown some encouraging results against plant pathogens, but their application in field is yet in very preliminary stages. 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