The Impact of D-limonene on Cell Membrane Barrier of Pichia kluyveri Y-11519 from Sichuan Pickles

Main Article Content

Chaoyi Zeng
Atittaya Tandhanskul
Samatcha Krungkaew
Tanawan Likhanapaiboon
Witthawat Kasayapanan
Watanya Chaisayan
Patchanee Yasurin
Jie Tang
Theerawut Phusantisampan
Atthasit Tawai

Abstract

Sichuan pickles (SCP) are a traditional method of preserving vegetables in China. Through the spontaneous fermentation of microorganisms in brine water, it forms a unique flavor to meet with food industry’s requirements. However, the microorganisms in salt water determine the quality of SCP, and the film-forming phenomenon is considered to be the key to the spoilage of SCP, which seriously restricts the industrial development of SCP. We have noticed that in folk, lemon peel is often added to pickles to prevent the appearance of the film. Currently, the extract D-limonene from orange or lemon peel is recognized as a Generally Recognized as Safe (GRAS) food additive and exhibits broad-spectrum antimicrobial properties. However, there have been no reports on the effects of D-limonene on Pichia kluyveri (P. kluyveri), the microorganism responsible for the "film-forming" phenomenon in SCP. In this study, D-limonene was used to treat P. kluyveri Y-11519, a membranous microorganism of SCP, and the cell morphology, surface charge, membrane potential, and intracellular macromolecule leakage before and after treatment were observed. The results showed that the minimum inhibitory concentration of D-limonene against P. kluyveri Y-11519 was 20 μL/mL, and the minimum fungicidal concentration was 40 μL/mL. After treatment with this concentration of D-limonene, the growth of P. kluyveri Y-11519 cells was delayed, cells exhibited deformation and shrinkage, cell membrane integrity was compromised, permeability increased, intracellular substances leaked, ultimately leading to cell death.

Article Details

How to Cite
Zeng, C., Tandhanskul, A., Krungkaew, S., Likhanapaiboon, T., Kasayapanan, W., Chaisayan, W., Yasurin, P., Tang, J., Phusantisampan, T., & Tawai, A. (2024). The Impact of D-limonene on Cell Membrane Barrier of Pichia kluyveri Y-11519 from Sichuan Pickles. Applied Science and Engineering Progress, 17(3), 7407. https://doi.org/10.14416/j.asep.2024.06.014
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Research Articles

References

F. Zhang, Y. Ren, K. Yao, Q. He, Y. Wan, and Y. Chi, “Microbial composition of spoiled industrial-scale Sichuan paocai and characteristics of the microorganisms responsible for paocai spoilage,” International Journal of Food Microbiology, vol. 275, pp. 32–38, 2018.

Y. Rao, Y. Tao, X. Chen, X. She, Y. Qian, Y. Li, Y. Du, W. Xiang, H. Li, and L. Liu, “The characteristics and correlation of the microbial communities and flavors in traditionally pickled radishes,” LWT, vol .118, 2020, Art. no. 108804.

W. L. Xiang, N. D. Zhang, Y. Lu, Q. H. Zhao, Q. Xu, Y. Rao, L. Liu, and Q. Zhang, “Effect of Weissella cibaria co-inoculation on the quality of Sichuan Pickle fermented by Lactobacillus plantarum,” LWT, vol. 121, 2020, Art. no. 108975.

J. Y. Kim, J. Kim, I. T. Cha, M. Y. Jung, H. S. Song, Y. B. Kim, C. Lee, S. Y. Kang, J. W. Bae, Y. E. Choi, and T. W. Kim, “Community structures and genomic features of undesirable white colony-forming yeasts on fermented vegetables,” Journal of Microbiology, vol. 57, pp. 30–37, 2019.

T. Cai, P. Shi, S. Zhang, W. Xiang, J. Liu, Z. Lin, and J. Tang, “Inhibition of perilla frutescens essential oil on pellicle formation of candida tropicalis and pichia kluyveri and its effect on volatile compounds in sichuan pickles,” Foods, vol. 12, no. 8, p. 1593, 2023.

C. Ravichandran, P. C. Badgujar, P. Gundev, and A. Upadhyay, “Review of toxicological assessment of d-limonene, a food and cosmetics additive,” Food and Chemical Toxicology, vol. 120, pp. 668–680, 2018.

N. Chaichana, “Nutrition composition and analysis of medicinal herbal potential of horsfieldia glabra Warb. seeds,” Applied Science and Engineering Progress, vol. 9, no. 1, pp. 61– 69, 2016, doi: 10.14416/j.ijast.2015.12.001.

J. F. Sun, L. I. Min, G. U. Liang, M. L. Wang, and M. H. Yang, “Recent progress on anti-Candida natural products,” Chinese Journal of Natural Medicines, vol. 19, no. 8, pp. 561–579, 2021.

J. Vicente, F. Calderón, A. Santos, D. Marquina, and S. Benito, “High potential of Pichia kluyveri and other Pichia species in wine technology,” International Journal of Molecular Sciences, vol. 22, no. 3, p. 1196, 2021.

S. Akhavan-Mahdavi, R. Sadeghi, A. F. Esfanjani, S. Hedayati, R. Shaddel, C. Dima, N. Malekjani, S. Boostani, and S. M. Jafari, “Nanodelivery systems for d-limonene; techniques and applications,” Food Chemistry, vol. 384, 2022, Art. no. 132479.

G. Bulkan, S. Sitaresmi, G. T. Yudhanti, R. Millati, R. Wikandari, and M. J. Taherzadeh, “Enhancing or inhibitory effect of fruit or vegetable bioactive compound on Aspergillus niger and A. oryzae,” Journal of Fungi, vol. 8, no. 1, p. 12, 2021.

A. Masood, N. Ahmed, M. F. M. Razip Wee, A. Patra, E. Mahmoudi, and K. S. Siow, “Atmospheric pressure plasma polymerisation of D-limonene and its antimicrobial activity,” Polymers, vol. 15, no. 2, p. 307, 2023.

C. Salinas, G. Florentín, F. Rodríguez, N. Alvarenga, and R. Guillén, “Terpenes combinations inhibit biofilm formation in staphyloccocus aureus by interfering with initial adhesion,” Microorganisms, vol. 10, no. 8, p. 1527, 2022.

N. Tomaś, K. Myszka, L. Wolko, K. Nuc, A. Szwengiel, A. Grygier, and M. Majcher, “Effect of black pepper essential oil on quorum sensing and efflux pump systems in the fish-borne spoiler Pseudomonas psychrophila KM02 identified by RNA-seq, RT-qPCR and molecular docking analyses,” Food Control, vol. 130, 2021, Art. no. 108284.

A. L. Umagiliyage, N. Becerra-Mora, P. Kohli, D. J. Fisher, and R. Choudhary, “Antimicrobial efficacy of liposomes containing D-limonene and its effect on the storage life of blueberries,” Postharvest Biology and Technology, vol. 128, pp. 130–137, 2017.

H. Yu, Z. X. Lin, W. L. Xiang, M. Huang, J. Tang, Y. Lu, Q. H. Zhao, Q. Zhang, Y. Rao, and L. Liu, “Antifungal activity and mechanism of D-limonene against foodborne opportunistic pathogen Candida tropicalis,” LWT, vol. 159, 2022, Art. no. 113144.

W. K. Costa, A. M. de Oliveira, I. B. da S. Santos, V. B. G. Silva, E. K. C. da Silva, J. V. de O. Alves, A. P. S. A. da Silva, V. L. de M. Lima, M. T. dos S. Correia, and M. V. da Silva, “Antibacterial mechanism of Eugenia stipitata McVaugh essential oil and synergistic effect against Staphylococcus aureus,” South African Journal of Botany, vol. 147, pp. 724–730, 2022.

P. Yasurin, S. Asavasanti, N. Lawthienchai, T. Tongprasan, and C. Tangduangdee, “Effect of extraction methods on antibacterial activity and chemical composition of chinese chives (Allium tuberosum Rottl. ex Spreng) extract”, Applied Science and Engineering Progress, vol. 10, no. 2, pp. 97–106, 2017, doi: 10.14416/ j.ijast.2017.05.001.

F. Alderees, R. Mereddy,S. Were, M. E. Netzel, and Y. Sultanbawa, “Anti-yeast synergistic effects and mode of action of Australian native plant essential oils,” Applied Sciences, vol. 11, no. 22, 2021, Art. no. 10670.

F. Z. K. Labbani, B. Turchetti, L. Bennamoun, S. Dakhmouche, R. Roberti, L. Corazzi, Z. Meraihi, and P. Buzzini, “A novel killer protein from Pichia kluyveri isolated from an Algerian soil: Purification and characterization of its in vitro activity against food and beverage spoilage yeasts,” Antonie van Leeuwenhoek, vol. 107, pp. 961–970, 2015.

S. Thananimit, P. Sorsiw, W. Wanna, and S. Phongpaichit, “Antifungal activity of silver nanoparticles with the potential to control fungal contamination in the male inflorescences of palmyra palm,” Applied Science and Engineering Progress, vol. 15, no. 4, p. 4532, 2022, doi: 10.14416/j.asep.2021.07.007.

Y. X. Wu, Y. D. Zhang, N. Li, D. D. Wu, Q. M. Li, Y. Z. Chen, G. C. Zhang, and J. Yang, “Inhibitory effect and mechanism of action of juniper essential oil on gray mold in cherry tomatoes,” Frontiers in Microbiology, vol. 13, 2022, Art. no. 1000526.

Z. Yang, Q. He, B. B. Ismail, Y. Hu, and M. Guo, “Ultrasonication induced nano-emulsification of thyme essential oil: Optimization and antibacte¬rial mechanism against Escherichia coli,” Food Control, vol. 9 133, 2022, Art. no. 108609.

H. S. Alvarez-Manzo, Y. Zhang, W. Shi, and Y. Zhang, “Evaluation of disulfiram drug combinations and identification of other more effective combinations against stationary phase Borrelia burgdorferi,” Antibiotics, vol. 9, no. 9, p. 542, 2022.

Y. Cai, G. Zou, M. Xi, Y. Hou, H. Shen, J. Ao, M. Li, J. Wang, and A. Luo, “Juglone inhibits Listeria monocytogenes ATCC 19115 by targeting cell membrane and protein,” Foods, vol. 11, no. 17, p. 2558, 2022.

F. A. Tapouk, R. Nabizadeh, N. Mirzaei, and M. A. V. Hasanloei, “Comparative efficacy of hospital disinfectants against nosocomial infection pathogens,” Antimicrob Resist Infect Control, vol. 9, no. 115, 2020, doi: 10.1186/ s13756-020-00781-y.

G. Rajivgandhi, A. Stalin, C. C. Kanisha, G. Ramachandran, N. Manoharan, N. S. Alharbi, S. Kadaikunnan, J. M. Khaled, K. F. Alanzi, and W. J. Li, “Physiochemical characterization and anti-carbapenemase activity of chitosan nanoparticles loaded Aegle marmelos essential oil against K. pneumoniae through DNA fragmentation assay,” Surfaces and Interfaces, vol. 23, 2021, Art. no.100932.

T. L. Wu, B. Q. Zhang, X. F. Luo, A. P. Li, S. Y. Zhang, J. X. An, Z. J. Zhang, and Y. Q. Liu, “Antifungal efficacy of sixty essential oils and mechanism of oregano essential oil against Rhizoctonia solani,” Industrial Crops and Products, vol. 191, 2023, Art. no.115975.

G. M. Bruinsma, M. Rustema-Abbing, H. C. van der Mei, C. Lakkis, and H. J. Busscher, “Resistance to a polyquaternium-1 lens care solution and isoelectric points of Pseudomonas aeruginosa strains,” Journal of Antimicrobial Chemotherapy, vol. 57, no. 4, pp. 764–766, 2006.

R. L. Soon, R. L. Nation, S. Cockram, J. H. Moffatt, M. Harper, B. Adler, J. D. Boyce, I. Larson, and J. Li, “Different surface charge of colistin-susceptible and-resistant Acinetobacter baumannii cells measured with zeta potential as a function of growth phase and colistin treatment,” Journal of Antimicrobial Chemotherapy, vol. 66, no. 1, pp. 126–133, 2011.

P. Nikolic, and P. Mudgil, “The cell wall, cell membrane and virulence factors of staphylococcus aureus and their role in antibiotic resistance,” Microorganisms, vol. 11, no. 2, p. 259, 2023

B. Li, K. Zheng, J. Lu, D. Zeng, Q. Xiang, and Y. Ma, “Antibacterial characteristics of oregano essential oil and its mechanisms against Escherichia coli O157: H7,” Journal of Food Measurement and Characterization, vol. 16, no. 4, pp. 2989– 2998, 2022.

M. Gupta, N. Nayyar, M. Chawla, R. Sitaraman, R. Bhatnagar, and N. Banerjee, “The chromosomal parde2 toxin–antitoxin system of Mycobacterium tuberculosis H37Rv: Genetic and functional characterization,” Frontiers in microbiology, vol. 7, p. 886, 2016.

J. Su, Q. Guo, L. Mao, Y. Gao, and F. Yuan, “Effect of gum arabic on the storage stability and antibacterial ability of β-lactoglobulin stabilized d-limonene emulsion,” Food Hydrocolloids, vol. 84, pp. 75–83, 2018.

J. Kang, W. Jin, J. Wang, Y. Sun, X. Wu, and L. Liu, “Antibacterial and anti-biofilm activities of peppermint essential oil against Staphylococcus aureus,” LWT, vol.101, pp. 639–645, 2019.

H. Cui, M. Bai, Y. Sun, M. A. S. Abdel-Samie, and L. Lin, “Antibacterial activity and mechanism of Chuzhou chrysanthemum essential oil,” Journal of Functional Foods, vol. 48, pp. 159–166, 2018.

S. Liao, G. Yang, Y. Ou, S. Huang, B. Li, A. Li, and J. Kan, “Inhibitory impacts of essential oil (Zanthoxylum schinifolium Sieb. et Zucc) on the growth of Staphylococcus epidermidis,” Food Bioscience, vol. 49, 2022, Art. no. 101906.

Z. Pang, Q. Li, Y. Jia, W. Yan, J. Qi, Y. Guo, F. Hu, D. Zhou, and X. Jiang, “Controlling the pyridinium–zwitterionic ligand ratio on atomically precise gold nanoclusters allowing for eradicating Gram-positive drug-resistant bacteria and retaining biocompatibility,” Chemical Science, vol. 12, no. 44, pp. 14871–14882, 2021.

F. Lv, H. Liang, Q. Yuan, and C. Li, “In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms,” Food Research International, vol. 44, no. 9, pp. 3057–3064, 2011.

Y. B. Zhang, X. Y. Liu, Y. F. Wang, P. P. Jiang, and S. Quek, “Antibacterial activity and mechanism of cinnamon essential oil against Escherichia coli and Staphylococcus aureus,” Food Control, vol. 59, pp. 282–289, 2016.