molecules Article Chemical Composition, Antimicrobial and Antiparasitic Screening of the Essential Oil from Phania matricarioides (Spreng.) Griseb. Yamilet I. Gutiérrez 1, Ramón Scull 1, Anabel Villa 2, Prabodh Satyal 3, Paul Cos 4,5, Lianet Monzote 5,6,* and William N. Setzer 3,5,7,* 1 Department of Pharmacy, Institute of Pharmacy and Food, Havana University, Coronela, Lisa, Havana 13600, Cuba; [email protected] (Y.I.G.); [email protected] (R.S.) 2 Genetic toxicology and antitumor laboratory, Drug Research and Development Center (CIDEM), Havana 10600, Cuba; [email protected] 3 Aromatic Plant Research Center, 230 N 1200 E, Suite 100, Lehi, UT 84043, USA; [email protected] 4 Laboratory for Microbiology, Parasitology and Hygiene (LMPH), Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, 2610 Wilrijk, Belgium; [email protected] 5 Research Network Natural Products against Neglected Diseases (ResNet NPND) 6 Parasitology Department, Center of Research, Diagnostic and Reference, Institute of Tropical Medicine “Pedro Kouri”, Havana 10400, Cuba 7 Department of Chemistry, University of Alabama in Huntsville, Huntsville, AL 35899, USA * Correspondence: [email protected] (L.M.); [email protected] or [email protected] (W.N.S.); Tel./Fax: +53-7-255-3612 (L.M.); +1-256-824-6519 (W.N.S.) Academic Editors: Valeria Patricia Sülsen and Albertina Moglioni Received: 3 April 2019; Accepted: 22 April 2019; Published: 24 April 2019 Abstract: Essential oils (EOs) have gained increasing attention due to their pharmacological effectiveness, and they also constitute some of the most popular natural products. In this study, we present the chemical characterization of the EO from Phania matricarioides and the in vitro activity/selectivity against a wide panel of bacteria, fungi and parasitic protozoa. Forty-five compounds were identified in the studied EO, of which lavandulyl acetate (40.1%) and thymyl isobutyrate (13.9%) were the major components. The EO did not inhibit bacterial or fungal growth at the maximum concentration tested (64 µg/mL), although it displayed activity on all evaluated protozoa (IC50 values ranging from 2.2 to 56.6 µg/mL). In parallel, the EO demonstrated a noteworthy cytotoxic activity against peritoneal macrophages (CC50 values of 28.0 µg/mL). The most sensitive microorganism was Trypanosoma cruzi, which had a superior activity (IC50 = 2.2 µg/mL) and selectivity (SI = 13) in respect to other parasitic protozoa and the reference drug (p < 0.05). Further in vivo studies are needed to evaluate the potential use of this EO and the main compounds as antitrypanosomal agents. To our knowledge, this is the first report of chemical characterization and antimicrobial assessment of the EO from P. matricarioides. Keywords: Phania matricarioides; essential oil; antimicrobial screening; cytotoxicity; Trypanosoma cruzi 1. Introduction Indiscriminate and irrational use of antimicrobial agents has created an unprecedented challenge for human civilization due to the microbes’ development of antimicrobial resistance. Complementary and alternative medicines (CAMs) are used by 60–80% of developing countries, as they are one of the most prevalent sources of medicine worldwide. In recent years, research on plant-based drugs has increased tremendously, and there is some hope seen in certain medicinal plants that have immense potential to combat bacterial, fungal, protozoal and viral diseases with Molecules 2019, 24, 1615; doi:10.3390/molecules24081615 www.mdpi.com/journal/molecules Molecules 2019, 24, x FOR PEER REVIEW 2 of 11 plant-based drugs has increased tremendously, and there is some hope seen in certain medicinal Moleculesplants that2019 ,have24, 1615 immense potential to combat bacterial, fungal, protozoal and viral diseases 2with of 11 safety. Such plant metabolites include quinones, alkaloids, lectins, polypeptides, flavones, flavonoids, flavonols, coumarins, terpenoids, phenylpropanoids and tannins [1,2]. In particular, safety.other plant Such-derived plant metabolites natural products, include quinones,such as essential alkaloids, oils lectins, (EOs) polypeptides,, have experienced flavones, an upsurge flavonoids, in flavonols,attention due coumarins, to their terpenoids, efficacious phenylpropanoids bioactivities [3], andand tannins represent [1,2 ].one In particular,of the most other popular plant-derived natural naturalproduct products,classes due such to astheir essential applications oils (EOs), in dermatology, have experienced cosmetics an upsurge and aromatherapy in attention due [4] to. There their ehavefficacious been bioactivitiesnumerous [publications3], and represent regarding one of thethe most utility popular of EOs natural as productantimicrobial, classes dueanticancer, to their applicationsanti-inflammatory in dermatology, and antiviral cosmetics agents. and In aromatherapy recent years, [4numerous]. There have papers been reporting numerous antimicrobial publications regardingproperties theof EOs utility extracted of EOs asfrom antimicrobial, higher plants anticancer, have been anti-inflammatory published, including and antiviral antibacterial, agents. Inantifungal recent years, and antiparasitic numerous papers activities reporting [5]. antimicrobial properties of EOs extracted from higher plantsRecently, have been we published, have focused including on Phania antibacterial, matricarioides antifungal (Spreng.) and Griseb. antiparasitic (Figure activities 1) (Asteraceae [5]. or CompositaeRecently, family), we have which focused has been on Phania traditionally matricarioides used for(Spreng.) digestive Griseb. conditions (Figure (stomach1) (Asteraceae pain, bad ordigestion Compositae and diarrhea) family), and which dermatological has been traditionally lesions [6,7] used. P. matricarioides for digestive is conditions included (stomachin a very large pain, badand digestionwidespread and family diarrhea) of flowering and dermatological plants that lesions grow [ 6for,7]. ornamentalP. matricarioides purposesis included [8], but in a the very family large andalso widespreadrepresents a familycertain of economic flowering importance plants that due grow to forthe ornamental provision of purposes products [8 such], but as the cooking family oils, also representslettuce, sunflower a certain seeds, economic artichokes, importance sweetenin due to theg agents, provision coffee of products substitutes such and as cooking herbal oils,teas lettuce,[9]. In sunfloweraddition, many seeds, species artichokes, possess sweetening medicinal agents, properties, coffee including substitutes antioxidant and herbal [10] teas, antiparasitic [9]. In addition, [11], manyanticancer species [12] possess and medicinal hepatoprotective properties, including[13]. In antioxidant particular, [10 ], antiparasiticthe antidiarrheal, [11], anticancer analgesic, [12] andanti- hepatoprotectiveinflammatory and [13 anti]. In-oxidant particular, effects the antidiarrheal, of extracts have analgesic, been demonstrated anti-inflammatory and andcorrelated anti-oxidant with esomeffects active of extracts common have phytochemicals been demonstrated such and ascorrelated phenolic withcompounds, some active tannins, common flavonoids, phytochemicals lactonic suchcompounds, as phenolic triterpenes compounds, or steroids, tannins, terpenes flavonoids, and organic lactonic acids compounds, [6,14,15]. Howeve triterpenesr, as or far steroids, as we terpenesknow, the and EO organic from acidsP. matricarioides [6,14,15]. However, has not as been far as chemically we know, the characterized EO from P. matricarioides, and its biologicalhas not beenproperties chemically have not characterized, been scientifically and its biologicaldemonstrated. properties have not been scientifically demonstrated. In this study, takingtaking intointo accountaccount thethe antimicrobialantimicrobial potential of EOs,EOs, we have chemically characterizedcharacterized of the EO from P. matricarioidesmatricarioides and screenedscreened forfor potentialpotential activityactivity/selectivity/selectivity against bacteria, fungi and parasitic protozoa of medicalmedical relevance.relevance. Figure 1. Phania matricarioidesmatricarioidesin in a a natural natural habitat. habitat. Picture Picture taken taken by by the the authors authors during during collection collection of the of plantthe plant (March (March 2013, 2013, Bauta Bauta municipality, municipality, Artemisa, Artemisa, Cuba). Cuba). 2. Results The obtained volatile oil from P. matricarioides was colorless and aromatic, and yielded 0.1 0.002%. The obtained volatile oil from P. matricarioides was colorless and aromatic, and yielded± 0.1 ± The0.002%. results The of theresults gas chromatography–massof the gas chromatography spectrometry–mass (GCspectrome/MS) aretry summarized (GC/MS) are in Table summarized1, and show in thatTable the 1, chemicaland show composition that the chemical of the EOcomposition was made of up the of EO 48 compounds, was made up of of which 48 compounds, 45 components of which were identified,45 components representing were identified, 98.9% of therepresenting total oil. The98.9% predominant of the total components oil. The predominant were lavandulyl components acetate (40.1%),were lavandulyl followed acetate by thymyl (40.1%) isobutyrate, followed (13.9%) by thymyl (Table isobutyrate1 and Figure (13.9%)2). (Table 1 and Figure 2). The EOEO diddid not not exhibit exhibit bacterial bacterial or fungalor fungal growth growth inhibition inhibition at the at maximum