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Inhibiting Stenotrophomonas maltophilia, a Pathogenic Bacterium Responsible for Kernel Rot Disease in Pili nut (Canarium ovatum Engl.) with Ionic Liquid-loaded Nanoemulsions

Roberth San Abando Solita, Felmer Sesaldo Latayada, Julius Anthony Magadan Leones, Elizabeth Pio Parac, Arnold Cafe Alguno, Rey Yonson Capangpangan

Abstract


Pili nut production in the Philippines has grown steadily, but it faces significant challenges from pests and diseases, notably kernel rot. Yield losses due to this pathogen are still not measured, but the damage could extend from the purple immature to the dried postharvest nuts. Therefore, there is a pressing need for safe, effective, and environmentally friendly control measures. This study reports on the successful formulation of various Ionic Liquid-loaded Eucalyptus Essential Oil Nanoemulsions (IL-EEONE) for potential applications against Stenotrophomonas maltophilia, a pathogenic bacterium responsible for kernel rot disease in Pili nut (Canarium ovatum). Combining eucalyptus essential oil (EO) and Tween 80 in an oil-in-water (O/W) system, followed by stirring and sonication, and the subsequent loading of 1-Butyl-3-methylimidazolium hydrogen sulfate ([Bmim][HSO4]), an ionic liquid, at varying ratios (1:1, 2:1, and 3:1), yielding the formation of IL-EEONE. The nanoemulsion droplets exhibited a size range of 9.4–12.26 nm, highlighting their nanoscale dimensions. The IL-loaded nanoemulsions formulated at varying ratios typically displayed nearly monodisperse characteristics, except for the higher concentration 1:1 ratio of IL:EEONE formulation, as indicated by their Polydispersity Index (PDI) values. Fourier Transform Infrared (FT-IR) analysis further confirmed the successful formulation of the different IL-EEONE nanoemulsion compositions. Significantly, these nanoemulsions demonstrated excellent inhibitory properties against S. maltophilia, as indicated by Zone of Inhibition (ZOI) ranging from 11.3 ± 0.58 mm to 32.7 ± 0.58 mm. The antibacterial activity varied from partially active to very active across different formulations, with the 1:1 IL-EEONE ratio formulation standing out as exceptionally effective. This study shows the potential of IL-loaded nanoemulsions, IL-EEONE, as a potential agent for mitigating S. maltophilia causing the kernel rot disease, offering innovative avenues for addressing bacterial infection in agricultural settings.


Keywords



[1] C. G. Millena and R. S. Sagum, “Philippine Pili (Canarium ovatum, Engl.) varieties as source of essential minerals and trace elements in human nutrition,” Journal of Food Composition and Analysis, vol. 69, pp. 53–61, Feb. 2018, doi: 10.1016/j.jfca.2018.02.008.

 

[2] C. G. Millena, N. I. P. Cañaveral, L. B. Colanza, T. A. G. Señora, J. M. V. Tarog, S. M. Enovejas, K. M. A. Renovalles, and S. S. Ruivivar, “Effects of pre-processing methods of Pili Nuts (Canarium ovatum Engl.) on its nutritional and mineral bioavailability,” Philippine Journal of Science, vol. 152, no. 6B, pp. 2343–2357, Dec. 2023.

 

[3] D. O. Esiegbuya, J. I. Osagie, F. I. Okungbowa, and E. O. Ekhorutomwen, “Fungi associated with the postharvest fungal deterioration of Shea Nuts and Kernels,” International Journal of Agriculture and Forestry, vol. 4, no. 05, pp. 373–379, 2014, doi: 10.5923/j.ijaf.20140405.05.

 

[4] J. S. Brooke, “Stenotrophomonas maltophilia: An emerging global opportunistic pathogen,” Clinical Microbiology Reviews, vol. 25, no. 1, pp. 2–41, 2012, doi: 10.1128/CMR.00019-11.

 

[5] J. Murugaiyan, P. A. Kumar, G. S. Rao, K. Iskandar, S. Hawser, J. P. Hays, Y. Mohsen, S. Adukkadukkam, W. A. Awuah, R. A. M. Jose, N. Sylvia, E. P. Nansubuga, B. Tilocca, P. Roncada, N. Roson-Calero, J. Moreno-Morales, R. Amin, B. K. Kumar, A. Kumar, A. R. Toufik, T. N. Zaw, O. O. Akinwotu, M. P. Satyaseela, and M. B. van Dongen, “Progress in alternative strategies to combat antimicrobial resistance: Focus on antibiotics,” Antibiotics, vol. 11, no. 2, p. 200, Feb. 2022, doi: 10.3390/antibiotics11020200.

 

[6] F. J. Álvarez-Martínez, E. Barrajón-Catalán, M. Herranz-López, and V. Micol, “Antibacterial plant compounds, extracts and essential oils: An updated review on their effects and putative mechanisms of action,” Phytomedicine, vol. 90, Jul. 2021, Art. no. 153626, doi: 10.1016/j.phymed. 2021.153626.

 

[7] E. M. Abdallah, B. Y. Alhatlani, R. D. P. Menezes, and C. H. G. Martins “Back to nature: Medicinal plants as promising sources for antibacterial drugs in the post-antibiotic era,” Plants, vol. 12, no. 17, p. 3077, Aug. 2023, doi: 10.3390/ plants12173077.

 

[8] N. Vaou, E. Stavropoulou, C. Voidarou, C. Tsigalou, and E. Bezirtzoglou, “Towards advances in medicinal plant antimicrobial activity: A review study on challenges and future perspectives,” Microorganisms, vol. 9, no. 10, p. 2041, Sep. 2021, doi: 10.3390/microorganisms9102041.

 

[9] A. Brandelli, A. C. Ritter, and F. F. Veras, “Antimicrobial activities of metal nanoparticles,” in Metal Nanoparticles in Pharma, M. Rai, R. Shegokar, Eds. Cham: Springer, pp. 337–363, 2017.

 

[10] O. Maťátková, J. Michailidu, A. Miškovská, I. Kolouchová, J. Masák, and A. Čejková, “Antimicrobial properties and applications of metal nanoparticles biosynthesized by green methods,” Biotechnology Advances, vol. 58, Jan. 2022, Art. no. 107905, doi: 10.1016/j.biotechadv. 2022.107905.

 

[11] D. Franco, G. Calabrese, S. P. P. Guglielmino, and S. Conoci, “Metal-based nanoparticles: Antibacterial mechanisms and biomedical application,” Microorganisms, vol. 10, no. 9, p. 1778, Sep. 2022, doi: 10.3390/microorganisms 10091778.

 

[12] S. Zhang, L. Lin, X. Huang, Y. G. Lu, D. L. Zheng, and Y. Feng, “Antimicrobial properties of metal nanoparticles and their oxide materials and their applications in oral biology,” Journal of Nanomaterials, vol. 2022, Jun. 2022, Art. no. 2063265, doi: 10.1155/2022/2063265.

 

[13] N. Dhull, V. Gupta, and M. Tomar, “Antimicrobial properties of metallic nanoparticles: A qualitative analysis,” Materials Today: Proceedings, vol. 17, no. 1, pp. 155–160, Aug. 2019, doi: 10.1016/j.matpr.2019.06.413.

 

[14] C. Bankier, R. K. Matharu, Y. K. Cheong, G. G. Ren, E. Cloutman-Green, and L. Ciric, “Synergistic antibacterial effects of metallic nanoparticle combinations,” Scientific Reports, vol. 9, Nov. 2019, Art. no. 16074, doi: 10.1038/s41598-019- 52473-2.

 

[15] M. N. Nadagouda, P. Vijayasarathy, A. Sin, H. Nam, S. Khan, J. B. Parambath, A. A. Mohamed, and C. Han, “Antimicrobial activity of quaternary ammonium salts: Structure-activity relationship,” Medicinal Chemistry Research, vol. 31, pp. 1663– 1678, Jul. 2022, doi: 10.1007/s00044-022- 02924-9.

 

[16] W. Dan, J. Gao, X. Qi, J. Wang, J. Dai, “Antibacterial quaternary ammonium agents: Chemical diversity and biological mechanism,” European Journal of Medicinal Chemistry, vol. 243, Dec. 2022, Art. no. 114765, doi: 10.1016/j.ejmech.2022.114765.

 

[17] S. Chouhan, K. Sharma, and S. Guleria, “Antimicrobial activity of some essential oils – Present status and future perspectives,” Medicines, vol. 4, no. 3, p. 58, Aug. 2017, doi: 10.3390/medicines4030058.

 

[18] M. Canto-Tejero, M. J. Pascual-Villalobos, and P. Guirao, “Aniseed essential oil botanical insecticides for the management of the currant-lettuce aphid,” Industrial Crops and Products, vol. 181, Jul. 2022, Art. no. 114804, doi: 10.1016/j.indcrop.2022.114804.

 

[19] S. Fijan, “Probiotics and their antimicrobial effect,” Microorganisms, vol. 11, no. 2, p. 528, Feb. 2023, doi: 10.3390/microrganisms11020528.

 

[20] B. Haghshenas, A. Kiani, S. Mansoori, E. Mohammadi-noori, and Y. Nami, “Probiotic properties and antimicrobial evaluation of silymarin-enriched Lactobacillus bacteria isolated from traditional curd,” Scientific Reports, vol. 13, no. 1, Jul. 2023, Art. no. 10916, doi: 10.1038/ s41598-023-37350-3.

 

[21] D. J. McClements, “Nanotechnology approaches for improving the healthiness and sustainability of the modern food supply,” ACS Omega, vol. 5, no. 46, pp. 29623–29630, Nov. 2020, doi: 10.1021/acsomega.0c04050.

 

[22] M. Heydari, A. Amirjani, M. Bagheri, I. Sharifian, and Q. Sabahi, “Eco-friendly pesticide based on peppermint oil nanoemulsion: Preparation, physicochemical properties, and its aphicidal activity against cotton aphid,” Environmental Science and Pollution Research, vol. 27, no. 6, pp. 6667–6679, Feb. 2020, doi: 10.1007/s11356- 019-07332-y.

 

[23] S. Kotta, A. W. Khan, S. H. Ansari, R. K. Sharma, and J. Ali, “Formulation of nanoemulsion: A comparison between phase inversion composition method and high-pressure homogenization method,” Drug Delivery, vol. 22, no. 4, pp. 455–466, Dec. 2013, doi: 10.3109/10717544.2013.866992.

 

[24] O. Alliod, J. P. Valour, S. Urbaniak, H. Fessi, D. Dupin, and C. Charcosset, “Preparation of oil-in-water nanoemulsions at large-scale using premix membrane emulsification and Shirasu Porous Glass (SPG) membranes,” Colloids and Surfaces A: Physicochemical and Engineering Aspects, vol. 557, pp. 76–84, Nov. 2018, doi: 10.1016/j.colsurfa.2018.04.045.

 

[25] E. O. M. Ali, N. A. Shakil, V. S. Rana, D. J. Sarkar, S. Majumder, P. Kaushik, B. B. Singh, and J. Kumar, “Antifungal activity of nano emulsions of neem and citronella oils against phytopathogenic fungi, Rhizoctonia solani and Sclerotium rolfsii,” Industrial Crops and Products, vol. 108, pp. 379–387, Dec. 2017, doi : 10.1016/j.indcrop.2017.06.061.

 

[26] X. Zhao, H. Cui, Y. Wang, C. Sun, N. Cui, and Z. Zeng, “Development strategies and prospects of nano-based smart pesticide formulation,” Journal of Agricultural and Food Chemistry, vol. 66, no. 26, pp. 6504–6512, Jun. 2017, doi : 10.1021/ acs.jafc.7b02004.

 

[27] J. Hudzicki, “Kirby-Bauer disk diffusion susceptibility test protocol,” American Society for Microbiology, vol. 15, pp. 55–63, Dec. 2009.

 

[28] A. W. Bauer, W. M. Kirby, J. C. Sherris, and M. Turck, “Antibiotic susceptibility testing by a standardized single disk method,” American Journal of Clinical Pathology, vol. 45, no. 4, pp. 493–496, Apr. 1966.

 

[29] N. Khalid, I. Kobayashi, M.A. Neves, K. Uemura, and M. Nakajima, “Preparation and characterization of water-in-oil emulsions loaded with high concentration of l-ascorbic acid,” LWT-Food Science and Technology, vol. 51, no. 2, pp. 448– 454, May 2013, doi: 10.1016/j.lwt.2012.11.020.

 

[30] M. Sandhya, D. Ramasamy, K. Sudhakar, K. Kadirgama, and W. S. W. Harun, “Ultrasonication an intensifying tool for preparation of stable nanofluids and study the time influence on distinct properties of graphene nanofluids – A systematic overview,” Ultrasonics Sonochemistry, vol. 73, May 2021, Art. no. 105479, doi: 10.1016/j.ultsonch.2021.105479.

 

[31] N. Riquelme, R. N. Zúñiga, and C. Arancibia, “Physical stability of nanoemulsions with emulsifier mixtures: Replacement of tween 80 with quillaja saponin,” LWT, vol. 111, pp. 760– 766, Aug. 2019, doi: 10.1016/j.lwt.2019.05.067.

 

[32] X. Kang, X. Sun, and B. Han, “Synthesis of functional nanomaterials in ionic liquids,” Advanced Materials, vol. 28, no. 6, pp. 1011– 1030, Nov. 2015, doi: 10.1002/adma.201502924.

 

[33] I. J. Dinshaw, N. Ahmad, N. Salim, and B. F. Leo, “Nanoemulsions: A review on the conceptualization of treatment for psoriasis using a ‘green’surfactant with low-energy emulsification method” Pharmaceutics, vol. 13, no. 7, p. 1024, Jul. 2021, doi: 10.3390/pharmaceutics13071024.

 

[34] A. M. Curreri, S. Mitragotri, and E. E. Tanner, “Recent advances in ionic liquids in biomedicine,” Advanced Science, vol. 8, no. 17, Jul. 2021, Art. no. 2004819, doi: 10.1002/advs.202004819.

 

[35] Q. Liu, H. Huang, H. Chen, J. Lin, and Q. Wang, “Food-grade nanoemulsions: Preparation, stability and application in encapsulation of bioactive compounds,” Molecules, vol. 24, no. 23, p. 4242, Dec. 2019, doi: 10.3390/molecules24234242.

 

[36] K. Bhattacharjee, “Importance of surface energy in nanoemulsion,” in Nanoemulsions-Properties, Fabrications and Applications, K. S. Koh, V. L. Wong, Eds. London, UK: IntechOpen, 2019, doi: 10.5772/intechopen.84201.

 

[37] K. S. Koh and V. L. Wong, Nanoemulsions: Properties, Fabrications and Applications. London, UK: InTechOpen, 2019, doi: 10.5772/ intechopen.78812.

 

[38] J. Jin, C. H. Ooi, D. V. Dao, and N. T. Nguyen, “Coalescence processes of droplets and liquid marbles,” Micromachines, vol. 8, no. 11, p. 336, Nov. 2017, doi: 10.3390/mi8110336.

 

[39] I. M. Mahbubul, “Stability and dispersion characterization of nanofluid,” in Preparation, Characterization, Properties and Application of Nanofluid: A Volume in Micro and Nano Technologies. Amsterdam, Natherlands: Elsevier, pp. 47–112, 2019.

 

[40] K. Ziani, Y. Fang, and D. J. McClements, “Fabrication and stability of colloidal delivery systems for flavor oils: Effect of composition and storage conditions,” Food Research International, vol. 46, no. 1, pp. 209–216, Jan. 2012, doi : 10.1016/j.foodres.2011.12.017.

 

[41] P. Witayaudom and U. Klinkesorn, “Effect of surfactant concentration and solidification temperature on the characteristics and stability of nanostructured lipid carrier (NLC) prepared from rambutan (Nephelium lappaceum L.) kernel fat,” Journal of Colloid and Interface Science, vol. 505, pp. 1082–1092, Nov. 2017, doi: 10.1016/j.jcis. 2017.07.008.

 

[42] Z. Khoshraftar, A. A. Safekordi, A. Shamel, and M. Zaefizadeh, “Synthesis of natural nanopesticides with the origin of Eucalyptus globulus extract for pest control,” Green Chemistry Letters and Reviews, vol. 12, no. 3, pp. 286–298, Jul. 2019, doi: 10.1080/17518253.2019.1643930.

 

[43] H. Alipanah, A. Abdollahi, S. Firooziyan, E. Zarenezhad, M. Jafari, and M. Osanloo, “Nanoemulsion and nanogel containing Eucalyptus globulus essential oil;  Larvicidal activity and antibacterial properties,” Interdisciplinary Perspectives on Infectious Diseases, vol. 2022, Aug. 2022, Art. no. 1616149, doi: 10.1155/2022/1616149.

 

[44] B. A. Khan, A. Khan, M. K. Khan, and V. A. Braga, “Preparation and properties of High sheared Poly (Vinyl Alcohol)/Chitosan blended Hydrogels films with Lawsonia inermis extract as wound dressing,” Journal of Drug Delivery Science and Technology, vol. 61, Nov. 2020, Art. no. 102227, doi: 10.1016/j.jddst.2020.102227.

 

[45] B. Q. Guevara, A guidebook to plant screening: Phytochemical and Biological. Manila, Philippines: University of Santo Tomas Publishing House, 2005.

 

[46] S. Rout, S. Tambe, R. K. Deshmukh, S. Mali, J. Cruz, P. P. Srivastav, P. D. Amin, K. K. Gaikwad, E. H. de Aguiar Andrade, and M. S. de Oliveira, “Recent trends in the application of essential oils: The next generation of food preservation and food packaging,” Trends Food Science & Technology, vol. 129, pp. 421–439, Nov. 2022, doi: 10.1016/j.tifs.2022.10.012.

 

[47] J. N. P. Carneiro, R. P. da Cruz, F. F. Campina, M. D. S. Costa, A. T. L. dos Santos, D. L. Sales, C. F. Bezerra, L. E. da Silva, J. P. de Araujo, W. do Amaral, R. A. Rebelo, I. M. Begnini, L. F. de Lima, H. D. M. Coutinho, and M. F. B. Morais- Braga, “GC/MS analysis and antimicrobial activity of the Piper mikanianum (Kunth) Steud. essential oil,” Food and Chemical Toxicology, vol. 135, Jan. 2020, Art. no. 110987, doi: 10.1016/j.fct.2019.110987.

 

[48] J. N. Cruz, S. G. Silva, D. S. Pereira, A. P. D. S. S. Filho, M. S. de Oliveira, R. R. Lima, and E. H. D. A. Andrade, “In Silico evaluation of the antimicrobial activity of thymol-major compounds in the essential oil of Lippia thymoides Mart. & Schauer (Verbenaceae),” Molecules, vol. 27, no. 15, p. 4768, Jul. 2022, doi: 10.3390/molecules27154768.

 

[49] M. Ben Jemaa, H. Falleh, and R. Ksouri, “Encapsulation of natural bioactive compounds: nanoemulsion formulation to enhance essential oils activities,” in Microencapsulation - Processes, Technologies and Industrial Applications, F. Salaün Ed. London, UK: InTechOpen, 2019, doi : 10.5772/intechopen.84183.

 

[50] N. Nikfarjam, M. Ghomi, T. Agarwal, M. Hassanpour, E. Sharifi, D. Khorsandi, M. A. Khan, F. Rossi, A. Rossetti, E. N. Zare, N. Rabiee, D. Afshar, M. Vosough, T. K. Maiti, V. Mattoli, E. Lichtfouse, F. R. Tay, and P. Makvandi, “Antimicrobial ionic liquid‐based materials for biomedical applications,” Advanced Functional Materials, vol. 31, no. 42, Jul. 2021, Art. no. 2104148, doi: 10.1002/adfm.202104148.

 

[51] M. M. Fernandes, E. O. Carvalho, D. M. Correia, J. M. Esperança, J. Padrão, K. Ivanova, J. Hoyo, T. Tzanov, and S. Lanceros-Mendez, “Ionic liquids as biocompatible antibacterial agents: A case study on structure-related bioactivity on Escherichia coli,” ACS Applied Bio Materials, vol. 5, no. 11, pp. 5181–5189, Oct. 2022, doi: 10.1021/acsabm.2c00615.

 

[52] M. Zunita and B. Batara, “Antibacterial-based ionic liquids for environmental wastewater treatment,” Case Studies in Chemical and Environmental Engineering, vol. 7, Jun. 2023, Art. no. 100341, doi: 10.1016/j.cscee.2023.100341.

 

[53] Y. Hu, Y. Xing, P. Ye, H. Yu, X. Meng, Y. Song, G. Wang, and Y. Diao, “The antibacterial activity and mechanism of imidazole chloride ionic liquids on Staphylococcus aureus,” Frontiers in Microbiology, vol. 14, Feb. 2023, Art. no. 1109972, doi : 10.3389/fmicb.2023.1109972.

 

[54] C. F. Carson, K. A. Hammer, and T. V. Riley, “Melaleuca alternifolia (Tea Tree) oil: A review of antimicrobial and other medicinal properties,” Clinical Microbiology Reviews, vol. 19, no. 1, pp. 50–62, Jan. 2006, doi: 10.1128/CMR.19.1.50- 62.2006.

 

[55] H. Cui, X. Zhang, H. Zhou, C. Zhao, and L. Lin, “Antimicrobial activity and mechanisms of salvia sclarea essential oil,” Botanical Studies, vol. 56, p. 16, Dec. 2015, doi: 10.1186/s40529-015- 0096-4.

 

[56] F. Nazzaro, F. Fratianni, L. De Martino, R. Cop­pola, and V. D. Feo, “Effect of essential oils on pathogenic bacteria,” Pharmaceuticals, vol. 6, no. 12, pp. 1451–1474, Dec. 2013, doi: 10.3390/ ph6121451.

 

[57] S. Elangovan and P. Mudgil, “Antibacterial properties of Eucalyptus globulus essential oil against MRSA: A systematic review,” Antibiotics, vol. 12, no. 3, p. 474, Mar. 2023, doi: 10.3390/antibiotics12030474.

 

[58] J. M. V. Makabenta, A. Nabawy, A. N. Chattopadhyay, J. Park, C. H. Li, R. Goswami, D. C. Luther, R. Huang, M. A. Hassan, and V. M. Rotello, “Antimicrobial-loaded biodegradable nanoemulsions for efficient clearance of intracellular pathogens in bacterial peritonitis,” Biomaterials, vol. 302, Nov. 2023, Art. no. 122344, doi: 10.1016/j.biomaterials.2023.122344.

 

[59] B. D. da Silva, D. K. A. do Rosário, L. T. Neto, C. A. Lelis, and C. A. Conte-Junior, “Antioxidant, antibacterial and antibiofilm activity of nanoemulsion-based natural compound delivery systems compared with non-nanoemulsified versions,” Foods, vol. 12, no. 9, p. 1901, May 2023, doi: 10.3390/foods12091901.

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DOI: 10.14416/j.asep.2024.07.004

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