Chemical Composition and Antibacterial Activity of the Essential Oil from Leaves of Zanthoxylum kleinii (R.S. Cowan) P.G. Waterman (Rutaceae)

Abstract

Z. kleinii is an endemic species in Brazil. No reports of popular use, regarding its chemical composition or biological activities were reported to date. The study aimed to investigated the chemical composition of the essential oil of Zanthoxylum kleinii leaves and evaluate its antibacterial activity against Escherichia coli, Pseudomonas aeruginosa, Enterococcus faecalis and methicillin-sensitive Staphylococcus aureus. The essential oil was extracted from fresh leaves by hydrodistillation method, using a Clevenger apparatus, having a yield of 0.12% (v/m) volume of essential oil in relation to the amount of plant material. Quantitative analysis was performed by GC-MS and the results showed that the essential oil contains 30 compounds. The major compounds are monoterpene hydrocarbons, including β-phellandrene (37.80%), α-pinene (13.32%) and myrcene (10.05%). The essential oil showed no antibacterial activity against the strains tested (E. coli, P. aeruginosa, E. faecalis and S. aureus).

Keywords:
Zanthoxylum 1; Zanthoxylum kleinii 2; antibacterial 3; GC-MS 4; volatile oil 5

HIGHLIGHTS

Extraction of essential oil from leaves of Z. kleinii;

The volatile components of Z. kleinii were analyzed by GC-MS;

Antibacterial activity against Escherichia coli, Pseudomonas aeruginosa, Enterococcus faecalis and methicillin-sensitive Staphylococcus aureus.

GRAPHICAL ABSTRACT (OPTIONAL)

INTRODUCTION

Antimicrobial resistance is a challenge to public health. The antibiotics available on the market, the lack of new compounds, and the indiscriminate use of existing drugs lead to an increase in antibiotic resistance [¹; ²].

Escherichia coli is Gram-negative pathogen that produces Shiga toxins and is responsible for causing diseases such as hemolytic uremic syndrome, hemorrhagic colitis, and fatal thrombotic thrombocytopenic purpura. In addition, it can form biofilms on biotic and abiotic surfaces, such as stainless-steel sheets, polymers, glass, and plant tissues, if the appropriate conditions are given [¹; ³]. Pseudomonas aeruginosa is a Gram-negative bacillus, which is cosmopolitan and belongs to the normal microbiota of plants and animals, which is why it is considered opportunistic [⁴]. It is an organism capable of adapting to changes in the environment, rapidly developing resistance to antibiotics and producing a variety of virulence factors [⁵].

Staphylococcus aureus is prevalent in hospital environments, infections caused by this microorganism are difficult to cure due to the biofilm formed that increases the resistance of S. aureus to antibiotics [⁶; ⁷]. Enterococcus faecalis are Gram-positive pathogens, these microorganisms facilitate infective endocarditis [⁸].

Essential oils have aroused interest because they have broad biological activity. Some species of the Zanthoxylum genus exhibit insecticidal activity [⁹], antiasthmatic effect [¹⁰], antiparasitic against P. falciparum [¹¹], antiproliferative effect in human cancer cells [¹²], antinociceptive and anti-inflammatory [¹³], anti-influenza activities [¹⁴] antibacterial [¹⁵], and are commonly used to treat diseases such as inflammation, rheumatism, toothache, sickle cell anemia, malaria, febrifuge and genitourinary diseases [¹⁶].

The genus Zhantoxylum is one of the largest in the Rutaceae family, comprising around 200 species [¹⁷]. It is found on all continents, primarily in tropical and subtropical regions, excluding Antarctica. Twenty-seven species were identified in Brazil, all of which have oil glands distributed throughout the leaf blade [¹⁷].

The morphoanatomical study of the species was described for Zanthoxylum kleinii (R.S. Cowan) P.G. Waterman [¹⁸], however, there are no records in the literature about the tradicional use and biological activities for this species. With this in mind, the aim of this study was to extract, evaluate the composition and test the essential oil of Z. kleinii against strains of Escherichia coli, Pseudomonas aeruginosa, Enterococcus faecalis and methicillin-sensitive Staphylococcus aureus.

MATERIAL AND METHODS

Essential oil collection and extraction

We collected the aerial parts of the species Z. kleinii in March 2022 at the Federal University of Paraná (UFPR), at the following geographic coordinates 25°26'53.2"S 49°14'25.4"W, the tree was in the vegetative stage. The identification was carried out by Rodrigo Trompczynski Dall. The studied species is registered at the Curitiba School of Forestry Herbarium under register EFC-11981, and access to its genetic heritage is registered with the National System for the Management of Genetic Heritage and Associated Traditional Knowledge (SisGen) under register A0A1FD4.

Then, 328.1 g of fresh plant material from the total aerial parts (leaflet, rachis and petiole) was subjected to hydrodistillation using a Clevenger apparatus. The material was added to 3.5 L of distilled water and boiled for 6 hours. The resulting volatile oil was then stored in an airtight container in a freezer (-20 ºC) for subsequent analysis.

Gas chromatography analysis

A sample (1μL) of the essential oil was dissolved in dichloromethane (1 mL) and analyzed on a Shimadzu GCMS 2010Plus (Shimadzu Co, Kyoto, Japan) equipment, equipped with an AOC-5000 Plus automatic injector and fitted with an electron ionization source operating at 70 eV and a triple quadrupole mass spectrometer model TQ8040. The transfer line was at a temperature of 250°C, with an ion source at 250°C, with a mass range of 40 to 400 m/z, and 1250 scans. A DB-5 capillary column (Agilent Technologies, Santa Clara, California, USA) - non-polar stationary phase, 5% phenyl methylpolysiloxane, length 30 m, internal diameter 0.25 mm, film thickness 0.25 µm was installed. The injection temperature of the equipment was 250.00 °C, split injection mode, with a sample partition of 1/50, with helium (He) as the carrier gas (flow rate of 1.02 mL/min), and pressure of 59.0 kPa. The initial temperature of the oven was set at 60 °C, with a heating rate of 3 ºC/min, and final isotherm at 250 °C for 5 minutes.

The chemical composition of essential oils was determined by comparing the mass spectra obtained from the substances analyzed as well as by comparing their retention indices with those found in the literature, NIST library search [¹⁹; ²⁰]. The relative amounts of individual components were calculated based on the GC peak area (MS response). The similarity percentage included in Table 1 was equal to or above 90%. The constituents of essential oil were quantified using the GCMS Postrun Analysis software, the arithmetic index (AI) was obtained in the same software.

Antibacterial assay

We assessed the antibacterial activity by employing the broth microdilution method, in accordance with the Clinical and Laboratory Standards Institute (CLSI) [²¹]. We utilized the following strains for the test: Escherichia coli (ATCC 25922) (Gram-negative bacteria) and Pseudomonas aeruginosa (ATCC 27853) (Gram-negative bacteria), and Enterococcus faecalis (ATCC 29212) (Gram-positive bacteria) and methicillin-sensitive Staphylococcus aureus (MSSA, ATCC 6538) (Gram-positive bacteria). Initially the strains were stored in 20% glycerol in BHI broth (-80 ºC), and then reactivated in BHI broth and grown on Mueller-Hinton agar to obtain isolated colonies (35 ± 1 ºC).

The stock solution used in the test was prepared using volatile oil of Z. kleinii diluted in dimethylsulfoxide (DMSO) 1:1 (v/v). Dilutions for the MIC were made serially (0.19 -12.50 μL/mL) in Mueller-Hinton II Broth to a final volume of 100 μL. The bacterial inoculum was prepared in 0.85% saline solution obtained from an 18-hour plate culture adjusted to the 0.5 McFarland turbidity standard (~1.0 × 10⁸ CFU/mL). This suspension was then diluted at 1:20 (~5 × 10⁶ CFU/mL), out of which 10 μL was added to each well.

The negative control group was treated with 1% DMSO. Gentamicin was used for the positive control under the same conditions as the sample. The plates were incubated for an additional 18 hours at (35 ± 1 ºC) for further determination of the MIC.

RESULTS

Yield and chemical composition of Zanthoxylum kleinii essential oil

The essential oil was light yellow in color and had a citrus aroma. The yield of the essential oil of Z. kleinii was 0.12% (v/m) volume of essential oil in relation to the amount of plant material.

Thirty-one compounds were identified in the essential oil of Zanthoxylum kleinii, representing 63.83% of the essential oil's constituents, as shown in Figure 1 and Table 1, sixteen compounds were not identified, these are shown in figure 1. Of these, 46.6% were monoterpenes, 23.3% were sesquiterpenes, 20% were oxygenated monoterpenes and 10% were oxygenated sesquiterpenes. The main components belong to the monoterpene class: β-phellandrene (37.8%) and α-pinene (13.32%) and myrcene (10.05%).

Figure 1
Chromatogram with compounds identified in the essential oil obtained from the leaves of Z. kleinii

Table 1
Compounds identified in the essential oil obtained from the upper aerial parts of Z. kleinii

ID	RI	RI REFERENCE	COMPOUND NAME	RELATIVE AREA (%)	CLASSIFICATION
01	924	924	α-thujene (1)	0.51	monoterpene hydrocarbons
02	932	932	α-pinene (2)	13.32	monoterpene hydrocarbons
03	948	946	Camphene (3)	0.2	monoterpene hydrocarbons
04	970	969	Sabinene (4)	7.04	monoterpene hydrocarbons
05	977	974	β-pinene (5)	0.46	monoterpene hydrocarbons
06	987	988	Myrcene (6)	10.05	monoterpene hydrocarbons
07	1006	1002	α-phellandrene (7)	0.62	monoterpene hydrocarbons
08	1016	1014	α-terpinene (8)	1.26	monoterpene hydrocarbons
09	1027	1024	Limonene (9)	5.96	monoterpene hydrocarbons
10	1029	1025	β-phellandrene (10)	37.8	monoterpene hydrocarbons
11	1033	1032	(Z)-β-ocimene (11)	0.29	monoterpene hydrocarbons
12	1043	1044	(E)-β-ocimene (12)	2.91	monoterpene hydrocarbons
13	1055	1054	γ-terpinene (13)	1.93	monoterpene hydrocarbons
14	1084	1085	ρ-mentha-2,4(8)-diene (14)	0.97	monoterpene hydrocarbons
15	1099	1095	Linalol (15)	0.19	oxygenated monoterpene
16	1123	1118	cis-ρ-menth-2-en-1-ol (17)	0.33	oxygenated monoterpene
17	1140	1136	trans-ρ-menth-2-en-1-ol (18)	0.22	oxygenated monoterpene
18	1178	1174	Terpinen-4-ol (19)	2.88	oxygenated monoterpene
19	1193	1186	α-terpineol (20)	0.21	oxygenated monoterpene
20	1250	1249	Piperitone (22)	0.14	oxygenated monoterpene
21	1332	1335	δ-elemene (24)	0.61	sesquiterpene hydrocarbons
22	1415	1417	(E)-caryophyllene (27)	0.88	sesquiterpene hydrocarbons
23	1451	1452	α-humulene (29)	0.34	sesquiterpene hydrocarbons
24	1476	1480	Germacrene D (31)	4.25	sesquiterpene hydrocarbons
25	1490	1494	Bicyclogermacrene (33)	2.09	sesquiterpene hydrocarbons
26	1514	1511	δ-amorphene (38)	0.51	sesquiterpene hydrocarbons
27	1553	1559	Germacrene B (39)	0.28	sesquiterpene hydrocarbons
28	1558	1561	(E)-nerolidol (40)	0.32	oxygenated sesquiterpene
29	1637	1638	epi-α-cadinol (46)	0.49	oxygenated sesquiterpene
30	1650	1652	α-cadinol (47)	0.33	oxygenated sesquiterpene

• Legend: ID = compound number; RI = retention indices; RI REFERENCE = retention indices reported previously.
• Obs: the number in parentheses next to the name corresponds to the peak in the chromatogram.

DISCUSSION

The yield of the essential oil of Z. kleinii is similar to that described for the leaves of Zanthoxylum armatum var. subtrifoliolatum (Franch.) Kitam, which ranged from 0.088% to 0.176% [²²].

Studies carried out on other species of the genus have evidenced these substances in minor concentration. 𝛽-phellandrene was identified in the species Zanthoxylum armatum at a concentration of 2,2% in seeds essential oil [²³] and in fresh leaves of the species Zanthoxylum rhetsa DC. at a concentration of 2.5% [²⁴]. The constituent α-pinene was found in the volatile oil of Zanthoxylum bungeanum var. zimmermannii (Rehder & E.H. Wilson) C.C. Huang with a concentration of 0.19% [²⁵], in fresh leaves of Z. rhetsa with a concentration of 5.62% [²⁴], and in the volatile compounds obtained from the leaves of the species Zanthoxylum pistacifolium Griseb with a concentration of 12.35% [²⁶]. Myrcene was found in the essential oil of Z. rhetsa at a concentration of 2.0% [²⁴] and in the essential oil extracted from the leaves of the species Zanthoxylum pistacifolium at a concentration of 3.08% [²⁶].

Unlike other species, Z. kleinii presented β-phellandrene (37.8%) as the major constituent, other species of the genus presented other major compounds (Table 2).

Table 2
Major constituents identified in other species of the genus Zanthoxylum.

PLANT NAME	PARTS	COUNTRY REGION	MAJOR COMPOUNDS	REFERENCE
Zanthoxylum armatum	-	India	Linalol (75,7%)	[10]
Zanthoxylum ovalifolium var. spinifolium (Rehder & E.H. Wilson) C.C. Huang	leaves	India	β -pineno (72,3%)	[27]
Zanthoxylum bungeanum	leaves	China	Geranyl acetate (15,4%)	[28]
Zanthoxylum bungeanum	seed oi	China	Linalol (32,41%)	[29]
Zanthoxylum schinifolium fo. macrocarpum (Loes.) Rehder	-	China	Linalol (34,15%)	[30]
Zanthoxylum limonella Alston	fruits	Tailândia	Limoneno (34,59%)	[31]
Zanthoxylum armatum	fruits	Nepal	Linalol (58,31%)	[32]
Zanthoxylum myriacanthum var. pubescens (C.C. Huang) C.C. Huang	fruits	China	p-cimeno (30,58%)	[33]
Zanthoxylum acanthopodium var. villosum C.C. Huang	fruits	Indonésia	d-limonene (30,71%)	[34]
Zanthoxylum acanthopodium	fruits	China	Limonene (29,78%)	[35]
Zanthoxylum rhetsa	fresh leaves	Vietnã	Sabinene (38,35%)	[24]
Zanthoxylum nitidum var. tomentosum C.C. Huang	leaves	Vietnã	Limonene (44,3%)	[36]
Zanthoxylum schinifolium	fruits	Província de Sichuan	Linalol (28,2%)	[37]
Zanthoxylum alatum var. subtrifoliolatum Franch.	fresh leaves	Himalaia	Linalol (30,58%)	[38]
Zanthoxylum alatum	seeds	India	Linalol (71%)	[39]
Zanthoxylum bungeanum	fruits	Sichuan Province	Limonene (29,36%)	[40]
Zathoxylum acuminatum subsp. Tripetalum (Standl.) Reynel	leaf	Costa Rica	1,8-Cineole (30,9%)	[41]
Zanthoxylum melanostictum subsp. Chiriquinum (Standl.) Reynel	leaf	Costa Rica	trans-2-Hexenal (23,2%)	[41]
Zanthoxylum piperitum Franch.	aerial parts	Ireland	β-phellandrene (29.39%)	[42]
Zanthoxylum bungeanum	fruits	China	d -limonene (22,19%)	[43]

As can be seen in Table 2, linalool and limonene are the major compounds in the composition of the essential oil of different species of the genus Zanthoxylum.

Zanthoxylum piperitum presented β-phellandrene as the major constituent of the essential oil, it presented an antinociceptive effect [⁴²].

Antibacterial activity of the essential oil of the total aerial parts

The essential oil did not inhibit the gram-negative bacteria (E. coli and P. aeruginosa) or the gram-positive bacteria (E. faecalis and S. aureus) evaluated.

We found other studies that reported the absence of antibacterial activity with oils obtained from other species, corroborating the present research. Antibacterial activity has been verified in oils that have different major compounds to those found in this study. The volatile compound obtained from the leaves of the species Zanthoxylum rhoifolium var. surparanaense (Najera, Galdeano & Escal.) P.G. Waterman showed no inhibitory activity against E. coli [⁴⁴], and the essential oil from the leaves of Zanthoxylum avicennae var. touranense Pierre had no activity against S. aureus [⁴⁵].

The essential oil obtained from the leaves of Z. armatum showed moderately effective activity against gram-negative bacteria (E. coli) and inhibitory activity against S. aureus using 100 μL of oil [⁴⁴], like the species Z. bungeanum, it showed activity against E. coli and S. aureus at a concentration of 0.5% [²⁹]. One of the main components described for the essential oil of this species was bornyl acetate (16%) and cymene (8%) [²²]. The volatile oil from the bark of Z. armatum was active against E. coli and S. aureus, and its main constituent was α-pinene (approximately 30%). This oil was used at a concentration of 0.75 μL/mL [²³].

CONCLUSION

The essential oil showed no antibacterial activity against the tested strains. The difference in antibacterial activity observed between the species may be due to the major chemical constituents of each of them and the concentration of essential oil used to perform each test. The species searched in the literature presented linalool and limonene as major constituents. We recommend the conduction of follow-up studies, since other species of the genus were reported to have antinociceptive effect, antifungal and larvicidal potential.

Acknowledgements

We thank the Coordination for the Improvement of Higher Education Personnel (CAPES), the Federal University of Paraná (UFPR), the Postgraduate Programme in Pharmaceutical Sciences (PPG-CF), the Centre for Studies in Natural Products and Pharmacotechnics (NEPNF), and the Laboratory of Chemical Ecology and Synthesis of Natural Products (LECOSIN).

The authors would also like to thank the Academic Publishing Advisory Center (Centro de Assessoria de Publicação Acadêmica, CAPA - http://www.capa.ufpr.br) of the Federal University of Paraná (UFPR) for assistance with English language translation and developmental editing.

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• Funding:
  This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001

Edited by

• Editor-in-Chief:
  Paulo Vitor Farago

• Associate Editor:
  Jane Manfron Budel

Publication Dates

• Publication in this collection
  03 Feb 2025
• Date of issue
  2025

History

• Received
  07 Feb 2024
• Accepted
  09 Oct 2024