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Scientific Papers. Series B, Horticulture. Vol. LXII, 2018 Print ISSN 2285-5653, CD-ROM ISSN 2285-5661, Online ISSN 2286-1580, ISSN-L 2285-5653

ANTIMICROBIAL POTENTIAL OF ROMANIAN SPONTANEOUS FLORA - A MINIREVIEW

Tomina PURCARU, Camelia DIGUŢĂ, Florentina MATEI

University of Agronomic Sciences and Veterinary Medicine of Bucharest, Faculty of Biotechnologies, 59 Mărăşti Blvd, District 1, Bucharest,

Corresponding author email: [email protected]

Abstract

In the past decades, clinical microbiologists, practitioners and professionals in food safety, are facing new challenges related to new born microbial pathogens as well as to the phenomenon of the antibiotic and biocide resistance developed by the pathogens. Meanwhile, in Romania has been noticed an increase in scientific publications dealing with the potential of Romanian aromatic and medicinal and their therapeutic use. The paper proposes a mini- review on scientifically proved antimicrobial activity of aerial and underground parts of some spontaneous from Romanian flora. The review approaches annual and perennial plants, from herbaceous to bushes and . In our search we have identified a total of 64 species from autochthonous flora involved in studies on antimicrobial activity, belonging to 21 botanical families. Among these species, 28.1% are annual plants, 46.9% are herbaceous perennial plants and the rest (25%) are woody perennial species (bushes and trees). Almost 50% of the active species belongs to and botanical families. For 89% of the species have been reported antibacterial activity, while only 57.8% of the species have proven antifungal activity.

Key words: Romanian spontaneous flora, antibacterial, antifungal, phytopharmaceutical use.

INTRODUCTION different mechanisms, more or less elucidated, the microorganisms became over and over In the past decades, clinical microbiologists, resistance to the new antibiotics and biocids. practitioners and professionals in food safety, Meanwhile, with the growing consumer are facing new challenges related to new born demand for natural preservatives to replace microbial pathogens as well as to the chemical compounds, plant antimicrobial phenomenon of the antibiotic and biocide compounds must be thoroughly investigated for resistance developed by the pathogens, of their potential to serve as natural preservatives which the most studied is methicillin-resistant (Hintz et al, 2015); on this side, very recently, Staphyloccous aureus MRSA (Lee et al., 2015). an exhaustive overview on natural food The antibiotic resistance crisis has been preservatives with antimicrobial properties has attributed to the overuse and misuse of the been reported by Pisoschi et al. (2018).In this medications, as well as the lack of new drug context, the “return to the origins”, meaning the development by the pharmaceutical industry use of the spontaneous flora as antimicrobial due to reduced economic incentives and tool may be a solution of the antibiotic “crisis” challenging regulatory requirements (Ventola, and the replacement of chemical preservatives. 2015). In ancient times, microbial infections A lot of studies have been published in the past were treated empirically, by the use of different two decades and it has been proven that natural solutions, including the use of different spontaneous flora of each continent, plants prepared under different formulations. hemisphere, country or region has an immense Starting with the discovery of penicillin by Sir potential in obtaining different products with Alexander Fleming in 1928, antibiotics have antimicrobial and anti-inflammatory impact. transformed modern medicine. Over the past The repository of the whole information is decades, starting with 1950, it has been proven quite difficult because of the huge volume of that bacteria have developed resistance to data, but there are some reports related to different antibiotics; as a consequence, new different countries or regions. For example, in synthesis substances have been developed to Balkan regions (Southeast ), where treat the infections (Ventola, 2015); because of Romania belongs, an ethnobotanical analysis 667 showed that 128 plant species (105 wild, 22 proposes to present an overview of Romanian cultivated and 1 wild/cultivated) are used in the spontaneous flora proved by experimental treatment of wounds. Their application is approach to have antimicrobial effect. external, in the form of infusions, decoctions, tinctures, syrups, oils, ointments, and balms, or MATERIALS AND METHODS direct to the skin. Among those plants recorded, the most commonly used in are Online information research was conducted by Plantago major, Hypericum perforatum, the use of different database collections and on- Plantago lanceolata, Achillea millefolium, searching engines (Google Academic, Web of , nigra, Knowledge, PubMed, ScienceDirect and Tussilago farfara and Prunus domestica (Jaric Embase, InTech and Hindawi databases). The et al., 2018). As in all the other countries or information has been structured in relation to regions, on the ancient lands of the actual the plants type (annual/biennial and perennial Romania, it was a vivant interest in the use of plants, from herbaceous species to bushes and different plants to treat human, animal or even trees).Where information was available, the plants’ infections. Jaric et al. (2018) make district or the county of the plant origin have references to different studies and report that in been specified. Romania, out of more than 3600 species of plants, over 700 are medicinal plants. RESULTS AND DISCUSSIONS Nowadays the interest has been resuscitated and more complex studies have been performed The database screening has led to a collection related to the chemical composition of the of over sixty scientific publications, dated from popular plants, as well as on testing their 2007 to 2018. The authors have reported the antimicrobial effect by the use of a use of different types of extracts (aqueous, standardized methodological approach. On our alcoholic or PEG extracts), as well as the use knowledge, there is no comprehensive review essential oils of different plants in testing the on the published studies developed on antimicrobial activity. Different methods have Romanian level in relation to our local flora been used to test the antimicrobial activity of and its antimicrobial properties. However, different plants products. The most usual Amarioarei et al. (2016) has published a method is the agar diffusion method described scientometric analysis performed on data by different authors or clinical standards in collected from Scopus, during 2000-2015; the USA or Europe (Brown, 1978; Das et al., review contains information on number of 2010). The findings are described in the papers, citations, affiliation and number of following, grouped in annual or perennial authors dealing with the potential of Romanian plants, herbaceous or woody groups. aromatic and medicinal plants and their therapeutic use. The authors have reported an 1) Annual / Biennial plants increasing trend for such publications in The reported antimicrobial activity of Romania starting with 2007 which we could annual/biennial plants from Romanian flora are rely with the variety of funding available synthetized in Table 1 and their appurtenance through the national and regional funding to botanical is clearly specified. programs. Also, there is some information There are different studies targeting the provided from some Romanian geographical botanical family Lamiaceae, which includes regions on plants having different most of the aromatic plants like phytopharmaceutical effects; for example, in vulgare L., officinalis L. or Banat region were identified about 140 plant L.; ethanolic extracts of aerial parts species with antioxidant potential (Antal, of these plants have been proven to have some 2010). Generally, antioxidant activity is due to antibacterial activity on Listeria polyphenol content, especially flavonoids monocytogenes, Stahpylococcus aureus compounds, and it is assumed that same (Benedec et al., 2015), as well as antifungal compounds are partially responsible for the activity on Candida albicans (Tuchila et al., antimicrobial activity. The present paper 2008; Benedec et al., 2015).

668

Table 1. Romanian annual herbaceous plants with antimicrobial activity

Plant species Botanical Plant part Antimicrobial activity Reference family Bacteria Fungi Origanum vulgare L. Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Stahpylococcus aureus Dobre et al., 2011 E. coli Sandru et al., 2015 Salmonella enteridis Melissa officinalis L. Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Stahpylococcus aureus Hancianu et al., 2008 Ocimum basilicum L. Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Staphylococcus aureus Stefan et al., 2011 E. coli Tuchila et al., 2008 Streptococcus cricetus Vlase et al., 2014 vulgaris L. Lamiaceae hb; fl; fs Staphylococcus aureus Candida albicans Boruga et al., 2014. Klebsiella pneumoniae Aspergillus niger Dobre et al., 2011 Salmonella typhimurium Grigore Armatu et al., E. coli 2012 Enterococcus faecalis Varga et al., 2015 Salmonella enteridis Pseudomonas aeruginosa Listeria innocua Streptococcus pyogenes hb E. coli Candida albicans Pavel et al., 2010 Enterobacter cloacae Varga et al., 2015 Proteus mirabilis Bacillus subtilis Micrococcus flavus Lamiaceae Staphylococcus aureus Streptococcus faecalis Pseudomonas aeruginosa Listeria innocua Streptococcus pyogenes Thymus glabrescens Lamiaceae hb Salmonella typhimurium Candida albicans Pavel et al., 2010 Pseudomonas aeruginosa Varga et al., 2015 Proteus mirabilis Listeria innocua Streptococcus pyogenes hortesis Lamiaceae hb Streptococcus cricetus Botrityis cinerea Sesan et al., 2015 Staphylococcus aureus Candida albicans Tuchila et al., 2008 Anethum graveolens Apiaceae hb; fl; fs; Shigella flexneri Jianu et al., 2012 sm Klebsiella pneumoniae Salmonella typhimurium E. coli majus Tropaeolaceae hb Pseudomonas aeruginosa Candida albicans Butnariu et Bostan, 2011 Salmonella sp. Bacillus sp. Veronica officinalis Plantaginaceae hb Listeria monocytogenes - Mocan et al., 2015a Listeria ivanovii Mocan et al., 2015b Veronica Plantaginaceae hb Staphylococcus aureus - Mocan et al., 2015a Bacillus cereus Mocan et al., 2015b Enterococcus faecalis Peptostreptococcus anaerobius Veronica orchidea Plantaginaceae hb Listeria monocytogenes - Mocan et al., 2015a Listeria ivanovii Mocan et al., 2015b Peptostreptococcus anaerobius Veronica persica Poiret Plantaginaceae hb; fl; fs Aspergillus niger Fierascu et al., 2018 Penicillium hirsutum Arctium lappa Asteraceae rx E. coli Aspergillus niger Fierascu et al., 2018 Salmonella abony Penicillium hirsutum Ionescu et al., 2013 fl Staphylococcus aureus Pirvu et al., 2017 Staphylococcus epidermidis Xanthium strumarium Asteraceae hb - Phytophthora infestans Rodino et al., 2013 Cnicus benedictus Asteraceae fs Salmonella typhimurium - Szabo et al., 2009 Salmonella enteritidis, Shigella sonnei Staphylococcus aureus Streptococcus pyogenes Proteus vulgaris, E. coli, Pseudomonas aeruginosa, Enterococcus faecalis Calendula officinalis Asteraceae hb Klebsiella penumoniae Candida albicans Jianu et al, 2016 S. aureus E. coli patula Asteraceae fs Pythium sp. Rodino et al., 2015 a Botrytis cinerea Sesean et al., 2015 Legend: hb: herba (flowering aerial parts); fl: folium (); fs: flos (); nd: needles; fr: fructus (); cx: cortex (bark); sm: semen (grains); rx: radix (roots); rh: rhizoma (); st: stipites (branches).

669 Similar results on essential oil of Melissa inhibit the growth of Pseudomonas aeruginosa, officinalis L. have been reported by Hancianu Listeria innocua and Streptococcus pyogenes. et al. (2008). Regarding Origanum vulgare, In the same family (Lamiaceae), Satureja Sandru et al. (2015) have proven that essential hortensis harvested in Southern Romania has oils made of the aerial parts have strong been reported to have antifungal effect on inhibitory effect on E.coli, same as other Botrytis cinerea (Sesan et al., 2015). Aqueous different species of Ocimum used as essential extracts of Satureja hortensis from Banat oils (Stefan et al., 2011). Ocimum sp. spectrum county have inhibited Streptococcus cricetus, is completed by Streptococcus cricetus which while in alcoholic extract inhibited is inhibited by the alcoholic extract (Tuchila et Staphylococcus aureus and Candida albicans al., 2008). (Tuchila et al., 2008). In the same family, essential oils of Thymus The list of aromatic plants with antimicrobial vulgaris aerial parts, harvested in Mehedinţi activity is also completed by the dill. Essential County, have moderate to strong inhibition on oils from , stems, immature and Staphylococcus aureus, Klebsiella pneumoniae, mature of Anethum graveolens L. grown Salmonella typhimurium, E. coli, Enterococcus in Western Romania (Timis county) were faecalis and Candida albicans (Boruga et al, isolated by steam distillation and tested on 2014); the authors correlate this activity with different bacteria. Significant antimicrobial the presence of phenolic compounds (thymol) activity was recorded against Shigella flexneri, and hydrocarbons (γ-terpinene). Some Klebsiella pneumoniae, Salmonella other authors reported higher antibacterial typhimurium and E. coli, while no inhibitory activity of extracts originated in effects were observed against Streptococcus Southern Romania (Dobre et al., 2011), as well pyogenes and Staphylococcus aureus, results as anti-fungal effect (Grigore Armatu et al., which is partially in contradiction with other 2012). reported results (Jianu et al., 2012). Other Thymus species have been investigated. From a plant mainly cultivated as ornamental Aerial parts of Thymus pulegioides collected at plant, , Butanriu and Bistan the flowering stage from two areas of the (2011) have extracted essential oils starting Bucegi Mountains at different altitudes (1000 from dehydrated leaves and flowers harvested and 1800 m above sea level) and aerial parts of in Timis county. The authors assumed that the T. glabrescens from the district of Gorj have antimicrobial action is determined by the been used for essential oils extraction (Pavel et phenols and metil-ethers identified in the T. al., 2010). Escherichia coli, Enterobacter majus extracts, but also by the tymol and cloacae, Proteus mirabilis, Bacillus subtilis carvacrol present in the volatile oil; the volatile and Micrococcus flavus were the strains most oils tested presented a wide range of action susceptible to T. pulegioides essential oil. over both Gram-positive and Gram–negative T.glabrescens essential oil inhibited the growth species. The most sensitive microorganism to of Salmonella typhimurium, Pseudomonas the action of the tested natural compounds of T. aeruginosa and Proteus mirabilis. The authors majus proved to be P. aeruginosa and C. have related the inhibitory activity tothe albicans, followed by Salmonella sp. and presence of monoterpenoid alcohols in this Bacillus sp, while the most resistant is the E. sample, especially of geraniol (55.5%), which coli stem. manifests an antiseptic activity comparable to A plant considered annual, but sometime being that of thymol, often against Pseudomonas. All an over winter specie, is Veronica persica the tested samples showed antifungal effects by Poiret. Crude hydroalcoholic extracts of its inhibiting the growth of Candida albicans. aerial parts originated in Pitesti hills showed The Thymus sp. spectrum of antibacterial important inhibitory effect on two pathogenic activity is completed with data reported by fungal species, Aspergillus niger and Varga et al. (2015). Essential oils of four Penicillium hirsutum (Fierascu et al., 2018). different Thymus species (T. vulgaris, T. This results have completed the image of serpyllum, T. pulegioides, and T. glabrescens) antimicrobial effect of Veronica sp. described harvested in Mures county have been proven to by Mocan et al. (2015), which have proven that

670 V. officinalis, V. teucrium and V. orchidea have typhimurium, Salmonella enteritidis to Shigella inhibitory effect on Staphylococcus aureus, sonnei, Staphylococcus aureus, Streptococcus Listeria monocytogenes and Listeria ivanovii. pyogenes, Proteus vulgaris, Escherichia coli, Other species of Veronica have been Pseudomonas aeruginosa and Enterococcus studied by Mocan et al. (2015 a, b). faecalis (Szabo et al., 2009). Hydroalcoholic extracts of aerial parts From Asteraceae family have been taken into harvested in Cluj county shows that in the case account also a species growing as , of V. officinalis, the most sensitive bacterial Xanthium strumarium. Ethanolic extracts of strains were Listeria monocytogenes and aerial parts of the plant have been demonstrated Listeria ivanovii; regarding V. teucrium to have inhibitory effect on the growth of a antibacterial activity, the strains of phytopathogenic fungi, Phytophthora infestans, Staphylococcus aureus, Bacillus cereus, the causative agent of late blight in tomatoes Enterococcus faecalis have been the most and potatoes (Rodino et al., 2013). Further, sensitive. Referring to the V. orchidea extract, Rodino et al. (2015 a) have tested another the most sensitive strains were Listeria Asteraceae representative, Tagetes patula monocytogenes and Listeria ivanovii. Also, the (marigold) on the phytopathogenic fungi extracts of V. teucrium and V. orchidea have Pythium sp., which can cause serious diseases been proven to have antibacterial activity, on such as damping off, rot, root rot and soft Peptostreptococcus anaerobius, an anaerobic rot in , , soybean, peppers, bean, Gram-positive bacteria responsible for clinical cucumber, tomato. Ethanolic extracts of infections. The authors come with the marigold flowers harvested from Southern assumption that the activity of Veronica Romanian from non-polluted sites, exhibited ethanolic extracts against Gram-positive moderate to high inhibition on the fungal bacteria like L. monocytogenes, L. ivanovii and specie. Other authors (Sesan et al., 2015) S. aureus could be attributed at least in part to reported Tagetes sp. extracts as having good their high β-sitosterol content but also to the antifungal activity on Botrytis cinerea. presence of campesterol and stigmasterol and Another annual member of Asteraceae family, may be might be influenced also by the Calendula officinalis, rarely studied for its presence of hispidulin. Relatively recently, antimicrobial activity, as essential oils of aerial have been given special attention to the parts has inhibited the growth of Klebsiella biennial Arctium lappa. Crude roots penumoniae, S. aureus, E. coli and of the hydroalcoholic extract proved inhibitory effect Candida albicans (Jianu et al., 2016). on Escherichia coli, Salmonella abony (Ionescu There are some other annual plants studied for et al., 2013), as well as on fungi as Aspergillus their antimicrobial activity, activity which have niger and Penicillium hirsutum (Fierascu et al., been proven to be weak on Romanian extracts, 2018). Authors have attributed the even some other reports are opposite. An antimicrobial properties to the phenolic acids example is Agrimoniae herba ethanolic extract content (such as chlorogenic acid, rutin, which has only a weak inhibitory effect on quercitrin, luteolin, p-coumaric acid, caffeic Pseudomonas aeuroginosa (Pirvu et al., 2016). acid and quercetin). In 2017, results obtained by Pirvu et al. suggest the potential uses of 2) Perennial plants Arctii folium whole (70%, v/v) ethanol extract The reported antimicrobial activity of perrenial in restoring the activity of the antibiotics plants from Romanian flora are synthetized in affected by microbial resistance, as well as Table 2 () and Table 3 ( inhibitory effect on Stapyloccous epidermidis. and trees), including their appurtenance to A thistle-like plant from Asteraceae family, botanical family and the plants’ part tested for Cnicus benedictus in different extracts of the inhibitory activity. immature capitulum harvested in North- Herbaceous plants Western Romania during prebloom period, Different species from Asteraceae family have have been proven to have a very large been proven to have inhibitory activity on antibacterial spectrum, from Salmonella pathogenic microorganisms. Achillea sp.

671 Table 2. Romanian perennial herbaceous plants with antimicrobial activity Plant species Botanical Plant part Antimicrobial activity Reference family Bacteria Fungi Achillea distans Asteraceae fs Listeria monocytogenes Benedec et al., 2013 Stahpylococcus aureus Achillea shurii Asteraceae fs Listeria monocytogenes Benedec et al., 2016 Staphylococcus aureus Salmonella typhimurium Achillea millefolium Asteraceae hb Klebsiella pneumoniae Candida albicans Jianu et al., 2016 Salmonella typhimurium Staphylococcus aureus Achillea collina Asteraceae fs E. coli, Shigella flexneri Jianu et al., 2015 Klebsiella pneumoniae Salmonella typhimurium Staphylococcus aureus spp. Asteraceae fs Sclerotinia sclerotiorum Badea and Delian, 2014 Tanacetum vulgare Asteraceae fs Bacillus cereus Muresan, 2015 Staphylococcus aureus Muresan et al., 2015 Inula helenium Asteraceae rx E. coli, Enterococcus faecalis Candida albicans Diguta et al., 2014 Bacillus cereus Candida parapsilosis Staphylococcus aureus Santolina rosmarinifolia Asteraceae hb; fl; fs Staphylococcus aureus Candida albicans Ioannou et al., 2007

Cynara scolymus Asteraceae fl E. coli, Salmonella abony Ionescu et al., 2013 Listeria innocua, Bacillus cereus Vamanu et al., 2011 Taraxacum officinale Asteraceae fl Escherichia coli Ionescu et al., 2013 Salmonella abony cannabium Asteraceae fl Escherichia coli Candida albicans Purcaru et al., 2015 Bacillus subtilis officinalis Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Stahpylococcus aureus Ilie et al., 2016 Klebsiella pneumoniae officinalis Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Stahpylococcus aureus Aspergillus flavus Aspergillus ochraceus officinalis Lamiaceae hb; fl; fs Listeria monocytogenes Candida albicans Benedec et al., 2015 Stahpylococcus aureus Jianu et al., 2016 P. aeruginosa Mihai and Popa, 2015 Vlase et al., 2014 piperita Lamiaceae hb - Candida albicans Jianu et al., 2016 Botrytis cinerea Sesan et al., 2015 Mentha smithiana Lamiaceae hb - Candida albicans Jianu et al., 2016 Mentha spicata Lamiaceae hb Listeria monocytogenes Candida albicans Moldovan et al., 2014 Mentha rotundifolia Lamiaceae hb Listeria monocytogenes Candida albicans Moldovan et al., 2014 genevensis Lamiaceae hb Staphylococcus aureus Toiu et al., 2016 Pseudomonas aeruginosa Listeria monocytogenes, E. coli, Salmonella typhimurium Lamiaceae hb Staphylococcus aureus Candida albicans Vlase et al., 2014 Hypericum perforatum Hypericaceae hb S. aureus, S. typhimurium Candida albicans Jianu et al., 2016 E. coli Eryngium campestre Apiaceae hb; fl; fs Staphylococcus aureus Conea et al., 2016 Stahpylococcus epidermidis Pseudomonas aeruginosa lupulus fs Bacillus subtilis, E. coli - Arsene et al., 2015 Enterococcus faecalis, Bacillus cereus, Staphylococcus aureus, Enterobacter cloacae, Pseudomonas fluorescens, helix Araliaceae fs; fr Stahpylococcus aureus Pop et al., 2017 Listeria monocytogenes Allium ursinum Amaryllidaceae Bacillus subtilis Aspergillus glaucus Lupoae et al., 2013 Allium sativum Staphylococcus aureus Geotrichum candidum Streptococcus pyogenes Candida albicans E.coli Botrytis cinerea Sesan et al., 2015 hb E. coli, Staphylococcus aureus Candida albicans Pirvu et al., 2017a nummularium Salmonella typhimurium Salmonella enterritidis Pseudomonas aerugionsa hb Staphylococcus aureus Pirvu et al., 2014 E. coli Pirvu et al., 2015 Chelidonium majus Papaveraceae hb Botrytyis cinerea Parvu et al, 2011 Glycyrrhiza glabra Fabaceae rx Pythium sp. Rodino et al., 2015a Paeonia officinalis Paeoniaceae E. coli, Pseudomonas aeruginosa Aspergillus niger Soare et al., 2012 Salmonella abony, Staphylococcus aureus Enterococcus faecalis Brevibacterium flavum Sarcina sp., Bacillus cereus Legend: hb: herba (flowering aerial parts); fl: folium (leaves); fs: flos (flowers); nd: needles; fr: fructus (fruits); cx: cortex (bark); sm: semen (grains); rx: radix (roots); rh: rhizoma (rhizome); st: stipites (branches). 672 Is one of the most studied in the family. aeruginosa (Muresan, 2015; Muresan et al., Achillea distans Waldst. et Kit. ex Willd., 2015). found in the Rodna Mountains (a subdivision The Asteraceae list is completed by Inula of the Eastern Carpathians in Northern helenium; the ethanolic extracts were obtained Romania), is confirmed as a native species of from the roots of plants harvested in Brasov the Romanian flora; its flowers hydroalcoholic county (Transilvania); moderate to high extract showed inhibitory activity on Gram- bacterial inhibition have been shown on positive bacteria as reported by Benedec et al Escherichia coli, Enterococcus faecalis, (2013). From the same family, hydroalcoholic Bacillus cereus and Staphylococcus aureus; extract of Achillea schurii Sch.-Bip., an meanwhile, moderate anti-Candida effects have endemic species from Romania, has revealed a been proven (Diguta et al., 2014). remarkable inhibitory effect on Listeria Essential oils of the heads and leaves of monocytogenes, Staphylococcus aureus and Santolina rosmarinifolia L. were obtained Salmonella typhimurium (Benedec et al., 2016). through hydrodistillation and tested against Essential oil of harvested from Gram-positive and Gram-negative bacteria Achillea millefolium and its Achillea strains and the fungus Candida albicans collina Becker growing wild in Western (Ioannou et al., 2007). The highest inhibitory Romania inhibited most strongly the growth of potential has been shown on Staphylococcus E. coli, followed by Shigella flexneri, aureus and Candida albicans. Klebsiella pneumoniae, Salmonella In the same family (Asteraceae) two other typhimurium and Staphylococcus aureus. No species, Cynara scolymus and Taraxacum effects were observed against Clostridium officinale have proven antibacterial activity in perfringens and Streptococcus pyogenes (Jianu hydroalcoholic leaves extracts against et al., 2015; Jianu et al., 2016). The authors Escherichia coli and Salmonella abony assumed this could be the results of the (Ionescu et al., 2013). Meanwhile, Vamanu et inhibitory effects exhibited by the major al. (2011) has reported that freeze-dried constituents of the analyzed essential oils, ethanolic extracts of Cynara scolymus respectively chamazulene, caryophyllene and harvested in Hunedoara county (Transylvania) β-pinene; also they noticed the presence of have significant inhibitory effect on Listeria certain minor components, known for their innocua and Bacillus cereus. strong antimicrobial activity, such as limonene, Purcaru et al. (2015) have tested different dried α-pinene or 1.8-cineole. leaves Eupatorium cannabium extracts made of Essentila oils obtained by hydro distillation, a Romanian from Brasov county. In the from Artemisia spp growth in different case of the chloroformic extract and hydro- Romanian areas, as spontaneous flora or as alcoholic extract the inhibitory activity has cultivated species have been tested against been noticed only in the case of Escherichia fungal pathogen Sclerotinia sclerotiorum (Lib.) coli and Bacillus cereus, as well as on the de Bary, from roots stored in the dimorphic Candida albicans. No clear refrigerator (Badea and Delian, 2014); inhibition has been noticed in the case of minimum inhibitory concentration (MIC) was Staphylococcus aureus, Enterococcus faecalis found to be 2400 μL L-1 for A. santonica, A. and Aspergillus niger. pontica, A. annua, A. austriaca, A. Lamiaceae family is on the top list of plants dracunculus, A. lerchiana, A. vulgaris and A. tested for their antimicrobial activity. Benedec vulgaris var. pilosa. et al. (2015) has proven that the Tanacetum vulgare is known mainly for its from L. and Rosmarinus toxicity and insect repelent properties. Essential officinalis L. has strong antibacterial effect on oils and ethanolic extracts of this plant, Gram positive bacteria, even higher than harvested in Transylvania (Sibiu and Alba gentamicin; similarly, strong effect has been county) exhibited moderate inhibition on noticed against Candida albicans, higher than Staphylococcus aureus and Bacillus subtilis, fluconazole. Meanwhile, essential oils from but low activity on E. coli and Pseudomonas aerial part of Salvia officinalis originated in Arad county showed strong inhibitory effect of

673 Staphyloccus aureus and Klebsiella from E. planum and E. campestre from Cluj pneumoniae (Ilie et al., 2016). The county and E. maritimum from Constanta antimicrobial activity recorded have been county have proven to have moderate attributed mainly to the major components of S. antibacterial activity on Stahpylococcus aureus officinalis essential oils, i.e., camphor, alpha- and Stahpylococcus epidermidis and high thujone and alpha-humulene, recognized for inhibitory activity on Pseudomonas their biological activities. Also, essential oils aeruginosa, especially in the case of E. and terpens extracted from Rosamarinus campestre (Conea et al., 2016); authors officinalis have been proven to have antifugal assumed that the activity of Eryngium tinctures effects, both on growth and sporulation of probably results from the synergistic effect of Aspergillus flavus and Aspergillus ochraceus; triterpene , polyphenols, sterols, lower effect have been registered on and other active compounds. Aspergillus niger (Mihai and Popa, 2015). (common hop) from Southern Remaining in the same Lamiaceae family, in Romania, an herbaceous climbing plant, as Romania has been reported for the first time hydroalcoholic extracts of female antimicrobial activity of essential oils of inflorescences, has been proven to have Mentha smithiana (Jianu et al., 2016). Aside antagonistic effect on both Gram-positive and Mentha piperita, their essential oils inhibited negative bacteria (Aresene et al., 2015). In the mainly the Gram-positive bacteria, as well as case of hope the substances associated with the fungus Candida albicans. Similar results antibacterial activity are humulone, lupulone have been obtained by the same authors in the and xanthohumol (Cermak et al., 2017). case of essential oils of Hypericum perforatum. Another climbing plant, Hedera helix harvested Also. Mentha sp. has been reported to have in Cluj county as leaves, flower and immature significant antifungal activity on Botrytis fruits has been tested by Pop et al. (2017). They cinerea (Şesan et al., 2015). Other species of have arrived to the conclusion that the Mentha genus have been reported for anti- immature fruits extract showed a significant Candida activity by Moldovan et al. (2014), activityagainst S. aureus, followed by the respectively extracts of M. spicata subsp. flower extract with a good growth inhibitory crispata and M. x rotundifolia. Same research effect against the same bacterial strain. Both group reported that other Mentha sp. extracts immature fruits and flowers extracts possess have strong inhibitory activity on Listeria appropriate antibacterialcapacity against L. monocytogenes. monocytogenes. Aerial part of harvested from Among perennial bulbous of Romanian wild wild populations from Cluj county at full flora has been tested Allium ursinum in flowering stage, in alcoholic extracts showed hydroalcoholic or acetic acid extracts obtained high inhibitory activity against Staphylococcus from different parts (leaves, roots, bulbs). The aureus, followed by Pseudomonas aeruginosa, extracts inhibited the growth of different Listeria monocytogenes, Escherichia coli and altering or pathogen fungi like Aspergillus Salmonella typhimurium (Toiu et al., 2016). glaucus, Geotrichum candidum and Candida Lamiaceae family list of plants with albicans, as well as on different Gram-positive animicorbial activity is completed by the and Gram-negative bacteria (Lupoae et al., ornamental Teucrium chamaedrys. Aerial parts 2013). The authors recommend their use in the harvested during summer in Sibiu county food industry as additive. Şesan et al. (2015) (Transilvania) have been prepared as ethanolic have also demonstrated that Allium sativum extract; the extract showed stronger extracts have inhibitory effects on Botrytis antibacterial activity against S. aureus than cinerea (grey mould)affecting cultures of Ribes gentamicin used as reference antibiotic, as well nigrum. as antifungal activity against Candida albicans, The hydroalcoholic extract of Chelidonium higher than fluconazole(Vlase et al., 2014). majus (Papaveraceae) obtained from powder of From Apiaceae family, different species of dried aerial plant organs collected from a Erymgium have been tested for their private homegarden in Cluj county had antimicrobial activity. Tincture of aerial plants antifungal effect against B. cinerea (Pârvu et

674 al., 2011). Another phytopathogenic fungi, harvested in July from Romanian Carpathian Pythium sp., have been proven to be inhibited Mountains. These extracts show certain by ethanolic extracts of Glycyrrhiza glabra antimicrobial activity on E. coli, as well as (Fabaceae) roots harvested in Southern weak to moderate activity on S. aureus, S. Romania from non-polluted sites (Rodino et al., typhimurium and S. enterritidis; the list is 2015a). completed by Pseudomonas aueriginosa and A novelty may be considered the studies Candida albicans. conducted by Pîrvu et al. (2017 a) regarding the Among perennial herbaceous plants tested for antimicrobial activities of extracts from rock antimicrobial activity an was rose ( Mill.) in the research attention. Red of Paeonia

Table 3. Romanian perennial woody plants with antimicrobial activity

Botanical Plant Antimicrobial activity Plant species Reference family part Bacteria Fungi BUSHES/SHRUBS angustifolia Lamiaceae fs Shigella flexneri Candida albicans Jianu et al., 2013 Lavandula x intermedia Staphylococcus aureus Robu et al., 2016 E. coli opulus hb; fl; fs Staphylococcus aureus Bubulica et al., 2012 Staphylococcus epidermidis Lonicera tatarica Caprifoliaceae hb; fl; fs Staphylococcus aureus Bubulica et al., 2012 Staphylococcus epidermidis Aronia melanocarpa fr; fl Vibrio vulnificus, Giupana et al., 2016 V. cholera, V. mimicus E. coli Enterococcus faecalis Lycium barbarum Solanaceae fl; fs Staphylococcus aureus Mocanu et al., 2014 Listeris monocytogenes Mocanu et al., 2015c Bacillus subtilis Lycium chinense Solanaceae fl Staphylococcus aureus Mocanu et al., 2014 Bacillus subtilis Listeria monocytogenes Salmonella thyphimurium Adoxaceae fr Pseudomonas fluorescens Rodino et al., 2015b Enterococcus faecalis Juniperus communis Cupressaceae fr Bacillus subtilis Ivopol et al., 2016 Streptococcus luteus Staphylococcus aureus Escherichia coli Abies alba Pinaceae nd; cx Bacillus subtilis Ivopol et al., 2016 Streptococcus luteus Staphylococcus aureus Escherichia coli Sandru et al., 2015 Picea abies Pinaceae nd Staphylococcus aureus Candida albicans Radulescu et al., 2011 Bacillus cereus Aspergillus niger Proteus vulgaris Pinus sylvestris Pinaceae nd; cx Bacillus subtilis Ivopol et al., 2016 Streptococcus luteus Staphylococcus aureus Escherichia coli Pinus cembra L. Pinaceae nd; cx Staphylococcus aureus Candida albicans Apetrei et al., 2011 Sarcina lutea Apetrei et al., 2013 Bacillus cereus Escherichia coli Pseudomonas aeruginosa Fagus sylvatica Fagaceae fl Staphylococcus aureus Pirvu et al., 2014

Robinia pseudoacacia Fabaceae fs; sm Staphyloccous sp., Candida albicans Rosu et al., 2012 cx; fl Streptococcus sp. E coli., Pseudomonas aeruginosa, Proteus sp., Salmonella enterica Cydonia oblonga Rosaceae fl Staphylococcus aureus Cerempei et al., 2016 Escherichia coli Pseudomonas aeruginosa Legend: hb: herba (flowering aerial parts); fl: folium (leaves); fs: flos (flowers); nd: needles; fr: fructus (fruits); cx: cortex (bark); sm: semen (grains); rx: radix (roots); rh: rhizoma (rhizome); st: stipites (branches). officinalis, in ethanolic and methanolic extracts coli, Pseudomonas aeruginosa, Salmonella have shown strong inhibitory activity on abony, Staphylococcus aureus, Enterococcus bacteria and fungi, respectively Escherichia faecalis, Brevibacterium flavum, Sarcina sp.,

675 Bacillus cereus and Aspergillus niger (Soare et was shown by L. chinense extract against al., 2012). Bacillus subtilis. Meanwhile, extract made of L. Bushes/Shrubs barbarum flowers was found to be more active Lavender (L. angustifolia Miller) and lavandin on the Gram-positive bacterial strains; the best (Lavandula x intermedia) are well known for antibacterial activity was shown against their medical and cosmetics applications. Staphylococcus aureus (Mocan et al., 2015 c). Essential oils obtained by steam distillation The perennial herbaceous extracts of Epilobium from fresh inflorescences harvested in Western hirsutum harvested in Prahova county inhibited Romania showed antimicrobial activity against both Stapyloccous aureus and E. coli (Pirvu et Shigella flexneri, Staphylococcus aureus, E. al., 2014). Same group (Pîrvu et al., 2015) coli and Salmonella typhimurium, while suggested an augmented antimicrobial potency Streptococcus pyogenes was not sensitive to on Stapyloccous aureus of the combination their action (Jianu et al., 2013). The authors kaempferol-caffeic acid derivates (aqueous emphasize the fact that even in the absence of fraction) than myricetin-gallic acid derivate active principles like and linalyl (ethyl acetic fraction). acetate, considered responsible for the The dwarf elderberry (Sambucus ebulus) used antibacterial and antifungal properties of in traditional medicine, has proven to have essential oils obtained from different species of antibacterial effects on Pseudomonas Lavandula. This results looks to be in contrast fluorescens and Enterococcus faecalis when with results reported by Robu et al. (2016) on used as ethanolic extract made of fruits (Rodino essential oils of lavandin (Lavandula hybrida et al., 2015 b). Reverchon) harvested in North-Eastern Romania (Neamt county); these oils showed no Trees activity against Gram-negative strains; also the Conifers are widely used for the extraction of results showed that the antistaphylococcal essential oils and their volatile oils contain activity is reduced, while there is a moderate mainly monoterpene (Ivopol et al., 2016). antifungal activity. Among the conifers Pinus sp. (Pinaceae) has Two bushes belonging to Caprifoliaceae been widely studied. Pinus cembra L. from family, and Lonicera tatarica Carpahtian Mountains, bark and needles, have from Craiova, Dolj county have been tested by antimicrobial effects against Staphylococcus Bubulica et al. (2012); aqueous extracts of aureus, Sarcina lutea, Bacillus cereus, aerial parts (stem, flower , pulp) have Escherichia coli, Pseudomonas aeruginosa and been tested on Staphylococcus aureus and Candida albicans (Apetrei et al., 2011; Apetrei Staphylococcus epidermidis. The results et al., 2013). Common Pinus sylvestris showed a higher inhibition in the case of essential oils from needles and sprouts showed Lonicera tatarica extracts. inhibitory effects on Bacillus subtilis, Studies on bacterial strains isolated from wild Streptococcus luteus, Staphylococcus aureus birds captured in Danube Delta Biosphere and Escherichia coli; similar results have been Reservation proved that extracts of fresh fruits obtained by the use of essential oils from of Aronia melanocarpa has important Juniperus communis berries and Abies alba inhibition on Vibrio spp. (V. vulnificus, V. needles and sprouts (Ivopol et al., 2016). cholera, V. mimicus), E. coli, Enterococcus Sandru et al. (2015) also proved inhibition on faecalis (Giupana et al., 2016). E. coli by the use of Abies alba essential oils. Ethanolic extracts of Lycium sp. (Solanaceae) Antimicrobial properties of volatile oil is olated leaves originated in Cluj county, have been from sprouts of Picea abies growing wild in tested for antimicrobial activity (Mocan et al., Romanian Carpathian Mountains (Prahova 2014). The authors reported that L. chinense Valley) have been tested by Radulescu et al. extract was more active than L. barbarum (2011). The most evident inhibitory effect was against both Gram-positive and Gram-negative noticed against the Gram-positive bacterial strains and that these species as (Staphylococcus aureus, Bacillus cereus), important sources of flavonoids and Gram-negative (Proteus vulgaris) and fungal chlorogenic acid. The best antibacterial activity strains (Candida albicans, Aspergillus niger).

676 There are authors which have tested more herbaceous perennial and the rest (25%) are species from a specific Romanian region for woody perennial species (bushes and trees). their antimicrobial activity. For example, Pirvu The antimicrobial studies have been mainly et al. (2014) have focused on herbaceous and focused on species belonging to two botanical woody plants from Prahova county in families, Asteracea and Lamiaceae, which propylene glycol solutions or in separate represents 50% of the total studies species. aqueous, ethyl acetate and chloroform In terms of microbial species can be noticed an fractions. Among the trees, extracts from leaves intensive focus on pathogenic Gram-positive of Fagus sylvatica exhibited moderate and Gram-negative bacteria, responsible for inhibitory effect on Stapyloccous aureus, clinical infections or food contamination. For ethanolic extracts from flowers and seeds of 89% of the species have been reported Robinia pseudoacacia have inhibitory activity antibacterial activity, while only 57.8% of the mainly on Gram-positive coci (Staphyloccous species have proven antifungal activity. The sp., Streptococcus sp.), while same extracts most reported susceptible fungus was Candida from bark and leafs inhibited E coli, albicans; few reports are focused on Pseudomonas aeruginosa, Proteus sp., filamentous fungi like Aspergillus sp., Salmonella enterica and Candida albicans. Penicillium sp, Botrytis cinerea or Pythium sp. As a novelty can be mentioned the use of fall It has been noticed that some of the reports are quince (Cydonia oblonga) leavesoriginated in novelty in the subject and the researchers have North-Eastern Romania for the production of approached some spontaneous species little or natural dye; it has been proven (Cerempei et not ever reported in the international databases al., 2016) that such dye with mordant (silver (e.g. Helianthemum nummularium, Cydonia nitrate) have a good antibacterial activity oblonga, Paeonia officinalis). This trend may against Gram-positive (S. aureus) and Gram- be a solution for further research in the topic, as negative (E. coli and Ps. aeruginosa); the well as enlarging the studies on filamentous authors assumed that a possible explanation can fungi, even if they are of medical or feed/food be that the wool-Ag-flavonoid complex has a interest. larger surface area that gives antibacterial effect. REFERENCES

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