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Antimicrobial Activity of Extracts of Two Native Fruits of Chile: Arrayan (Luma Apiculata) and Peumo (Cryptocarya Alba)

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Antimicrobial Activity of Extracts of Two Native Fruits of Chile: Arrayan (Luma Apiculata) and Peumo (Cryptocarya Alba) antibiotics Article Antimicrobial Activity of Extracts of Two Native Fruits of Chile: Arrayan (Luma apiculata) and Peumo (Cryptocarya alba) Jitka Viktorová 1, Rohitesh Kumar 1, Kateˇrina Rehoˇrovˇ á 1, Lan Hoang 1 , Tomas Ruml 1 , Carlos R. Figueroa 2 , Monika Valdenegro 3 and Lida Fuentes 4,* 1 Department of Biochemistry and Microbiology, University of Chemistry and Technology Prague, 166 28 Prague, Czech Republic; [email protected] (J.V.); [email protected] (R.K.); [email protected] (K.R.);ˇ [email protected] (L.H.); [email protected] (T.R.) 2 Institute of Biological Sciences, Campus Talca, Universidad de Talca, Talca 3465548, Chile; cfi[email protected] 3 Agronomy School, Faculty of Agronomic and Food Sciences, Pontificia Universidad Católica de Valparaíso, Quillota 2260000, Chile; [email protected] 4 Regional Center for Studies in Healthy Food (CREAS), CONICYT-Regional GORE Valparaíso Project R17A10001, Avenida Universidad, Valparaíso 2340000, Chile * Correspondence: [email protected] Received: 22 June 2020; Accepted: 21 July 2020; Published: 25 July 2020 Abstract: Arrayan and peumo fruits are commonly used in the traditional medicine of Chile. In this study, the concentration of the extracts halving the bacterial viability and biofilms formation and disruption of the drug-sensitive and drug-resistant strains of Staphylococcus aureus and Pseudomonas aeruginosa was determined. The chemical composition of extracts was analyzed by high-resolution liquid chromatography coupled with mass spectrometry (U-HPLC/MS). The arrayan extract (Inhibitory concentration IC 0.35 0.01 mg/mL) was more effective than peumo extract (IC 0.53 0.02 mg/mL) 50 ± 50 ± in the inhibition of S. aureus planktonic cells. Similarly, the arrayan extract was more effective in inhibiting the adhesion (S. aureus IC 0.23 0.02 mg/mL, P. aeruginosa IC 0.29 0.02 mg/mL) than 50 ± 50 ± peumo extracts (S. aureus IC 0.47 0.03 mg/mL, P. aeruginosa IC 0.35 0.01 mg/mL). Both extracts 50 ± 50 ± inhibited quorum sensing in a concentration-dependent manner, and the most significant was the autoinducer-2 type communication inhibition by arrayan extract. Both extracts also disrupted preformed biofilm of P. aeruginosa (arrayan IC 0.56 0.04 mg/mL, peumo IC 0.59 0.04 mg/mL). 50 ± 50 ± However, neither arrayan nor peumo extracts disrupted S. aureus mature biofilm. U-HPLC/MS showed that both fruit extracts mainly possessed quercetin compounds; the peumo fruit extract also contained phenolic acids and phenylpropanoids. Our results suggested that both extracts could be used as natural antimicrobials for some skin and nosocomial infections. Keywords: traditional medicine; drug-resistant bacteria; high-resolution HPLC/MS; biofilm disruption; quorum sensing 1. Introduction As part of the diets, many fruits of native species have been used as a traditional medicine in the South American region [1,2]. The Chilean trees, arrayan [Luma apiculata (DC.) Burret] and peumo [Cryptocarya alba (Molina) Looser], are ancestral species used in food and medicinal preparations [3,4]; however, the antimicrobial properties of both species are have not yet been described in detail. Arrayan (Luma apiculata) is a Myrtaceae [5] endemic plant from the Valparaiso to Aysen regions of Chile (latitude 33◦ to 45◦ S). It grows in the temperate forests of Chile and Argentina. Its fruit is an edible black or purple berry (Figure1A), with an intense flavor, aromatic, and a pleasant sweet Antibiotics 2020, 9, 444; doi:10.3390/antibiotics9080444 www.mdpi.com/journal/antibiotics Antibiotics 20202020, 9, x 444 2 of 13 14 edible black or purple berry (Figure 1A), with an intense flavor, aromatic, and a pleasant sweet taste. Lumataste. speciesLuma species (namely (namely L. apiculataL. apiculata and L. chequenand L.) chequenhave been) have previously been previously described described as a rich source as a rich of phenolicsource of compounds phenolic compounds with high antioxidant with high antioxidant activity [4]. activity Extracts [ 4of]. ripe Extracts fruits of of ripe arrayan fruits showed of arrayan the presenceshowed the of presenceflavonol of and flavonol anthocyanins, and anthocyanins, with high with highoxygen oxygen radical radical absorption absorption capacity capacity and concentrationconcentration-dependent-dependent vascular protectio protectionn under high glucose conditions [6] [6].. Moreover, Moreover, aqueous extracts demonstrated inhibition of the the collagen collagen-induced-induced aggregation aggregation of platelets platelets in in human human blood blood [7] [7],, indicatingindicating thethe potencypotency toto treat treat wounds wounds and and inflammations. inflammations. Further, Further, the the addition addition of dryof dry leaves leaves into into the thelettuce lettuce substratum substratum resulted resulted in betterin better control control of Meloidogyneof Meloidogyne hapla haplapopulation, population, nematode nematode known known as as a avegetable vegetable pathogen, pathogen, which which produces produces tiny tiny galls galls [ 8[8].]. ArrayanArrayan hashas alsoalso shownshown activityactivity against Herpes simplex virus type 2 [9] [9].. Figure 1. Branches with leaves and fruits of arrayan and peumo. ( (AA)) Arrayan [ [Luma apiculata (DC.)(DC.) Burret.Burret.]] *; (B) PeumoPeumo [[CryptocaryaCryptocarya albaalba(Molina) (Molina) Looser] Looser] **. ** Photography. Photography credit credit to to Carlos Carlos R. R. Figueroa Figueroa (*) (*)and and Lida Lida Fuentes Fuentes (**). (**). PPeumoeumo belongs belongs to to the the Lauraceae Lauraceae family family and and is isspread spread from from the the Maule Maule to toAraucania Araucania regions regions of Chileof Chile (latitude (latitude 35 35to ◦38toS) 38. The◦ S). ripe The fruit ripe is fruit a red is to a smooth red to smooth pink berry pink (Figure berry 1B (Figure), crowned1B), crowned with the remainswith the of remains the stamens of the and stamens calyx andlobes calyx. It has lobes. a large It hasseed a simil largear seedto a similarnut. Its toleaves a nut. and Its bark leaves are usedand barkin traditional are used inmedicine traditional to treat medicine liver diseases to treat liver and diseasesrheumatism and [10]. rheumatism The essential [10]. Theoil prepared essential byoil the prepared distillation by the of distillationpeumo showed of peumo activity showed against activityNosema againstceranae, Nosemathe originator ceranae of, the nosemosis originator in honeybeeof nosemosis [11]; in against honeybee insect [11 Sitophilus]; against zeamais insect Sitophilus Motschulsky zeamais, knownMotschulsky, as a maize known weevil, as acausing maize significantweevil, causing loses during significant cereals loses’ storage during [12] cereals’; and against storage Musca [12]; domestica and against L. [13]Musca. Moreover, domestica the L.leaves [13]. extractMoreover, demonstrated the leaves extract a protective demonstrated effect against a protective ethyl e ffmethaneect against sulph ethylonate methane-induced sulphonate-induced mutagenesis in Drosophilamutagenesis melanogaster in Drosophila [14] melanogaster. The edible[14 peumo]. The skin edible has peumo a large skin number has a largeof polyphenol number ofic polyphenolic compounds [15]compounds, related [to15 high], related antioxidant to high capacity antioxidant [15,16] capacity. Besides [15 ,the16]. other Besides biologically the other active biologically compounds, active cryptofolionecompounds, cryptofolione and its dihydro and its-derivative dihydro-derivative were isolated were isolatedfrom the from fruits the fruits of C. of C.alba alba [17][17. ].In In the the trypanocidal assay,assay, cryptofolione cryptofolione at at 250 250µg µg/mL/mL reduced reduced the the number number of trypomastigotes of trypomastigotes by 77%, by while77%, whileits dihydro-derivative its dihydro-derivative was inactive. was inactive However,. However, cryptofolione cryptofolione at tenfold at tenfold lower concentration lower concentration (25 µg/mL) (25 µg/mL)reduced reduced the viability the viability of macrophages, of macrophages demonstrating, demonstrating a cytotoxic a cytotoxic effect instead effect ofinstead selectivity of selectivity towards Trypanosomatowards Trypanosoma cruzi [17]. cruzi [17]. The antimicrobial activity of fruit extracts extracts,, including the native fruit fruitss of Chile, has usually be beenen related to total phenolic content and compounds compounds such as as chlorogenic chlorogenic acid, quercetin, quercetin, ellagic acid, and quercetinquercetin-3-galactoside-3-galactoside [18 [18–21]21].. T Thehe hydroxyl hydroxyl groups of polyphenolic compounds play a significant significant role in inhibit inhibitinging the key enzymatic activities of bacteria and inducing cell toxicity [[22]22].. TThishis study aimed to characterize the antimicrobial activity and the phytochemical profile profile of fruitfruit-extracts-extracts and seek potential uses of arrayan and peumo species in the medicinal treatment.treatment. 2. Results 2.1. Inhibition of Multidrug-Resistant Bacterial Strains Antibiotics 2020, 9, 444 3 of 14 2. Results 2.1. Inhibition of Multidrug-Resistant Bacterial Strains As drug-resistant strains, we used clinical isolates obtained from the Collection of the Laboratory of Medical Microbiology (Czech Laboratory, lnc., NEM) resistant to several drugs. Overall, arrayan extract was effective in inhibiting both the drug-resistant and drug-sensitive strains of S. aureus, with almost the same IC50 values (Table1). However, the
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  • Introduction
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