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Chemical composition and antibacterial activities of Juniperus horizontalis essential oil
T. Eryig˘it, N. Okut, K. Ekici, and B. Yildirim 323327
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H. M. Hassan, Z.-H. Jiang, C. Asmussen,
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Nitrogen form, time and rate of application, and nitrification inhibitor effects on crop production R. E. Karamanos, K. Hanson, and
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Chemical composition and antibacterial activities of
Juniperus horizontalis
essential oil
T. Eryig˘it
1, N. Okut
2, K. Ekici
3, and B. Yildirim
11Department of Field Crops, Ig˘dir University, Turkey;2Department of Field Crops, Van Yuzuncu Yil
University, Turkey; and3Department of Biology, Van Yuzuncu Yil University, Turkey.
Received 24 July 2013, accepted 29 October 2013. Published on the web 31 October 2013.
Eryig˘it, T., Okut, N., Ekici, K. and Yildirim, B. 2014. Chemical composition and antibacterial activities of Juniperus horizontalis essential oil. Can. J. Plant Sci. 94: 323327. In recent years, the screening of antibacterial activity has been the subject of much research, and the antibacterial activity of essential oils could be a promising subject for future investigation. In this study, the antibacterial activities of Juniperus horizontalis essential oils and their components were investigated. Essential oils were isolated using the hydro-distillation method and their components were analyzed by gas chromatographymass spectrometry (GC-MS). The main compounds found in the oil of leaves were linalool (33.76%), P-cymene (23.20%), gamma-terpinene (8.67%), trans-sabinene hydrate (8.59%), thyme camphor (8.49%), carvol (5.08%) and borneol (4.22%). Juniperus horizontalis essential oils were evaluated for antibacterial activity against six bacterial strains using the disc diffusion method. The results indicate that the essential oil of J. horizontalis shows variable and significant antibacterial activities against the six tested bacteria species. The diameters of the inhibition zones formed for bacteria were measured. The lowest inhibition zone was 12 mm (sensitive) against Pseudomonas aeruginosaATCC 10145 and the highest zone was 32 mm (extremely sensitive) against Enterococcus faecalis ATCC 29212.
Key words: Antibacterial activity, gas chromatographymass spectrometry, essential oil, Juniperus horizontalis Eryig˘it, T., Okut, N., Ekici, K. et Yildirim, B. 2014. Composition chimique et pouvoir antibacte´rien de l’huile essentielle de Juniperus horizontalis.Can. J. Plant Sci. 94: 323327. Depuis quelques anne´es, le de´pistage des proprie´te´s antibacte´riennes fait l’objet de maintes recherches, car, en raison d’un tel pouvoir, les huiles essentielles pourraient devenir des agents prometteurs qui justifieront de vastes e´tudes a` l’avenir. Les auteurs se sont penche´s sur le pouvoir antibacte´rien de l’huile essentielle de Juniperus horizontalis et de ses composants. L’huile essentielle a e´te´ purifie´e par hydro-distillation et ses constituants ont e´te´ analyse´s par chromatographie en phase gazeuse/spectrome´trie de masse (GC-MS). Les principaux constituants de l’huile issue des feuilles sont le linalool (33,76 %), le p-cyme`ne (23,20 %), le gamma-terpine`ne (8,67 %), l’hydrate de trans-sabine`ne (8,59 %), le camphre du thym (8,49 %), le carvol (5,08 %) et le borne´ol (4,22 %). On a teste´ le potentiel antibacte´rien de l’huile essentielle de J. horizontalis sur six souches bacte´riennes, selon la me´thode de diffusion en ge´lose. Les re´sultats indiquent que le pouvoir antibacte´rien de l’huile essentielle de J. horizontalis sur les six bacte´ries teste´es varie. Les auteurs ont mesure´ le diame`tre de la zone d’inhibition de la croissance bacte´rienne. La plus petite zone avait 12 mm (sensible) sur une culture de Pseudomonas aeruginosa ATCC 10145; la plus grande mesurait 32 mm (tre`s sensible) sur une culture d’Enterococcus faecalis ATCC 29212.
Mots cle´s: Activite´ antibacte´rienne, GC-MS, huile essentielle, Juniperus horizontalis
Many plants have been used throughout human history for the treatment of disease. These plants have great importance in traditional folk medicines. Herbal medi-cines have been the basis of treatment and cure for various diseases in traditional methods. Therefore, herbal drugs have been a part of the evolution of human healthcare to sustain a healthy way of living for thousands of years (Govindarajan et al. 2008; Faydaog˘lu and Su¨ru¨cu¨og˘lu 2011). Many types of medicines used today are obtained from medicinal plants. Throughout the world, plants existing in the natural flora have been used for many different purposes, e.g., treatment, food, tea, spices, paint, insecticide, veterinary medicine, resin, glue, essen-tial oil, beverage and in the cosmetics industry that has been a part of our traditional culture for years (Faydaog˘lu and Su¨ru¨cu¨og˘lu 2011).
Juniperus is the second most diverse genus of the conifers. The genus Juniperus, belonging to Cupresse-ceae family, contains at least 60 species. It is wide-spread in temperate regions of the Eastern Hemisphere, Europe (including the Azores, the Canary Islands, Asia Minor and Africa), central Asia (Turkmenistan to the western Himalayas), China, the Far East (Japan, Korea, Sakhalin Island, Taiwan), the Western Hemisphere, Continental North America, the United States and Canada, Mexico, Guatemala, and the Caribbean (Adams 2008).
Creeping juniper (Juniper horizontalis) is an evergreen prostrate (sprawling) woody plant that grows mainly along the ground rather than vertically. The creeping
Abbreviation: GC-MS, gas chromatographymass spectrometry Can. J. Plant Sci. (2014) 94: 323327 doi:10.4141/CJPS2013-242 323
branches produce short erect branches with scale-like leaves. The leaves are green, but turn reddish purple in winter. The seed cones, which generally mature in 2 yr, are of two distinct sizes and contain several seeds each. Creeping juniper withstands hot, dry situations, but is very intolerant of shade and poor drainage. It is slow-growing, long-lived and susceptible to juniper blight.
The potential applications of Juniperus oils include aromatherapy, mood scents, scent masks, soaps, can-dles, cosmetics, fragrances, and lotions (Yesenofski 1996). Juniperus species are also used in traditional medicine for the treatment of hyperglycemia, tubercu-losis, bronchitis, pneumonia, ulcers, intestinal worms, to heal wounds and cure liver diseases (Burits et al. 2001; Ehsani et al. 2012a; Jirovetz et al. 2003).
The antibacterial activity of different extracts is being investigated throughout the world. New and effective antimicrobial agents and components with broad-spectrum activities from natural sources are now becom-ing the demand of the day, because of the development of resistance by pathogens to modern antibiotics caused by their indiscriminate use (Ehsani et al. 2012b; Kakar et al. 2012). So, instead of chemical medicine, the use of drugs derived from natural sources has gained importance. Plant essential oils, used individually or in combination, may provide an efficacious method of inactivating microorganisms (Bauer et al. 1996).
Many plants, because of their essential oil chemical compounds, exhibit antimicrobial activity (Celikel 2008). Essential oils are aromatic oily liquids obtained from plant material (flowers, buds, seeds, leaves, twigs, bark, herbs, fruits and roots). They can be obtained by expression, fermentation, enfleurage or extraction, but steam distillation is the most commonly used method for commercial production of essential oils (Burt 2004). A unit commonly used in the measurement of anti-microbial activity is the diameter of the zone of inhibition of bacterial growth on a solid medium. For plant essential oil samples, the zone of inhibition will depend on the ability of oil to diffuse uniformly through an agar medium and the effect on bacteria of oil vapors that may be released (Friedman et al. 2002).
Plant essential oils are a potentially useful source of antimicrobial compounds (Friedman et al. 2002), but essential oils have very complex chemical make-ups and no batch is ever the same. A single oil may have dozens or even hundreds of chemical constituents all working together. The biological activity of essential oils depends on their chemical composition, which is determined by the plant genotype, and is greatly influenced by several factors, such as geographical origin, and environmental and agronomic conditions (Yaldiz and S¸ekerog˘lu 2012). Because of that, the flora of plants has significant effects on their essential oils.
Turkey has a rich flora of medicinal plants that is widely distributed throughout the country. Van pro-vince, in particular, possesses rich medicinal herbal resources, but they have not been evaluated
scientifi-cally. Different plants of the province or its regions are generally used to treat different animals and human ailments.
The aim of this study was to identify the chemical composition and to provide an overview of antibacterial activity of essential oils of J. horizontalis leaves.
MATERIALS AND METHODS
Plant Collection and Isolation of Essential Oils Plants
The leaves of creeping J. horizontalis (Cupresseceae) were collected in August 2010 from wild populations growing in the plateaus and rangelands of Mount Artos, in Gevas¸ county, Van, Turkey, at an altitude of 1730 1950 m.
The taxonomic identification of the plant materials was performed by a plant taxonomist, Fevzi O¨zgo¨kc¸e, in the Department of Biology, Yuzuncu Yil University, Van, Turkey, and plants were grouped according to the names of species and localities where they were col-lected. The collected plant materials were then air dried in the shade and ground into small particles.
Isolation of the Essential Oil
Shade-dried plant material was subjected to hydrodis-tillation for 3 h using a Clevenger apparatus, in Department of Field Crops, Faculty of Agriculture, Yuzuncu Yil University.
Gas Chromatography
Mass Spectrometry Temperature ProgramThe analyses were carried out using a Shimadzu QP2010 brand model gas chromatographymass spectrometry (GC-MS) instrument equipped with a TRB-WAX column (30 m 0.25 mm film, thickness 0.25 mm). The oven temperature was 60 to 2408C with increments at a rate of 108C min1. Helium was used as the carrier gas with a linear velocity of 36.25 cm s1, split ratio was 1:50, ionization source temperature was 2008C, interface temperature was 2408C and mass range was 40 to 350 amu (resolution). The essential oil compounds were identified by comparison of their mass spectra with those in the device computer libraries (Wiley and Nist).
Identification of Essential Oil Components
The essential oils obtained were transferred from the water to the solvent (N-hexane) and after dilution the components were identified by GC-MS. The essential oil components were identified in a preliminary study of previously collected plant species. The best temperature program for the GC-MS analysis of the essential oils was subsequently determined and the same program was used for all samples.
Determination of Anti-bacterial Activity Microorganisms
Six bacterial species were used to test the antimicrobial activity of J. horizontalis essential oils. The microorgan-isms were Staphylococcus aureus ATCC 12600, Bacillus subtilis ATCC 6051, Pseudomonas aeruginosa ATCC 10145, Enterococcus faecalis ATCC 29212, Salmonella typhimurium ATCC 25241, and Escherichia coli ATCC 11775.
Disc Diffusion Method
Antimicrobial activity was identified using the agar disc diffusion method proposed by Bauer et al. (1966). McFarland standard was prepared by adding 0.5 mL of 0.048 M BaC12 (1.17% wt/vol BaC12×2H2O) to 99.5
mL of 0.18 M H2SO4 (1% wt/vol) while stirring
constantly (Andrews 2004). The cultures, which were frozen in Glycerol Nutrient Brotta (Oxoid), dissolved in the refrigerator. They were then activated in Tryptic Soy broth (Oxoid) for 24 h.
Brain Hard Infusion Brotta (Oxoid) was activated from Tryptic Soy Agar (Oxoid) passages for 34 h. The density of these cultures was adjusted according to the McFarland 0.5 tubes blur.
Activated microorganisms were spread on the surface of predetermined MuellerHinton Agar (Merck) plates using a sterile swap, and incubated for half an hour. Paper discs (6 mm diameter, Whatman 2017-006) were impregnated with essential oils and transferred onto the MuellerHinton agar plates, whose surface had been spread with 0.5 mL of bacterial suspension.
Ampicilline and ofloxocine were used as control agents (O¨zc¸elik et al. 2005). Microorganisms were incubated in the oven according to the species and suitable temperaturetime. After the colonies formed around the zones, the zones were measured with the inhibition zone scale in millimeters. The sensitivity of the bacterial species to the essential oils was determined by comparing the sizes of inhibitory zones (Ponce et al. 2003).
The results were evaluated as follows: zones that were smaller than 8 mm were classified as insensitive, zones 914 mm were sensitive, zones 1519 mm were very sensitive, and those larger than 20 mm were extremely sensitive (Ponce et al. 2003). Each assay was carried out in duplicate.
RESULTS AND DISCUSSION Chemical Composition of the Essential Oil
As shown in Table 1, GC-MS analysis of the crude oil resulted in the identification of 11 compounds repre-senting 94.50% of the essential oil. Linalool (33.76%), P-cymene (23.20%), gamma-terpinene (8.67%), trans-sabinene hydrate (8.59%), thyme camphor (8.49%), carvol (5.08%) and borneol (4.22%) were the main compounds.
In this study, the antibacterial activity of essential oils from J. horizontalis leaves was determined. The extracts of J. horizontalis leaves showed a significant zone of inhibition against S. aureus ATCC 12600, B. subtilis ATCC 6051, E. faecalis ATCC 29212, S. typhimurium ATCC 25241, P. aeruginosa ATCC 10145 and E. coli ATCC 11775 (Table 2).
The results indicate that the tested crude extracts showed antibacterial activity towards the microorgan-isms, but, antimicrobial activity of the essential oil varies according to the species of microorganisms. Extracts of J. horizontalis leaves were tested against microorgan-isms, and the results revealed that all extracts showed high activity against six microorganism except P. aeruginosaATCC 2601 (Table 2).
The comparison of the antibacterial activity of essential oils of J. horizontalis and two antibiotics (ampicillin and ofloxacin) are presented in Table 1 and Fig. 1.
All tested bacterial species were sensitive to the essential oils of J. horizontalis leaves at a concentration of 20%, with the inhibition zones ranging from 12 to 32 mm (Table 2).
Table 1. Chemical composition of the essential oils of Juniperus horizontalis leaves
Peak Component Retention time Rate (%)
1 Limonene 3 176 1.47
2 Trans-sabinene hydrate 3 310 8.59 3 Gamma-terpinene 3 758 8.67
4 P-cymene 4 115 23.20
5 Trans linalool oxide 6 671 0.12
6 Camphor 7 791 0.36 7 Linalool 8 206 33.76 8 1-4 terpineol 8 987 0.54 9 Borneol 10 344 4.22 10 Thyme camphor 13 823 8.49 11 Carvol 16 178 5.08 Total 94.50
Table 2. Antimicrobial activity of Juniperus horizontalis essential oils (in mL) and two antibiotics (ampicillin and ofloxacin) against some pathogens (inhibition zones in mm)z
Antibiotic/ essential oily Ampicillin Ofloxacin J. horizontalis
Sa ATCC 12600 20 26 22 Bs ATCC 6051 25 30 20 Pa ATCC 10145 23 26 12 Ef ATCC 29212 26 20 32 St ATCC 25241 22 24 30 Ec ATCC 11775 28 28 26
zNot sensitive () for total diameter smaller than 8 mm, sensitive ()
for total diameter 914 mm, very sensitive () for total diameter 15 19 mm and extremely sensitive () for total diameter larger than 20 mm.
ySa, Staphylococcus aureus; Bs, Bacillus subtilis; Pa, Pseudomonas
aeruginosa; Ef, Enterococcus faecalis; St, Salmonella typhimurium; Ec, Escherichia coli.
In the present study, J. horizontalis showed variable antibacterial activities against six microorganisms. The inhibition zones of essential oils ranged from 12 to 32 mm. The smallest zone was 12 mm (sensitive) against P. aeruginosaATCC 10145 and the largest zone was 32 mm (extremely sensitive) against E. faecalis ATCC 29212 (Table 2 and Figs. 1 and 2).
In contrast to our results, it was reported that the essential oil of J. horizontalis leaves exhibited better antimicrobial activity against all the tested bacteria (Ehsani et al. 2012a). In addition, the essential oil of J. horizontalisshowed more antibacterial activity as com-pared with the chemical antibiotics ampicillin and ofloxacin.
The results of this study show that the J. horizontalis essential oils possess antibacterial properties, illustrating their potential to be used as natural antibacterial agents to treat infectious diseases. Furthermore, the
develop-ment and the use of natural antibacterial agents will help to decrease negative effects of modern antibiotics (chemical drugs).
The observed antibacterial properties show that the plant has potential for use in aromatherapy and pharmacy. Further laboratory and clinical studies of this plant are required in order to better understand its antibacterial activities, which will allow researchers to recommend its use as an accessible alternative to other synthetic drugs (antibacterial, antibiotics).
ACKNOWLEDGEMENTS
My heartiest thanks to Prof. Dr. B. Yildirim (Research supervisor), Head Department of Field Crops, Ig˘dIr University, Faculty of Agriculture.
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Fig. 1. The comparison of antimicrobial activity of essential oils of Juniperus horizontalis leaves and two antibiotics (ampicillin and ofloxacin). Sa, Staphylococcus aureus; Bs, Bacillus subtilis; Pa, Pseudomonas aeruginosa; Ef, Enterococcus faecalis; St, Salmonella typhimurium; Ec, Escherichia coli.
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