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Scientific Reports Volume 11, Article Number: 17125 (2021) Cite this article

The extensive use of pesticides in global agricultural production has attracted much attention because of their many adverse effects on human health and the environment. In recent years, the use of nanotechnology has become a tool to overcome these adverse effects. The purpose of this work is to test different particles (zinc oxide (ZnO MPs) and silica particles (SiO2 MPs)) and silver nanoparticles (Ag NPs) and study their toxicity to the model organism Tenebrio molitor. A comprehensive comparative study was conducted, which included more than 1,000 mealworms divided into nine different groups. In addition to the pure nano/microparticle solution, the effect of particles mixed with the microalgae extract Chlamydomonas reinhardtii was also observed. Compared with pure ZnO MPs, pure Ag NPs and SiO2 MPs caused more than 70% larval mortality, of which the mortality was about 33%. The death rate caused by the mixture of algae extract and zinc oxide particles is twice the death rate observed with pure ZnO MP. At the same time, atomic absorption spectroscopy (AAS) is used to determine the difference in the concentration of trace elements in dead larvae and live larvae.

Therefore, the increase in the global population has increased the demand for food, leading to an increase in global agricultural production, and more effective strategies are needed to optimize agricultural strategies that mainly target biological stress factors1. In today's agriculture, although pesticides have harmful effects on human health and the environment, their use is still inevitable. Unmanaged and excessive use of pesticides can cause various problems because it pollutes our ecosystems, including waterways, sediments, and soil, and is transferred through residues in the food chain2. However, there is an urgent need to find new products that are more effective, more specific, and less toxic to the environment. The use of genetically modified plants is still controversial, and so far, the EU has rarely supported it. Therefore, other ways to achieve sustainable agriculture are being looked for. Nanotechnology, mainly nanoparticles, is a material that is currently in-depth research in the field of medicine, materials industry, cosmetics, and agriculture3. In recent years, it has been reported that different nanoparticles/particulates (NPs/MPs) have a variety of properties and can be used for different applications in agriculture, such as fertilizers or pesticides. Several groups have reported the beneficial and/or harmful effects of different nanoparticles/particles on seed germination, root elongation and seedling growth4,5,6. In the initial stages of development, the potential of nanoparticles as new pesticides has been explored. In most cases, evidence has been found that they are toxic to selected pests, but have limited impact on non-target species. However, the lack of knowledge about the possible health effects on humans and the environment hinders their practical application and limits their many advantages as pesticides8,9,10,11.

The main idea behind our work is to show that nano/microparticles have the potential to provide effective solutions and help create new pesticides with higher insecticidal activity and less environmental persistence. In this study, commercially available zinc oxide nanoparticles (after our use-micro particles, ZnO MPs), silica nanoparticles (after our use-micro particles, SiO2 MPs) and silver nanoparticles (Ag NPs) ) And its efficiency at the 16th larval stage studied the yellow mealworm beetle (T. molitor). T. molitor is the most important food product storage pest in the world15. The control of stored-grain pests mainly relies on the extensive effects of pesticides16. Silica is the main component of agricultural soil, and zinc is an essential micronutrient for plant growth. Zinc is widely distributed in plant tissues and participates in many metabolic processes. Its deficiency reduces growth, stress tolerance and chlorophyll synthesis13. Silver is not necessary for plants, but it can stimulate plant productivity at low doses14. We compared the mortality during the application of ZnO MPs, SiO2 MPs, Ag NPs and Chlamydomonas reinhardtii extracts, and their effects on T. molitor with particles. The algae C. reinharditii belongs to unicellular flagellates and has been described as producing extracellular metabolites (1-tetradecene, phenol, 2,4-di-tert-butyl-, 1-pentadecene, 1-octadecene Carbene, 1-nonadecene, etc.) and antibacterial, anti-oxidant and anti-cancer activities, which have been proven by many studies16,17,18,19. In addition, the application of algae in the production of biological pesticides is becoming more and more attractive. Algae and its biologically active compounds have been used to study fungi, bacteria or insect pathogens in plants such as corn, sunflower, potato, tomato or watermelon. Such compounds mainly come from bromophenols, polyphenols, alkaloids or terpenoid metabolites. At present, the specific compounds involved are being studied in depth.

Commercial zinc oxide nanoparticles (SkySpring Nanomaterials, Inc., Houston, USA, 20–30 nm), silica nanoparticles (SiO2 NPs, Sigma-Aldrich®, 10–20 nm) and silver nanoparticles (Ag NPs, US Research Nanomaterials, 10 nm) is obtained in powder form. Disperse the received powder in water (20 g/L), sonicate for 10 minutes, and then dilute to the desired concentration.

Disperse the sample in the solution and dilute with demineralized water. Then, the sample was applied to Siegert Wafer Company's silicon wafer and dried at laboratory temperature (23 °C). The wafer is adhered to the short post inserted into the SEM with carbon conductive tape. The samples were inspected by SEM on Tescan MAIA 3 equipped with FEG (Tescan Ltd., Brno, Czech Republic). The image was recorded using an In-Lens SE detector at a working distance between 2.92 and 2.99 mm and an accelerating voltage of 5 kV under high vacuum conditions. The 768 × 858 pixel image was obtained at 100,000 times magnification, covering a 2.08 µm sample area. Performing full-frame capture in ultra-high (UH) resolution mode and enabling image offset correction through image accumulation takes approximately 0.5 minutes and approximately 0.32 microseconds/pixel dwell time. The spot size is set to 2.4 nm. The size of the nanoparticles was confirmed by dynamic light scattering technology (Malvern Instrument Ltd, UK). The Zn NPs and SiO2 NPs were sonicated in distilled water. After this treatment, the larger nanoparticles aggregate into microparticles.

The algae were cultured in Erlenmeyer flasks under aseptic conditions, cultured in Tris-acetic acid-phosphate (TAP) liquid medium at 22 ± 1 °C, and irradiated with 130 μmol m-2 s-1, 12 h light/ 12 h dark light cycle. After 7 days of cultivation, Chlamydomonas reinhardtii was freeze-dried for 24 hours (Feezone 2.5 freeze dryer, LBSCONCO), and 500 mg of biomass was dissolved in 200 mL of distilled water. Then, the solution was heated at 100 °C and sonicated in an ultrasonic bath (K-5 LM, Kraintek sro) for 10 minutes.

The working solution of ordered nano/microparticles is made in distilled water or by mixing with algae extracts. In addition, the adjuvant silwet star-shaped surfactant (SS) is added to each suspension because it helps the nanoparticles/particles to pass through the wax structure 20. Water lacking nanoparticles was used as a blank treatment.

To prepare the ZnO MP working solution, dissolve 5 mL of ZnO MP stock solution (20 g/L) in 45 mL of distilled water to obtain a final concentration of 2 g/L MP. Subsequently, 50 µL SS was added.

ZnO MPs algae extract is prepared by mixing 5 mL ZnO MPs (20 g/L), 45 mL Chlamydomonas reinhardtii extract and 50 µL SS.

To prepare a working solution of silica particles, mix 2.5 mL (20 g/L) of SiO2 particles with 47.5 mL of distilled water or algae extract and 50 µL of SS to obtain the required particle concentration of 1 g/L.

Prepare a solution of silver nanoparticles in water or algae extract by mixing 1.25 mL of Ag NP stock solution (20 g/L) and 48.75 mL of water or extract. The final silver content of these suspensions is 0.5 g/L.

Tenebrio molitor larvae are purchased from an animal store, and routinely cultured and reared in a petri dish (⌀ 90 mm) under laboratory conditions (25 ± 2 °C). During the experiment, the larvae were divided into nine different groups, each containing 150 mealworms (3 P. plates containing 50 mealworms). Then spray the larvae directly with the prepared NP/MP solution (approximately 170 µL per spray) for five days, and record the mortality of mealworms every 24 hours until the fifth day. Before treatment, the solution was sonicated for five minutes and sprayed. The mortality percentage of T. molitor is calculated by using the Henderson-Tilton formula. Collect dead larvae and live larvae, wash 3 times with distilled water, and then freeze-dry for 48 hours (Feezone 2.5 freeze dryer, LBSCONCO).

Then, weigh 0.2 g of freeze-dried mealworms into the digestion container. The digestion mixture (10 ml of 63% ultrapure HNO3 diluted 1:1 (v/v) with Milli-Q water (Merck, Millipore)) was added to 0.2 g of lyophilized mealworms. The sample was digested with the Ethos One microwave digestion system (Milestone, Italy) at 210 °C for 30 minutes. After digestion, store the sample in a plastic tube at 4 °C, protected from light.

A 240FS Agilent Technologies Atomic Absorption Spectrometer (Agilent, Santa Clara, USA) was used to determine the concentration of zinc and silver in digested mealworm samples by flame atomization and deuterium background correction. The instrument is operated under the conditions recommended by the manufacturer. The air-acetylene flame (flow rate 13.5 L/min and 2.0 L/min) uses an ultra-sensitive hollow cathode lamp (Agilent Technologies, Santa Clara, CA, USA) as the radiation source Zn (213.9 nm) ) And Ag (328.1 nm).

The content of Zn MPs and Ag NPs in the AAS analysis is expressed as the average relative standard deviation (RSD) in the Microsoft Excel program and R version 4.0.4. R core team (2020). R: A language and environment for statistical calculations. R Statistical Computing Foundation, Vienna, Austria. URL https://www.R-project.org/.

In recent years, the use of common fumigants and insecticides to control pests stored in grain has led to insect resistance22. At the same time, these pesticides are toxic to animals that feed on grain23. Pesticide residues are then transferred to animals and then to humans, so alternative strategies to protect stored grains need to be found. Nanotechnology and nanoparticles are now entering the field of agricultural biotechnology24,25. Slowing down the release kinetics of pesticides and reducing the amount of application are the main advantages of nanoparticles26. Recently, people have become more and more interested in the research of NPs and NPs as potential pesticides. Nanoparticles (NPs) have been tested against different kinds of pests, such as Coleoptera, Lepidoptera, Hemiptera, Diptera, such as silver (Ag), gold (Au), aluminum (Al), and silica ( Si) and zinc (Zn) and metal oxides, zinc oxide (ZnO) and titanium dioxide (TiO2) 22, 27, 28, 29, 30, 31, 32, 33.

To determine the size and shape of the nanoparticles, SEM was used. Figure 1 shows that the average diameter of the nanoparticles in the solution after sonication is larger than the diameter declared by the manufacturer. The microscopic images show that the particles are spherical in shape and composed of aggregates of a few microns in diameter, as shown in the images (Figure 1A, B, C). The SEM micrographs of Ag NPs showed that the aggregates consisted of fine-structured particles of various sizes. Dynamic light scattering (DLS) analysis also confirmed this. The same results were obtained using Zn nanoparticles and SiO 2 nanoparticles. The obtained results show their difference distribution curve, which is consistent with the SEM results (Figure 1D). The particle size analyzed by DLS shows that the average size of Ag NPs is 530 nm, and the average size of SiO2 MPs and ZnO MPs is 777 nm (2355 nm). In addition, the surface charge and colloidal stability of the nanoparticles used were determined by analysis of zeta potential. The zeta potentials of nanoparticles dispersed in water to Ag NPs, SiO2 MPs and ZnO MPs are -24.2 mV, -30.2 and -28.7 mV, respectively. These values ​​are slightly below the threshold of -30 mV, which is considered to be the minimum zeta potential for electrostatically stable suspensions.

(A) SEM images of Ag NPs, (B) SiO2 MPs and (C) ZnO MPs. (D) DLS size distribution curve of nanoparticles in aqueous solution.

This research is dedicated to studying the effects of NPs/MPs and NPs/MPs and algae extracts on the viability of T. molitor 16 in the larval stage, and to examine their insecticidal effects. The efficiency of selected nanoparticles/particles (ZnO MPs, SiO2 MPs and Ag NPs) on T. molitor was tested at concentrations of 2 g/L, 1 g/L and 0.5 g/L, as shown in Figure 2. Mortality was monitored for 5 days, and the results were collected every 24 hours. Select selected concentrations of NPs/MPs based on preliminary experiments.

Mortality of Tenebrio molitor larvae after using pure 2 g/L ZnO MPs, 1 g/L SiO2 MPs and 0.5 g/L Ag NPs and the combination of these MPs/NPs and Chlamydomonas reinhardtii extract. (A) The number of dead larvae within 5 days. Three spray treatments: 0, 48 hours, and 96 hours. 150 mealworms are used for each treatment. (B) Percentage of total mortality after 120 hours. The mortality rate is measured by the Henderson-Tilton formula 20.

Our results show that the activity of Chlamydomonas reinhardtii extract is negligible (14%) when tested alone, while increased mortality was observed when treated with ZnO MPs in water and mixed with algae extracts. The mortality rate of larvae treated with ZnO MP was 33%, while the mortality rate when mixed with Chlamydomonas reinhardtii was 66%. Recent studies on Chlamydomonas reinhardtii have shown its antioxidant activity and antibacterial potential against different strains. This activity is believed to be related to its main extracellular metabolites.

In fact, 1-nonadecene, 1-octadecene, 1-tetradecene and diisooctyl phthalate have been shown to have insecticidal or antibacterial activity against several species35. Although the mechanism of the Chlamydomonas reinhardtii extract is not discussed in detail here, the increased larvicidal activity of the nanoparticles and its extract may be due to the action of biologically active compounds such as phenolic compounds and flavonoids16,36. Previous studies on the antibacterial activity of ZnO nanoparticles hypothesized that reactive oxygen species (ROS) generated on the surface of ZnO nanoparticles trigger irreversible damage to the cell wall of microorganisms. Together with the active molecules from algae extracts, it can cause damage to cell integrity and ultimately lead to the death of pathogens.

It can be seen from Figure 2 that the difference between different nanoparticle treatments is obvious; however, this is to be expected, because when linked to factors such as composition, shape, size, and surface area to volume ratio, NPs/ The impact of MPs is more complicated. The different mechanisms by which the nanoparticles act may be the main reason for the observed differences in activity. In our experiments, silver nanoparticles are the most effective against mealworms. Compared with the untreated control, the larval effect of 0.5 g/L Ag NPs on larvae was confirmed. It is not clear what makes Ag NPs less effective when used in combination with algae extracts. One of the hypotheses may be the fact that metabolites of algae extract have bound to the surface of NPs, thereby inactivating the activity of silver NPs. However, this statement needs to be studied in more detail in further experiments. Silver has been commonly used as an ingredient in many plant antimicrobial preparations.

The toxicity of silver ions is well known, and it has been reported that one of the possible mechanisms relies on the ability of silver ions to bind to cysteine-containing proteins, leading to the rupture of pathogen membranes38.

Many studies have described the insecticidal effects of silica nanoparticles31,39,40,41. The reported potential mode of action is through the drying of the insect epidermis after the nanoparticles have absorbed the epidermal lipids and destroyed the structure. Exposure of T. molitor larvae to silica particles causes approximately 71% mortality and darkens the stratum corneum of the dead larvae. We confirmed the hypothesis that SiO2 NPs damage the epidermis and dermal cells, causing dehydration of the larvae, making them look dark. This morphological change in the presence of silica MPs is consistent with a decrease in cell viability43 and may therefore be considered to be related to the death of larvae caused by drying.

Table 1 shows the statistical analysis of Verticillium wilt mortality expressed as mean ± SD using Tukey HSD extrapolation. All treatments were compared with control samples (treated with water). The samples treated with 0.1% Silwet Star surfactant are insignificant. The pure Chlamydomonas reinhardtii extract showed statistical significance (*p <0.05). Compared with the control sample, the other samples showed a significant difference (** p <0.01).

Similarly, compared with their bulk materials, silicon, titanium dioxide, copper, aluminum oxide, zinc and silver nanoparticles have become potential candidates for combating different agricultural pests, improving plant response to various biotic and abiotic stresses, and improving plant growth performance. 44,45 ,46. In addition, the toxicity of nanoparticles to pests may have multiple mechanisms. Certain nanoparticles can penetrate and accumulate in cell membranes, which may cause cell lysis, while other nanoparticles may stimulate the production of cellular ROS, leading to loss of cell function and cell death47,48.

The accumulation of ZnO MPs and Ag NPs was estimated by atomic absorption spectroscopy (AAS). Due to technical reasons, we cannot measure the accumulation (content) of silicon in black moth larvae. The zinc and silver concentrations in live and dead larvae (Table 2) are expressed in mg/kg. The zinc content was determined in all larvae tested (Table 2). However, in the larvae treated with ZnO MPs, a higher zinc concentration was observed compared to the larvae not treated with ZnO MPs. The highest value of zinc (268.01 ± 9.20) was measured in dead larvae sprayed with 2 g/L ZnO MPs solution of algae extract and live larvae sprayed with the same solution (225.41 ± 6.20). The increase in zinc concentration in dead/live larvae indicates that these MPs are able to pass through the larval cuticle when mixed with algae extract. The water spray control sample contained a significant p <0.001 minus 48.02 ± 4.60 Zn in live larvae; in contrast, the measured zinc content in dead larvae was 70.00 ± 9.60 mg/kg.

All arthropods contain high concentrations of zinc, iron, manganese and other trace elements and heavy metals in their bodies. These metals are part of the body's epidermis 49, 50, 51. Zinc is an important part of more than 300 enzymes and transcription factors. In addition to the epidermal part of the body and enzyme complexes, zinc also plays a role in DNA synthesis, which is essential for the normal physiological functions of insects, and is also present in the area around the midgut (including Malpigh tubules) in pupae and adults 52,53 . In order to maintain homeostasis and reduce toxicity, the content of micronutrients is regulated. The excretion rate of zinc does not exceed the accumulation rate before approaching the toxic level, so more zinc is accumulated than needed. Mir et al.54 studied the accumulation of zinc in the whole body of the silkworm (Bombyx mori) insect that was fed leaves treated with ZnO NPs. In their experiments, they found that zinc accumulated in the body for 6 hours, after which its level began to drop.

Table 2 also shows the total content of silver nanoparticles (Ag NPs). Silver was only detected in larvae treated with Ag NPs, with or without algae extracts. The highest content of Ag NPs (16.54 ± 6.90 mg/kg) was measured in mealworm carcasses treated with Ag NPs and algae extracts. In contrast, the lowest measured silver content recorded in the bodies of live larvae treated with pure silver NPs (6.02 ± 4.30). Similar values ​​were measured in living bodies of mealworms (12.24 ± 5.90) ​​treated with Ag NPs and Chlamydomonas reinhardtii extracts and dead larvae treated with pure Ag NPs (12.89 ± 4.80). Silver cannot be detected in other samples because silver is not an essential micronutrient in living organisms. Although silver is not a part of cells and tissues, it has good antibacterial and insecticidal effects. It can induce cytotoxicity, increase ROS production, and cause DNA damage and apoptosis55, 56. Ionic silver strongly interacts with thiol groups and inactivates important enzymes 57,58. At present, silver nanoparticles have received high attention. Various studies have shown that Ag NPs can distribute and accumulate in certain organs of the body after exposure59,60. Silver nanoparticles have an impact on the development and growth of larvae, the duration of larval and pupal stages, and the viability of adults​​. It was found that as the exposure dose increased, the number of Ag NPs in Drosophila melanogaster increased. Even if the organism was not exposed, the insects could accumulate silver in the tissues for a long time. Further studies have also found that Ag NPs will accumulate in the body after application, leading to blackening of the body, and insecticidal effect on the model organism Drosophila melanogaster 61.

New tools for the management and control of agriculturally important pests are needed. In some cases, inorganic, raw nanoparticles that are not intentionally produced for insecticidal applications, such as the metal/metal oxide form of nanoparticles, may trigger this biological effect62,63. Here, we evaluated the larvicidal potential of three different types of commercially available nanoparticles on the survival rate of Tenebrio molitor at the sixteenth larval stage. Our results show that pure silver nanoparticles and silica particles have an insecticidal effect of more than 70% on larval vigor. In addition, we explored the efficiency of nano/microparticles in the presence of the algae Chlamydomonas reinhardtii extract. Compared with pure ZnO MPs (33%), the combination of algae extract and ZnO MPs doubled the mortality of larvae (66%). In contrast, compared with pure silver nanoparticles (76%), algae extract reduced the effectiveness of silver nanoparticles and the mortality rate was reduced to 11%. The components of algae extracts are considered safe for human health and the environment. This article shows that these active molecules can provide solutions and strategies for pest control by improving insecticidal effects.

This article does not contain any research conducted by any author on human participants or animals.

All designated authors have read and approved the final manuscript. We guarantee the originality of the presented works and do not consider publishing in other places.

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This work was financially supported by the internal funding agency of the Faculty of Agriculture of Mendel University in Brno. AF-IGA2019-IP036. We thank Dr. Pavel Svec and Dr. Lukas Richtera for the possibility of using SEM.

Department of Chemistry and Biochemistry, Faculty of Agricultural Sciences, Mendel University, Brno, Zemedelska 1, 613 00, Brno, Czech Republic

Ivan Rankic, Radim Zelinka, Andrea Ridoskova, Milica Gagic, Pavlina Pelcova and Dalibor Huska

Central European Institute of Technology, Brno University of Technology, Purkynova 123, 612 00, Brno, Czech Republic

Ivan Ranch and Milika Gaggic

Central European Institute of Technology, Brno Mendel University, Zemedelska 1, 613 00, Brno, Czech Republic

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IR and DH designed experiments and wrote manuscripts; IR, RZ, and MG performed experiments; AR and PP performed atomic absorption spectroscopy and statistical evaluation of the data; DH, PP and AR performed critical editing of the manuscript.

The author declares no competing interests.

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Rankic, I., Zelinka, R., Ridoskova, A. etc. Nano/microparticles combined with microalgae extracts are used as new insecticides against yellow mealworms and yellow mealworms. Scientific Representative 11, 17125 (2021). https://doi.org/10.1038/s41598-021-96426-0

DOI: https://doi.org/10.1038/s41598-021-96426-0

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