Abstract
Chemical composition and bioactivities including bacterial and fungal resistance of the essential oils extracted from leaves of Piper betle L. (T) and Cleistocalyx operculatus L. (V) and aerial parts of Ageratum conyzoides L. (H) were investigated. The components presenting in the essential oils of the natural sources were analysized by a gas chromatography–mass spectrometry. Molecular docking simulation was utilised to support an antimicrobial mechanism of the essential oil compounds on Candida albicans fungus and Streptococcus pyogenes bacteria. This was based on the inhibition of the extracted compounds onto the microbial proteins, i.e. 4ESW and P0C0C7, respectively. There are 32 compounds identified in total in the three essential oils. The most effective inhibitors are the following: (i) chavicol acetate (T3), eugenol acetate (T11) and eugenol (T4) found in Piper betle L.; (ii) precocene II (H10) and precocene I (H6) found in Ageratum conyzoides L.; and (iii) caryophyllene oxide (V15) and cis-Lanceol (V19) found in Cleistocalyx operculatus L.. The overall antifungal and antibacterial capability of the investigated essential oils given indirect justification via their average inhabitability towards the two proteins accords with the order Piper betle L. Ageratum conyzoides L. Cleistocalyx operculatus L.. The results suggest these as promising natural sources for antimicrobial remedies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adil M, Baig MH, Rupasinghe H (2019) Impact of citral and phloretin, alone and in combination, on major virulence traits of Streptococcus pyogenes. Molecules 24:4237. https://doi.org/10.3390/molecules24234237
Alakanse O, Sulaiman F, Arannilewa A, Anjorin F, Malachi O (2018) α-Selinene from Syzygium aqueum against aromatase p450 in breast carcinoma of postmenopausal women: in silico study. J Biomed Pharm Sci 2:1
Babu TMC, Rajesh SS, Bhaskar BV, Devi S, Rammohan A, Sivaraman T, Rajendra W (2017) Molecular docking, molecular dynamics simulation, biological evaluation and 2D QSAR analysis of flavonoids from Syzygium alternifolium as potent anti-Helicobacter pylori agents. RSC Adv 7:18277–18292. https://doi.org/10.1039/c6ra27872h
Boukeria S, Kadi K, Kalleb R, Benbott A, Bendjedou D, Yahia A (2016) Phytochemical and physicochemical characterization of Allium sativum L. and Allium cepa L. essential oils. J Mater Environ Sci. 7:2362–2368
Chandra M, Prakash O, Kumar R, Bachheti RK, Bhushan B, Kumar M, Pant AK (2017) β-Selinene-rich essential oils from the parts of Callicarpa macrophylla and their antioxidant and pharmacological activities. Medicines. 4:52. https://doi.org/10.3390/medicines4030052
Chauhan ES, Aishwarya J, Singh A, Tiwari A (2016) A review: nutraceuticals properties of Piper betel (Paan). Am J Phytomed Clin Ther. 4:28–41
Chavan M, Wakte P, Shinde D (2010) Analgesic and anti-inflammatory activity of Caryophyllene oxide from Annona squamosa L. bark. Phytomedicine 17:149–151. https://doi.org/10.1016/j.phymed.2009.05.016
Ciftci O, Ozdemir I, Tanyildizi S, Yildiz S, Oguzturk H (2011) Antioxidative effects of curcumin, β-myrcene and 1, 8-cineole against 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin-induced oxidative stress in rats liver. Toxicol Ind Health 27:447–453. https://doi.org/10.1177/0748233710388452
Devi KP, Nisha SA, Sakthivel R, Pandian SK (2010) Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 130:107–115. https://doi.org/10.1016/j.jep.2010.04.025
Diao W-R, Hu Q-P, Zhang H, Xu J-G (2014) 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
Doh KS, N’guessan K, Aké CB (2014) Effect of aqueous extract of ageratum conyzoides leaves on the glycaemia of rabbits. Pharm Innovat J 2:1–8
Dosoky NS, Pokharel SK, Setzer WN (2015) Leaf essential oil composition, antimicrobial; and cytotoxic activities of Cleistocalyx operculatus from Hetauda, Nepal. Am J Essent Oil Nat Prod. 3:34–37
Dung NT, Kim JM, Kang SC (2008) Chemical composition, antimicrobial and antioxidant activities of the essential oil and the ethanol extract of Cleistocalyx operculatus (Roxb.) Merr and Perry buds. Food Chem Toxicol 46:3632–3639. https://doi.org/10.1016/j.fct.2008.09.013
El Mokni R, Majdoub S, Chaieb I, Jlassi I, Joshi RK, Hammami S (2019) Chromatographic analysis, antimicrobial and insecticidal activities of the essential oil of Phlomis floccosa D. Don Biomed Chromatogr 33:e4603. https://doi.org/10.1002/bmc.4603
ElSohly MA, Radwan MM, Gul W, Chandra S, Galal A (2017) Phytochemistry of Cannabis sativa L. Prog Chem Org Nat Prod. https://doi.org/10.1007/978-3-319-45541-9_1
Farré-Armengol G, Filella I, Llusià J, Peñuelas J (2017) β-Ocimene, a key floral and foliar volatile involved in multiple interactions between plants and other organisms. Molecules 22:1148. https://doi.org/10.3390/molecules22071148
Fidyt K, Fiedorowicz A, Strządała L, Szumny A (2016) β-caryophyllene and β-caryophyllene oxide-natural compounds of anticancer and analgesic properties. Cancer Med 5:3007–3017. https://doi.org/10.1002/cam4.816
Gao Q, Wang Y, Hou J, Yao Q, Zhang J (2017) Multiple receptor-ligand based pharmacophore modeling and molecular docking to screen the selective inhibitors of matrix metalloproteinase-9 from natural products. J Comput Aided Mol Des 31:625–641
Govindarajan M, Benelli G (2016) Eco-friendly larvicides from Indian plants: effectiveness of lavandulyl acetate and bicyclogermacrene on malaria, dengue and Japanese encephalitis mosquito vectors. Ecotoxicol Environ Saf 133:395–402. https://doi.org/10.1016/j.ecoenv.2016.07.035
Gul A, Akhter Z, Perveen F, Kalsoom S, Ansari FL, Siddiq M (2019) Molecular docking and quantitative structure activity relationship (QSAR) studies of some newly synthesized poly (azomethine) esters. Int J Polym Sci 2019:1–10. https://doi.org/10.1155/2019/2103891
Iqbal M, Jayasinghe U, Herath H, Wijesekara K, Fujimoto Y (2004) A fungistatic chromene from Ageratum conyzoides. Phytoparasitica 32:119–126. https://doi.org/10.1007/bf02979776
Juergens UR, Dethlefsen U, Steinkamp G, Gillissen A, Repges R, Vetter H (2003) Anti-inflammatory activity of 1.8-cineol (eucalyptol) in bronchial asthma: a double-blind placebo-controlled trial. Respir Med 97:250–256. https://doi.org/10.1053/rmed.2003.1432
Karak S, Acharya J, Begum S, Mazumdar I, Kundu R, De B (2018) Essential oil of Piper betle L. leaves: chemical composition, anti-acetylcholinesterase, anti-β-glucuronidase and cytotoxic properties. J Appl Res Med Aromat Plants 10:85–92. https://doi.org/10.1016/j.jarmap.2018.06.006
Khosravi DN, Ostad S, Maafi N, Pedram S, Ajani Y, Hadjiakhoondi A, Khanavi M (2014) Cytotoxic activity of the essential oil of Salvia verticillata L. Res J Pharmacognosy 1:27–33
Lai R-Y et al (2012) Thiamin pyrimidine biosynthesis in Candida albicans: a remarkable reaction between histidine and pyridoxal phosphate. J Am Chem Soc 134:9157–9159. https://doi.org/10.1021/ja302474a
Liao SY, Chen JC, Qian L, Shen Y, Zheng KC (2008) QSAR, action mechanism and molecular design of flavone and isoflavone derivatives with cytotoxicity against HeLa. Eur J Med Chem 43:2159–2170. https://doi.org/10.1016/j.ejmech.2007.10.033
Mai TT, Fumie N, Van Chuyen N (2009) Antioxidant activities and hypolipidemic effects of an aqueous extract from flower buds of Cleistocalyx operculatus (Roxb.) Merr. Perry J Food Biochem 33:790–807. https://doi.org/10.1111/j.1745-4514.2009.00251.x
Matsuda H, Ando S, Morikawa T, Kataoka S, Yoshikawa M (2005) Structure–activity relationships of 1′ S-1′-acetoxychavicol acetate for inhibitory effect on NO production in lipopolysaccharide-activated mouse peritoneal macrophages. Bioorg Med Chem Lett 15:1949–1953. https://doi.org/10.1016/j.bmcl.2005.01.070
Muñoz A, Sojo F, Arenas DRM, Kouznetsov VV, Arvelo F (2011) Cytotoxic effects of new trans-2, 4-diaryl-r-3-methyl-1, 2, 3, 4-tetrahydroquinolines and their interaction with antitumoral drugs gemcitabine and paclitaxel on cellular lines of human breast cancer. Chem Biol Interact 189:215–221. https://doi.org/10.1016/j.cbi.2010.11.010
Nikolić B, Mitić-Ćulafić D, Vuković-Gačić B, Knežević-Vukčević J (2011) Modulation of genotoxicity and DNA repair by plant monoterpenes camphor, eucalyptol and thujone in Escherichia coli and mammalian cells. Food Chem Toxicol 49:2035–2045. https://doi.org/10.1016/j.fct.2011.05.015
Novato T et al (2018) In vitro assessment of the acaricidal activity of carvacrol, thymol, eugenol and their acetylated derivatives on Rhipicephalus microplus (Acari: Ixodidae). Vet Parasitol 260:1–4. https://doi.org/10.1016/j.vetpar.2018.07.009
Palmer-Young EC, Veit D, Gershenzon J, Schuman MC (2015) The sesquiterpenes (E)-ß-farnesene and (E)-α-bergamotene quench ozone but fail to protect the wild tobacco Nicotiana attenuata from ozone, UVB, and drought stresses. PLoS ONE 10:e0127296. https://doi.org/10.1371/journal.pone.0127296
Paridhi B, Ashita U, Swati P, Dilip N (2016) An invitro study of determination of anti-bacterial, antioxidant, anti-inflammatory potential of piper betel. Essential Oil 6:37–44
Patil S et al (2010) Synthesis, cytotoxicity and antibacterial studies of p-methoxybenzyl-substituted and benzyl-substituted N-heterocyclic carbene–silver complexes. Eur J Inorg Chem 2010:1020–1031. https://doi.org/10.1002/ejic.200900889
Rahmani R, Andersson F, Andersson MN, Yuvaraj JK, Anderbrant O, Hedenström E (2019) Identification of sesquisabinene B in carrot (Daucus carota L.) leaves as a compound electrophysiologically active to the carrot psyllid (Trioza apicalis Förster). Chemoecology 29:103–110. https://doi.org/10.1007/s00049-019-00280-6
Rani N, Kumar P, Singh R, Sharma A (2015) Molecular docking evaluation of imidazole analogues as potent Candida albicans 14α-demethylase inhibitors. Curr Comput Aid Drug 11:8–20. https://doi.org/10.2174/1573409911666150617113645
Row LCM, Ho JC (2009) The antimicrobial activity, mosquito larvicidal activity, antioxidant property and tyrosinase inhibition of Piper betle. J Chin Chem Soc 56:653–658. https://doi.org/10.1002/jccs.200900097
Rozza AL et al (2011) Gastroprotective mechanisms of Citrus lemon (Rutaceae) essential oil and its majority compounds limonene and β-pinene: involvement of heat-shock protein-70, vasoactive intestinal peptide, glutathione, sulfhydryl compounds, nitric oxide and prostaglandin E2. Chem Biol Interact 189:82–89. https://doi.org/10.1016/j.cbi.2010.09.031
Sapra A, Kumar P, Kakkar S, Narasimhan B (2014) Synthesis, antimicrobial evaluation and QSAR studies of p-hydroxy benzoic acid derivatives. Drug Res 64:17–22. https://doi.org/10.1055/s-0033-1349866
Thanh L, Dung NX, Bighelliand A, Casanova J, Leclercq PA (1997) Combination of capillary GC, GC/MS and 13C-NMR for the characterization of the rhizome oil of Piper betle L. (Piperaceae) from Vietnam. Spectroscopy 13:131–136. https://doi.org/10.1155/1997/397354
Tong T, Park J, Moon C, Park T (2018) Regulation of adipogenesis and thermogenesis through mouse olfactory receptor 23 stimulated by α-Cedrene in 3T3-L1 cells. Nutrients 10:1781. https://doi.org/10.3390/nu10111781
Ueda-Nakamura T et al (2006) Antileishmanial activity of Eugenol-rich essential oil from Ocimum gratissimum. Parasitol Int 55:99–105. https://doi.org/10.1016/j.parint.2005.10.006
Ukwe Chinwe V, Ekwunife Obinna I, Epueke Ebele A, Ubaka Chukwuemeka M (2010) Antimalarial activity of Ageratum conyzoides in combination with chloroquine and artesunate. Asian Pac J Trop Med 3:943–947. https://doi.org/10.1016/s1995-7645(11)60005-9
Vietnamese Pharmacopoeia (1997) Medical Publishing House, Hanoi, Vietnam
Crystal structure of C. albicans Thi5 H66G mutant. https://www.rcsb.org/structure/4ESW
S-ribosylhomocysteinase from Streptococcus suis. Https://www.rcsb.org/structure/4xch
S-ribosylhomocysteine lyase. https://www.uniprot.org/uniprot/P0C0C7
Acknowledgments
This research is funded by the Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 104.06-2017.303 (Nguyen Thi Ai Nhung).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
There is no ethical issue related to this study.
Conflict of interest
The authors have declared no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Thuy, B.T.P., Hieu, L.T., My, T.T.A. et al. Screening for Streptococcus pyogenes antibacterial and Candida albicans antifungal bioactivities of organic compounds in natural essential oils of Piper betle L., Cleistocalyx operculatus L. and Ageratum conyzoides L.. Chem. Pap. 75, 1507–1519 (2021). https://doi.org/10.1007/s11696-020-01404-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11696-020-01404-x