Antibacterial and Antifungal Sesquiterpenoids from Aerial Parts of Anvillea Garcinii

molecules Article Antibacterial and Antifungal Sesquiterpenoids from Aerial Parts of Anvillea garcinii Shagufta Perveen 1,*, Jawaher Alqahtani 1,2 , Raha Orfali 1, Hanan Y. Aati 1 , Areej M. Al-Taweel 1, Taghreed A. Ibrahim 1, Afsar Khan 3, Hasan S. Yusufoglu 4, Maged S. Abdel-Kader 4,5 and Orazio Taglialatela-Scafati 2,* 1 Department of Pharmacognosy, College of Pharmacy, King Saud University. P. O. Box 22452, Riyadh 11495, Saudi Arabia; [email protected] (J.A.); [email protected] (R.O.); [email protected] (H.Y.A.); [email protected] (A.M.A.-T.); [email protected] (T.A.I.) 2 Department of Pharmacy, School of Medicine and Surgery, University of Naples Federico II, Via D. Montesano 49, 80131 Naples, Italy 3 Department of Chemistry, COMSATS University Islamabad, Abbottabad Campus, Abbottabad-22060, Pakistan; [email protected] 4 Department of Pharmacognosy, College of Pharmacy, Prince Sattam Bin Abdulaziz University, P.O. Box 173, Al-Kharj 11942, Saudi Arabia; [email protected] (H.S.Y.); [email protected] (M.S.A.-K.) 5 Department of Pharmacognosy, Faculty of Pharmacy, Alexandria University, Alexandria 21215, Egypt * Correspondence: [email protected] (S.P.); [email protected] (O.T.-S.) Academic Editors: Pavel B. Drasar and Valeria Patricia Sülsen Received: 9 March 2020; Accepted: 7 April 2020; Published: 9 April 2020 Abstract: Two new sesquiterpenoids belonging to the guaiane, 4α,9α,10α-trihydroxyguaia- 11(13)en-12,6α-olide (1), and germacrane, 9β-hydroxyparthenolide-9-O-β-D-glucopyranoside (2), classes have been isolated from the leaves of the Saudi medicinal plant Anvillea garcinii along with seven known compounds (3–9). The structures of the new metabolites were elucidated by spectroscopic analysis, including one-dimensional (1D) and two-dimensional (2D) Nuclear Magnetic Resonance (NMR) and high-resolution electrospray ionization mass spectrometry (HR-ESIMS). The antimicrobial properties of 1–9 were screened against seven different pathogenic microbes, and compounds 1–3 showed a potent antifungal activity. Keywords: Anvillea garcinii; Saudi medicinal plants; sesquiterpene lactones; antifungal activity 1. Introduction Traditional medicines are a powerful weapon for mankind and they have been used to treat several health disorders since ancient times. The last few decades have witnessed a renaissance in the use of natural products, and traditional medicine in general, to prevent or cure several ailments. While they are considered one of the possible options in several countries, they are practically the main therapeutic option in many developing countries, including those of the Arabian Peninsula. Flora of Saudi Arabia is evidently and understandably not as rich and diverse as that of countries of the Mediterranean basin; however, it has a vital role for various ecosystems, especially in maintaining the environmental balance and stability [1]. The dominating plant family is Asteraceae, one of the largest plant families on the planet, which is a family that includes more than one thousand genera and twenty thousand species [2]. Asteraceae plants are well known for their biological and pharmacological effects, largely ascribable to the presence of phytochemicals belonging to polyphenol, flavonoid, and terpenoid classes [3]. Anvillea is probably the smallest genus of the Asteraceae family, since it includes only four species, distributed in a large area spanning from North Africa to Iran, including several Middle Eastern Molecules 2020, 25, 1730; doi:10.3390/molecules25071730 www.mdpi.com/journal/molecules Molecules 2020, 25, 1730 2 of 10 countries,Molecules 2020 such, 25 as, x Egypt,FOR PEER Palestine, REVIEW and Saudi Arabia [4]. In Saudi Arabia, Anvillea genus is represented2 of 10 by the following two species: A. garcinii and A. radiata. A. garcinii DC (Arabic name Nuqd) is one Eastern countries, such as Egypt, Palestine, and Saudi Arabia [4]. In Saudi Arabia, Anvillea genus is of the most important ethnomedicinal plants used in the Arabian Peninsula region, indicated for represented by the following two species: A. garcinii and A. radiata. A. garcinii DC (Arabic name symptomatic relief of various illnesses such as cold, gastrointestinal disorders, and respiratory system Nuqd) is one of the most important ethnomedicinal plants used in the Arabian Peninsula region, problemsindicated [3 ].for Traditionally, symptomatic the relief dried of plant various is crushed, illnesses mixed such withas cold, honey gastrointestinal or date and olive disorders, oil, and and used torespiratory treat cold symptoms system problems [4]. [3]. Traditionally, the dried plant is crushed, mixed with honey or date andFlavonoids olive oil, and and used sesquiterpene to treat cold lactones symptoms have [4]. been the predominant class of secondary metabolites obtainedFlavonoids by phytochemical and sesquiterpene studies on lactonesA. garcinii have[5– 11been]. Our the previous predominant investigations class of onsecondary this plant disclosedmetabolites the obtained presence by of phytochemical sesquiterpene studies lactones on A. of garcinii the guaianolide- [5–11]. Our previous and germacranolide-types, investigations on includingthis plant the disclosed corresponding the presence amino of sesquiterpen acid adducts,e lactones as well of as the some guaian flavonoidsolide- and glycosidesgermacranolide- [11–13]. Thetypes, class including of Anvillea the correspondingsesquiterpene amino lactones acid is adducts, dominated as well by as derivatives some flavonoids with theglycosides parthenolide [11– skeleton,13]. The germacranolides class of Anvillea sesquiterpene endowed with lactones significant is dominated biological by activities derivatives in cancer with the and parthenolide inflammation, asskeleton, well as ingermacranolides metabolic disorders endowed [14 with]. Previous significant examination biological activities of the aerial in cancer parts and of inflammation,A. garcinii have affasorded well severalas in metabolic members disorders of the parthenolide [14]. Previous class, examination such as of 9α the- and aerial 9β-hydroxyparthenolide, parts of A. garcinii have 9 α- andafforded 9β-hydroxy-1 several βmembers,10α-epoxyparthenolide, of the parthenolide parthenolid-9-one, class, such as 9α- andand its9β-hydroxyparthenolide,cis-isomer [15]. In addition, 9α- guaianolide-typeand 9β-hydroxy-1 sesquiterpenoids,β,10α-epoxyparthenolide, a class part of phytochemicalshenolid-9-one, and with its cis- a broadisomer range[15]. In of addition, activities, includingguaianolide-type cytotoxic, sesquiterpenoids, antiprotozoal, and a class anti-inflammatory of phytochemicals potential with [16a ],broad also constituterange of activities, prominent A.including garcinii metabolites. cytotoxic, antiprotozoal, Leucodin and and zaluzanin anti-infla Cmmatory and their potential derivatives [16], also [17], constitute as well as prominent garcinamine A. E garcinii metabolites. Leucodin and zaluzanin C and their derivatives [17], as well as garcinamine E and other guaianes [13], have been isolated from this species. and other guaianes [13], have been isolated from this species. This richness of bioactive secondary metabolites prompted us to continue our phytochemical This richness of bioactive secondary metabolites prompted us to continue our phytochemical and biological investigation of A. garcinii, with the final aim of obtaining a detailed picture of the and biological investigation of A. garcinii, with the final aim of obtaining a detailed picture of the metabolome of this plant, providing solid scientific grounds for its use in traditional medicines and metabolome of this plant, providing solid scientific grounds for its use in traditional medicines and possibly,possibly, to to develop develop a a new new phytotherapeutic phytotherapeutic drugdrug fromfrom this natural natural source. source. In In this this manuscript manuscript we we α α α reportreport the the isolation isolation of two of new two sesquiterpenoids new sesquiterpenoids belonging belonging to the guaiane to (4the ,9guaiane,10 -trihydroxyguaia- (4α,9α,10α- 11(13)en-12,6trihydroxyguaia-11(13)en-12,6α-olide, (1)) and germacranolideα-olide, (1)) and (9 germacranolideβ-hydroxyparthenolide-9- (9β-hydroxyparthenolide-9-O-β-D-glucopyranoside,O-β-D- (2))glucopyranoside, classes, along with(2)) classes, seven along known with compounds seven known (3– compounds9) (Figure1) (3 and–9) (Figure the results 1) and of the screening results of for antimicrobialscreening for activity antimicrobial on the activity isolated on metabolites. the isolated metabolites. HO OH HO O 14 1' OH 14 OH H OH OH O 10 1 1 9 HO 4 5 6 H 11 4 6 11 H 15 OH 13 OH O 13 O 12 O 15 O 12 O O O 3 1 2 HOOC OH OH OH O O HO HO O O OH OR OH O HO OH OR 4 R = H 6 R = H 7 R = CH 5 R = CH3 3 OH R1O O 8 β OR R = -D-glucose R1 = H β 9 R = H R1 = -D-glucose OH O FigureFigure 1. 1.Chemical Chemical structuresstructures of metabolites isolated isolated from from AnvilleaAnvillea garcinia. garcinia . Molecules 2020, 25, 1730 3 of 10 Molecules 2020, 25, x FOR PEER REVIEW 3 of 10 2.2. Results and Discussion PreviousPrevious investigationsinvestigations onon A.A. garciniigarcinii aerialaerial partsparts selectedselected thethe nn-butanol-butanol fractionfraction ofof thethe methanolmethanol extractextract asas the richest in polar sesquiterpenoids. It Itss chromatographic chromatographic separation separation was was achieved achieved using using a acombination combination of Sephadex of Sephadex LH-20, LH-20, silica silica gel, and

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