Abstract
Mosquitoes are a vector for many dreadful diseases known for their public health concern. The continued use of synthetic insecticides against vector control has led to serious environmental impacts, human health problems, and the development of insect resistance. Hence, alternative mosquito control methods are needed to protect the environment and human health. In the present study, the bioefficacy of (2-(((2-ethyl-2 methylhexyl)oxy)carbonyl) benzoic acid isolated from Bacillus pumilus were tested against Aedes aegypti, Culex quinquefasciatus and Anopheles stephensi. The isolated bioactive compound was characterized through thin layer chromatography (TLC), UV–visible spectroscopy (UV), Fourier-transform infrared spectroscopy, nuclear magnetic resonance spectroscopy, and gas chromatography–mass spectrometry analysis. The pure compound caused a high percent mortality rate in a dose-dependent manner, the obtained values were 96, 82, 69, 50 and 34%; 86, 72, 56, 43, and 44%; 100, 90, 83, 70 and 56% against Ae. aegypti, Cx. quinquefasciatus, and An. stephensi respectively. The effective lethal concentration values (LC50) were 13.65, 14.90 and 9.64 ppm against Ae. aegypti, Cx. quinquefasciatus, An. Stephensi, respectively. The effect of (2-(((2-ethyl-2 methylhexyl)oxy)carbonyl) benzoic acid significantly increased the superoxide dismutase, catalase, α, β esterase and Glutathione-S-transferase level after 24 h of the treatment period. The comet assay confirmed that isolated compound causes DNA damage in all tested insects. Histopathological examinations of treated larvae showed shrunken body posture, damaged epithelial cells and microvillus as compared to control organisms. The biosafety of the isolated compound was assessed against G. affinis and did not produce mortality which confirmed that the activity of the isolated compound is species specific. The current study concludes that the critical success factors of new insecticidal agent development are based on the eco-compatibility and alternative tools for the pesticide producing industry.
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References
Abbott W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:256–267
Abd-El-Kareem F, Elshahawy IE, Abd-Elgawad MMM (2021) Application of Bacillus pumilus isolates for management of black rot disease in strawberry. Egypt J Biol Pest Control 31:25. https://doi.org/10.1186/s41938-021-00371-z
AhbiRami R, Zuharah WF, Thiagaletchumi M, Subramaniam S, Sundarasekar J (2014) Larvicidal efficacy of different plant parts of railway creeper, Ipomoea cairica extract against dengue vector mosquitoes, Aedes albopictus (Diptera: Culicidae) and Aedes aegypti (Diptera: Culicidae). J Insect Sci 1(14):180. https://doi.org/10.1093/jisesa/ieu042
Ahmad S, Abdel-Salam NM, Ullah R (2016) In vitro antimicrobial bioassays, DPPH radical scavenging activity, and FTIR spectroscopy analysis of Heliotropium bacciferum. Biomed Res Int. https://doi.org/10.1155/2016/3818945
Ali S, Zhang C, Wang Z et al (2017) Toxicological and biochemical basis of synergism between the entomopathogenic fungus Lecanicillium muscarium and the insecticide matrine against Bemisia tabaci (Gennadius). Sci Rep 7:1–14. https://doi.org/10.1038/srep46558
Alves GB, Melo FL, Oliveira EE et al (2020) Comparative genomic analysis and mosquito larvicidal activity of four Bacillus thuringiensis serovar israelensis strains. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-60670-7
Ayalew AA (2020) Insecticidal activity of Lantana camara extract oil on controlling maize grain weevils. Toxicol Res App 4:1–10. https://doi.org/10.1177/2397847320906491
Balaraju K, Maheswaran R, Agastian P, Ignacimuthu S (2009) Egg hatchability and larvicidal activity of Swertia chirata buch. - hams ex wall. against aedes aegypti L. and Culex quinquefasciatus say Indian. J Sci Technol 2:46–49. https://doi.org/10.17485/ijst/2009/v2i12/29558
Baskar K, Maheswaran R, Ignacimuthu S (2012) Bioefficacy of Ceasalpinea bonduc (L.) Roxb. against Spodoptera litura Fab. (Lepidoptera: Noctuidae). Arch Phytopathol Plant Prot 45:1127–1137. https://doi.org/10.1080/03235408.2012.657931
Baskar K, Maheswaran R, Pavunraj M et al (2018) Toxicity and antifeedant activity of Caesalpinia bonduc (L.) Roxb. (Caesalpiniaceae) extracts and fractions against the cotton bollworm Helicoverpa armigera hub. (Lepidoptera: Noctuidae). Physiol Mol Plant Pathol 101:69–74. https://doi.org/10.1016/j.pmpp.2017.01.006
Bradford MM (1976) A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/j.cj.2017.04.003
Cabrera CVP, Selvaraj JJ (2020) Geographic shifts in the bioclimatic suitability for Aedes aegypti under climate change scenarios in Colombia. Heliyon 6(1):e03101
Cengiz EI, Unlu E (2006) Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: a microscopic study. Environ Toxicol Pharmacol 21:246–253. https://doi.org/10.1016/j.etap.2005.08.005
Datta R, Kaur A, Saraf I et al (2020) Assessment of genotoxic and biochemical effects of purified compounds of Alpinia galanga on a polyphagous lepidopteran pest Spodoptera litura (Fabricius). Phytoparasitica 48:501–511. https://doi.org/10.1007/s12600-020-00813-8
Deepali K, Sneha P, Sucheta P (2014) Larvicidal activity of rhamnolipid biosurfactant produced by Stenotrophomonas maltophilia. Int J Sci Eng Res 5:60–63
Deepika L, Kannabiran K (2010) Antagonistic activity of Streptomyces VITDDK1 spp. (GU223091) isolated from the coastal region of Tamil Nadu. India Pharmacol Online 1:17–29
ECDC (2022) European centre for disease prevention and control-vector-borne diseases. Found at: https://www.ecdc.europa.eu/en/climate-change/climate-change-europe/vector-borne-diseases
EPA (2004) Environmental protection agency (United States) overview of the ecological risk assessment process in the office of pesticide programs. found at: http://www.epa.gov/espp/consultation/ecorisk-overview.pdf
Ganesan P, Stalin A, Gabriel Paulraj M et al (2018) Biocontrol and non-target effect of fractions and compound isolated from Streptomyces rimosus on the immature stages of filarial vector Culex quinquefasciatus Say (Diptera: Culicidae) and the compound interaction with acetylcholinesterase (AChE1). Ecotoxicol Environ Saf 161:120–128. https://doi.org/10.1016/j.ecoenv.2018.05.061
Habig W, Pabst M, Jakoby W (1974) Glutathione s-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139. https://doi.org/10.2307/j.ctv18b5cjk.40
Hamaidia K, Tine-Djebbar F, Soltani N (2018) Activity of a selective insecticide (methoxyfenozide) against two mosquito species (Culex pipiens and Culiseta longiareolata): toxicological, biometrical and biochemical study. Physiol Entomol 43:315–323. https://doi.org/10.1111/phen.12261
Hegeto LA, Ronqui L, Lapenta AS, Albuquerque FA (2015) Identification and functional characterization of esterases in Euschistus heros (Hemiptera, pentatomidae) and their relationship with thiamethoxam and lambda-cyhalothrin. Genet Mol Res 14:11079–11088. https://doi.org/10.4238/2015.September.22.1
Huang SH, Xian JD, Kong SZ et al (2014) Insecticidal activity of pogostone against Spodoptera litura and Spodoptera exigua (Lepidoptera: Noctuidae). Pest Manag Sci 70:510–516. https://doi.org/10.1002/ps.3635
Kamatchi PAC, Maheswaran R, Ignacimuthu S (2016) Evaluation of larval toxicity of Lantana camara L. and Catharanthus roseus L. against Culex quinquefasciatus Say and Aedes aegypti L. Entomol Ornithol Herpetol 5:1–5
Karthi S, Vasantha-Srinivasan P, Ganesan R et al (2020) Target activity of Isaria tenuipes (Hypocreales: Clavicipitaceae) fungal strains against dengue vector Aedes aegypti (linn.) and its non-target activity against aquatic predators. J Fungi 6:1–14. https://doi.org/10.3390/jof6040196
Kaur M, Chadha P, Kaur S et al (2018) Schizophyllum commune induced genotoxic and cytotoxic effects in Spodoptera litura. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-22919-0
Kaushal M, Kumar A, Kaushal R (2017) Bacillus pumilus strain YSPMK11 as plant growth promoter and bicontrol agent against Sclerotinia sclerotiorum. 3 Biotech. 7:90. https://doi.org/10.1007/s13205-017-0732-7
Kontogiannatos D, Michail X, Kourti A (2011) Molecular characterization of an ecdysteroid inducible carboxylesterase with GQSCG motif in the corn borer, Sesamia nonagrioides. J Insect Physiol 57:1000–1009. https://doi.org/10.1016/j.jinsphys.2011.04.017
Kostyuk VA, Potapovich AI (1989) Superoxide-driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochem Int 19:1117–1124
Kovendan K, Arivoli S, Maheshwaran R et al (2012) Larvicidal efficacy of Sphaeranthus indicus, Cleistanthus collinus and Murraya koenigii leaf extracts against filarial vector, Culex quinquefasciatus say (Diptera: Culicidae). Parasitol Res 111:1025–1035. https://doi.org/10.1007/s00436-012-2927-5
Kumari K, Suresh A, Gallyot EJ et al (2020) Mosquito larvicidal and bactericidal action of crude extract of marine brown alga Turbinaria conoides. Asia-Pacific J Sci Technol 25:1–9
Lateef A, Adelere IA, Gueguim-Kana EB (2015) The biology and potential biotechnological applications of Bacillus safensis. Biologia 70:411–419. https://doi.org/10.1515/biolog-2015-0062
Maehly A, Chance B (1954) The assay of catalse and peroxidases. Methods Biochem Anal 1:358–423
Maheswaran R, Ignacimuthu S (2012) A novel herbal formulation against dengue vector mosquitoes Aedes aegypti and Aedes albopictus. Parasitol Res 110:1801–1813. https://doi.org/10.1007/s00436-011-2702-z
Maheswaran R, Ignacimuthu S (2013) Bioefficacy of essential oil from Polygonum hydropiper L. against mosquitoes, Anopheles stephensi and Culex quinquefasciatus. Ecotoxicol Environ Saf 97:26–31. https://doi.org/10.1016/j.ecoenv.2013.06.028
Maheswaran R, Ignacimuthu S (2014) Effect of Polygonum hydropiper L. against dengue vector mosquito Aedes albopictus L. Parasitol Res 113:3143–3150. https://doi.org/10.1007/s00436-014-4037-z
Maheswaran R, Ignacimuthu S (2015a) A novel biopesticide ponneem to control human vector mosquitoes Anopheles stephensi L. and Culex quinquefasciatus say. Environ Sci Pollut Res 22:13153–13166. https://doi.org/10.1007/s11356-015-4586-4
Maheswaran R, Ignacimuthu S (2015b) Effect of confertifolin from Polygonum hydropiper L. against dengue vector mosquitoes Aedes aegypti L. Environ Sci Pollut Res 22:8280–8287. https://doi.org/10.1007/s11356-014-3936-y
Maheswaran R, Sathish S, Ignacimuthu S (2008) Larvicidal activity of Leucas aspera (willd.) against the larvae of Culex quinquefasciatus say. and Aedes aegypti L. Int J Integr Biol 2:214–217
Maheswaran R, Sukumaran S, Nattudurai G, Ignacimuthu S (2016) Bioefficacy of essential oil from Toddalia asiatica (L.) lam. against dengue vector mosquitoes Aedes aegypti L. and Aedes albopictus Skuse. Indian J Nat Prod Resour 7:245–251
Maheswaran R, Baskar K, Ignacimuthu S, Maria Packiam S, Rajapandiyan K (2019) Bioactivity of Couroupita guianensis Aubl. against filarial and dengue vectors and non-target fish. South Afr J Bot 125:46–53
Manimegalai T, Raguvaran K, Kalpana M, Maheswaran R (2020) Green synthesis of silver nanoparticle using Leonotis nepetifolia and their toxicity against vector mosquitoes of Aedes aegypti and Culex quinquefasciatus and agricultural pests of Spodoptera litura and Helicoverpa armigera. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-10127-1
Manimegalai T, Raguvaran K, Kalpana M, Maheswaran R (2021) Facile Synthesis of Silver Nanoparticles Using Vernonia anthelmintica (L.) Willd. and Their Toxicity Against Spodoptera litura (Fab.), Helicoverpa armigera (Hüb.). Aedes Aegypti Linn and Culex Quinquefasciatus Say J Clust Sci. https://doi.org/10.1007/s10876-021-02151-z
Manimegalai T, Raguvaran K, Kalpana M et al (2022) Bio efficacy of synthesised silver nanoparticles using Dicrocephala integrifolia leaf extract and their insecticidal activity. Mater Lett 314:131860. https://doi.org/10.1016/j.matlet.2022.131860
Matowo J, Kulkarni MA, Mosha FW et al (2010) Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J 9:1–9. https://doi.org/10.1186/1475-2875-9-193
Nataraj J, Manivasagam T, Justin Thenmozhi A, Essa MM (2017) Neuroprotective effect of asiatic acid on rotenone-induced mitochondrial dysfunction and oxidative stress-mediated apoptosis in differentiated SH-SYS5Y cells. Nutr Neurosci 20:351–359. https://doi.org/10.1080/1028415X.2015.1135559
Pizzino G, Irrera N, Cucinotta M et al (2017) Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev. https://doi.org/10.1155/2017/8416763
Pradeepa V, Senthil-Nathan S, Sathish-Narayanan S et al (2016) Potential mode of action of a novel plumbagin as a mosquito repellent against the malarial vector Anopheles stephensi, (Culicidae: Diptera). Pestic Biochem Physiol 134:84–93. https://doi.org/10.1016/j.pestbp.2016.04.001
Raguvaran K, Maheswaran R (2021) Bauhinia variegata L and Croton sparsiflorus L against the human vector mosquitoes. In: Borek S (ed) New Visions in Biological Science. Book Publisher International (a part of SCIENCEDOMAIN International, India, pp 90–94
Raguvaran K, Kalpana M, Manimegalai T, Maheswaran R (2021) Insecticidal, not-target organism activity of synthesized silver nanoparticles using Actinokineospora fastidiosa. Biocatal Agric Biotechnol 38:102197. https://doi.org/10.1016/j.bcab.2021.102197
Raguvaran K, Kalpana M, Manimegalai T, Maheswaran R (2022) Larvicidal, antibacterial, antibiofilm, and anti-quorum sensing activities of silver nanoparticles biosynthesized from Streptomyces sclerotialus culture filtrate. Mater Lett 316:132000. https://doi.org/10.1016/j.matlet.2022.132000
Ramadan R, Abdel-Meguid A, Emara M (2020) Effects of synthesized silver and chitosan nanoparticles using Nerium oleander and Aloe vera on antioxidant enzymes in Musca domestica Catrina. Int J Environ Sci 21:9–14. https://doi.org/10.21608/cat.2020.20921.1036
Sayono S, Anwar R, Sumanto D (2020) Evaluation of toxicity in four extract types of tuba root against dengue vector, Aedes aegypti (Diptera: Culicidae) larvae. Pak J Biol Sci 23(12):1530–1538
Senthil-Nathan S (2020) A review of resistance mechanisms of synthetic insecticides and botanicals, phytochemicals, and essential oils as alternative larvicidal agents against mosquitoes. Front Physiol 10:1–21. https://doi.org/10.3389/fphys.2019.01591
Sharma P, Kalita MC, Thakur D (2016) Broad spectrum antimicrobial activity of forest-derived soil actinomycete, Nocardia sp. PB-52. Front Microbiol 7:1–17. https://doi.org/10.3389/fmicb.2016.00347
Sukumaran S, Maheswaran R (2020a) Effect of gut microbes from Eyprepocnemis alacris alacris (serv. 1838) against Culex quinquefasciatus say-an ecofriendly approach. Adv Zool Bot 8:199–208
Sukumaran S, Maheswaran R (2020b) Larvicidal activity of Elytraria acaulis against Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). J Arthropod Borne Dis 14:293–301
Tasneem S, Yasmeen R (2018) Evaluation of genotoxicity by comet assay (single-cell gel electrophoresis) in tissues of the fish Cyprinus carpio during sub-lethal exposure to Karanjin. J Basic Appl Zool 79:19. https://doi.org/10.1186/s41936-018-0033-7
Thenmozhi M, Jannu Vinay Gopal JV, Kannabiran K, Rajakumar G, Velayutham K, Rahuman AA (2013) Eco-friendly approach using marine actinobacteria and its compounds to control ticks and mosquitoes. Parasitol Res 112(2):719–729. https://doi.org/10.1007/s00436-012-3192-3
WHO (2005) Guidelines for laboratory and field testing of mosquito larvicides. World Heal Organ 1–41. WHO/CDS/WHOPES/GCDPP/2005.11
WHO (2021) Fact sheet about malaria. https://www.who.int/news-room/fact-sheets/detail/malaria.
Acknowledgements
The author (Dr. Rajan Maheswaran/Principal Investigator/DST-SERB Project, File No. EEQ/2018/000557) is thankful to the Department of Science and Technology, New Delhi, India for providing financial support and Periyar University, Salem, Tamil Nadu for providing laboratory facilities.
Funding
This work was funded by the Science and Engineering Board, Department of Science and Technology, New Delhi, India (File No. EEQ/2018/000557). Rajan Maheswaran declared that the funds were supported by the Science and Engineering Board, Department of Science and Technology, New Delhi, India (File No. EEQ/2018/000557); Krishnan Raguvaran, Manickam Kalpana, Thulasiraman Manimegalai, Suresh Kalaivani, Palanisamy Devapriya, Nagarajan Siddharthan, Rengasamy Balakrishnan, Tamil Selvan Silambarasan declared that there was no fund support in the research process. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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KR: investigation, writing—original draft, MK, TM, NS, RB, TSS, investigation, SK, PD: writing—review and editing, RM: conceptualization, supervision.
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Raguvaran, K., Kalpana, M., Manimegalai, T. et al. Larvicidal, antioxidant and biotoxicity assessment of (2-(((2-ethyl-2 methylhexyl)oxy)carbonyl)benzoic acid isolated from Bacillus pumilus against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. Arch Microbiol 204, 650 (2022). https://doi.org/10.1007/s00203-022-03264-3
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DOI: https://doi.org/10.1007/s00203-022-03264-3