α-Terpineol, terpinen-4-ol, and δ-terpineol, isomers of terpineol, are among the compounds that give Cinnamomum longepaniculatum leaf oil its distinguished pleasant smell. The objective of this study was to evaluate the antimicrobial activity of these three isomeric terpineols. The determination of antibacterial activity was based on the minimum inhibition concentration (MIC) and minimum bactericide concentration (MBC). Changes in time-kill curve, alkaline phosphatase (AKP), UV-absorbing material, membrane potential, and scanning electron microscopy (SEM) were measured to elucidate the possible antimicrobial mechanism. α-Terpineol, terpinen-4-ol, and δ-terpineol demonstrated good inhibitory effects against several gram-negative bacteria, particularly Shigella flexneri. MIC and MBC of α-terpineol and terpinen-4-ol were similar (0.766 mg/mL and 1.531 mg/mL, respectively) for S. flexneri, while the MIC and MBC values of δ-terpineol were 0.780 mg/mL and 3.125 mg/mL, respectively. Time-kill curves showed that the antibacterial activities of the tested compounds were in a concentration-dependent manner. Release of nucleic acids and proteins along with a decrease in membrane potential proved that α-terpineol, terpinen-4-ol, and δ-terpineol could increase the membrane permeability of Shigella flexneri. Additionally, the release of AKP suggested that the cell wall was destroyed. SEM analysis further confirmed that S. flexneri cell membranes were damaged by α-terpineol, terpinen-4-ol, and δ-terpineol. Our research suggests that these three isomeric terpineols have the potential of being used as natural antibacterial agents by destroying the cell membrane and wall, resulting in cell death. However, the specific antibacterial activity differences need further investigation.

College of Food and Biotechnology Xihua University Chengdu 610039 People's Republic of China

Key Lab of Aromatic Plant Resources Exploitation and Utilization in Sichuan Higher Education Yibin University Yibin 644000 People's Republic of China

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Alviano WS, Mendonça-Filho RR, Alviano DS, Bizzo HR, Souto-Padrón T, Rodrigues ML, Bolognese AM, Alviano CS, Souza MMG (2005) Antimicrobial activity of Croton cajucara Benth linalool-rich essential oil on artificial biofilms and planktonic microorganisms. Oral Microbiol Immunol 20:101–105. https://doi.org/10.1111/j.1399-302X.2004.00201.x PubMed DOI

Benameur Q, Gervasi T, Pellizzeri V, Pľuchtová M, Tali-Maama H, Assaous F, Guettou B, Rahal K, Gruľová D, Dugo G, Marino A, Ben-Mahdi MH (2018) Antibacterial activity of Thymus vulgaris essential oil alone and in combination with cefotaxime against blaESBL producing multidrug resistant Enterobacteriaceae isolates. Nat Prod Res 33:1–8. https://doi.org/10.1080/14786419.2018.1466124 DOI

Cao JR, Fu HJ, Gao LH, Zheng Y (2019) Antibacterial activity and mechanism of lactobionic acid against Staphylococcus aureus. Folia Microbiol 64:899–906. https://doi.org/10.1007/s12223-019-00705-3 DOI

Diao WR, Hu QP, Zhang H, Xu JG (2014a) Chemical composition, antibacterial activity and mechanism of action of essential oil from seeds of fennel (Foeniculum vulgare Mill.). Food Control 35:109–116. https://doi.org/10.1016/j.foodcont.2013.06.056 DOI

Diao WR, Zhang LL, Feng SS, Xu JG (2014b) Chemical composition, antibacterial activity, and mechanism of action of the essential oil from Amomum kravanh. J Food Prot 77:1740–1746. https://doi.org/10.4315/0362-028X.JFP-14-014 PubMed DOI

Du YH, Feng RZ, Li Q, Wei Q, Yin ZQ, Zhou LJ, Tao C, Jia RY (2014) Anti-inflammatory activity of leaf essential oil from Cinnamomum longepaniculatum (Gamble) N. Chao. Int J Clin Exp Med 7:5612–5620 PubMed PMC

Hart PH, Brand C, Carson CF, Riley TV, Prager RH, Finlay-Jones JJ (2000) Terpinen-4-ol, the main component of the essential oil of Melaleuca alternifolia (tea tree oil), suppresses inflammatory mediator production by activated human monocytes. Inflamm Res 49:619–626. https://doi.org/10.1007/s000110050639 PubMed DOI

Iseppi R, Sabia C, de Niederhäusern S, Pellati F, Benvenuti S, Tardugno R, Bondi M, Messi P (2019) Antibacterial activity of Rosmarinus officinalis L. and Thymus vulgaris L. essential oils and their combination against food-borne pathogens and spoilage bacteria in ready-to-eat vegetables. Nat Prod Res 33:3568–3572. https://doi.org/10.1080/14786419.2018.1482894 PubMed DOI

Kabat AG (2019) In vitro demodicidal activity of commercial lid hygiene products. Clin Ophthalmol (Auckland, N.Z.) 13:1493–1497. https://doi.org/10.2147/OPTH.S209067 DOI

Kentaro N, Kazumi H, Ishijima SA, Naho M, Hiroshi I, Junichi K, Shigeru A (2013) Suppression of inflammatory reactions by terpinen-4-ol, a main constituent of tea tree oil, in a murine model of oral candidiasis and its suppressive activity to cytokine production of macrophages in vitro. Biol Pharm Bull 36:838–844. https://doi.org/10.1248/bpb.b13-00033 DOI

Khaleel C, Tabanca N, Buchbauer G (2018) alpha-Terpineol, a natural monoterpene: a review of its biological properties. Open Chem 16:349–361 DOI

Kotan R, Kordali S, Cakir A (2007) Screening of antibacterial activities of twenty-one oxygenated monoterpenes. Zeitschrift Für Naturforschung C 62:507–513. https://doi.org/10.1515/znc-2007-7-808 DOI

Kuchenmüller T, Abela-Ridder B, Corrigan T, Tritscher A (2013) World Health Organization initiative to estimate the global burden of foodborne diseases. Rev Sci Tech 32:459–467. https://doi.org/10.20506/rst.32.2.2249 PubMed DOI

Lansdown ABG (2010) A pharmacological and toxicological profile of silver as an antimicrobial agent in medical devices. Adv Pharmacol Sci 2010:1–16. https://doi.org/10.1155/2010/910686 DOI

Li L, Li ZW, Yin ZQ, Wei Q, Jia RY, Zhou LJ, Xu J, Song X, Zhou Y, Du YH, Peng LC, Kang S, Yu W (2014) Antibacterial activity of leaf essential oil and its constituents from Cinnamomum longepaniculatum. Int J Clin Exp Med 7:1721–1727 PubMed PMC

Liu MY, Liu F, Zhou T, Zhu YZ, Xu WM (2012) Anti-Bacillus cereus mechanisms of Fructus mume extract. Food Sci 33:103–105

Liu GR, Song ZQ, Yang XL, Gao YK, Wang CG, Sun BG (2016) Antibacterial mechanism of bifidocin A, a novel broad-spectrum bacteriocin produced by Bifidobacterium animalis BB04. Food Control 62:309–316. https://doi.org/10.1016/j.foodcont.2015.10.033 DOI

Mirza ZRMH, Hasan T, Seidel V, Yu J (2018) Geraniol as a novel antivirulence agent against bacillary dysentery-causing Shigella sonnei. Virulence 9:450–455. https://doi.org/10.1080/21505594.2017.1412031 PubMed DOI

Mirzoeva OK, Grishanin RN, Calaer PC (1997) Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria. Microbiol Res 152:239–246. https://doi.org/10.1016/s0944-5013(97)80034-1 PubMed DOI

Morin N, Lanneluc I, Connil N, Cottenceau M, Pons AM, Sablé S (2010) Mechanism of bactericidal activity of microcin L in Escherichia coli and Salmonella enterica. Antimicrob Agents Chemother 55:997–1007. https://doi.org/10.1128/AAC.01217-10 PubMed DOI PMC

Polyanna DSN, Soares DCD, Gomes DSV, Borges DCLI, Barbosa ND, Beatriz DMSF, Thiago DSLA, Venes RMJ, Ferreira DSR, Rita DCMO (2018) Antidiarrheal activity of α-terpineol in mice. Biomed Pharmacother 110:631–640. https://doi.org/10.1016/j.biopha.2018.11.131 DOI

Pramanik K, Ghosh PK, Ray S, Sarkar A, Mitra S, Maiti TK (2017) An in silico, structural, functional and phylogenetic analysis with three-dimensional protein modeling of alkaline phosphatase enzyme of Pseudomonas aeruginosa. J Gen Eng Biotechnol 15:527–537. https://doi.org/10.1016/j.jgeb.2017.05.003 DOI

Quintans-Júnior LJ, Oliveira MGB, Santana MF, Santana MT, Guimarães AG, Siqueira JS, Sousa DPD, Almeida RN (2011) α-Terpineol reduces nociceptive behavior in mice. Pharm Biol 49:583–586. https://doi.org/10.3109/13880209.2010.529616 PubMed DOI

Resa CPO, Gerschenson LN, Jagus RJ (2016) Starch edible film supporting natamycin and nisin for improving microbiological stability of refrigerated Argentinian Port Salut cheese. Food Control 59:737–742. https://doi.org/10.1016/j.foodcont.2015.06.056 DOI

Shatalov DO, Kedik SA, Zhavoronok ES, Aydakova AV, Ivanov IS, Evseeva AS, Beliakov SV, Biryulin SI, Kovalenko AV, Mikhailenko EN (2017) The current state and development of perspectives of application of synthetic antimicrobial agents. Polym Sci Ser D 10:293–299. https://doi.org/10.1134/S1995421217030157 DOI

Shi C, Sun Y, Zhang XR, Zheng ZW, Yang MC (2016a) Antimicrobial effect of lipoic acid against Cronobacter sakazakii. Food Control 59:352–358. https://doi.org/10.1016/j.foodcont.2015.05.041 DOI

Shi C, Sun Y, Zheng ZW, Zhang XR, Song KK, Jia ZY, Chen YF, Yang MC, Liu X, Dong R, Xia XD (2016b) Antimicrobial activity of syringic acid against Cronobacter sakazakii and its effect on cell membrane. Food Chem 8:291–309. https://doi.org/10.1016/j.foodchem.2015.10.100 DOI

Sousa DPD, Quintans L, Reinaldo Nóbrega de Almeida (2008) Evolution of the anticonvulsant activity of α-terpineol. Pharm Biol 45:69–70. https://doi.org/10.1080/13880200601028388 DOI

Southwell IA, Freeman S, Rubel D (1997) Skin irritancy of tea tree oil. J Essent Oil Res 9(1):47–52. https://doi.org/10.1080/10412905.1997.9700713 DOI

Wang W, Chen SW, Zhu J, Zuo S, Ma YY, Chen ZY, Zhang JL, Chen GW, Liu YC, Wang PY (2015) Intestinal alkaline phosphatase inhibits the translocation of bacteria of gut-origin in mice with peritonitis: mechanism of action. PLoS One 10:1–22. https://doi.org/10.1371/journal.pone.0124835 DOI

Wei Q, Li Q, Luo Y, Wu B (2006) Antifungal activity of leaf essential oil from Cinnamomum longepaniculatum (Gamble) N.Chao. Chin J Oil Crop Sci CNKI:SUN:ZGYW. 0.2006-01-013

Wu VCH, Qiu X, Reyes BGDL, Lin CS, Pan YJ (2009) Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157:H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa. Food Microbiol 26:32–38. https://doi.org/10.1016/j.fm.2008.07.014 PubMed DOI

Xu C, Li JL, Yang LQ, Shi F, Yang Y, Ye M (2017) Antibacterial activity and a membrane damage mechanism of Lachnum YM30 melanin against Vibrio parahaemolyticus and Staphylococcus aureus. Food Control 73:1445–1451. https://doi.org/10.1016/j.foodcont.2016.10.048 DOI

Zhang YB, Liu XY, Wang YF, Jiang PP, Quek SY (2016) Antibacterial activity and mechanism of cinnamon essential oil against Escherichia coli and Staphylococcus aureus. Food Control 59:282–289. https://doi.org/10.1016/j.foodcont.2015.05.032 DOI

Zhang YT, Feng RZ, Li LX, Zhou X, Li ZW, Jia RY, Song X, Zou YF, Yin LZ, He CL, Liang XX, Zhou WH, Wei Q, Du YH, Yan K, Wu ZL, Yin ZQ (2018) The antibacterial mechanism of terpinen-4-ol against Streptococcus agalactiae. Curr Microbiol 75:1214–1220. https://doi.org/10.1007/s00284-018-1512-2 PubMed DOI

Zheng XY, Guo JL, Rao HS, Guo D, Huang YX, Xu YF, Liang S, Xia XD, Shi C (2020) Antibacterial and antibiofilm activity of coenzyme Q0 against Vibrio parahaemolyticus. Food Control 109:106955. https://doi.org/10.1016/j.foodcont.2019.106955 DOI