A Review on Antimicrobial Activity of Mushroom (Basidiomycetes) Extracts and Isolated Compounds
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Reviews 1707 A Review on Antimicrobial Activity of Mushroom (Basidiomycetes) Extracts and Isolated Compounds Authors Maria José Alves1, 2,3, 4, Isabel C. F. R. Ferreira3, Joana Dias4, Vânia Teixeira4, Anabela Martins3, Manuela Pintado1 Affiliations 1 CBQF-Escola Superior de Biotecnologia, Universidade Católica Portuguesa Porto, Porto, Portugal 2 Centro Hospitalar de Trás-os-Montes e Alto Douro-Unidade de Chaves, Chaves, Portugal 3 CIMO-Escola Superior Agrária, Instituto Politécnico de Bragança, Campus de Santa Apolónia, Bragança, Portugal 4 Escola Superior de Saúde, Instituto Politécnico de Bragança, Bragança, Portugal Key words Abstract crobial activity against gram-positive bacteria, l" mushrooms ! while 2-aminoquinoline, isolated from Leucopax- l" Basidiomycetes Despite the huge diversity of antibacterial com- illus albissimus, presents the highest antimicrobial l" antimicrobials pounds, bacterial resistance to first-choice anti- activity against gram-negative bacteria. l" gram‑positive bacteria biotics has been drastically increasing. Moreover, l" gram‑negative bacteria the association between multiresistant microor- ganisms and nosocomial infections highlight the Abbreviations problem, and the urgent need for solutions. Natu- ! ral resources have been exploited in the last years CSAP: Cordyceps sinensis antibacterial pro- and among them, mushrooms could be an alter- tein native source of new antimicrobials. In this re- CFU: colony forming unities view, we present an overview of the antimicrobial ERSP: erythromycin-resistant Streptococcus properties of mushroom extracts and highlight pyogenes some of the active compounds identified, includ- HMW: high-molecular weight compounds ing low- and high-molecular weight (LMW and IC50: concentration inhibiting 50% of the HMW, respectively) compounds. LMW com- growth pounds are mainly secondary metabolites, such IZD: internal zone diameter as sesquiterpenes and other terpenes, steroids, LMW: low-molecular weight compounds anthraquinones, benzoic acid derivatives, and M: mycelium quinolines, but also primary metabolites such as MIC: minimal inhibitory concentration oxalic acid. HMW compounds are mainly pep- MRSA: methicillin-resistant Staphylococcus tides and proteins. Data available from the litera- aureus ture indicate a higher antimicrobial activity of MRSE: methicillin-resistant Staphylococcus received July 3, 2012 revised August 8, 2012 mushroom extracts against gram-positive bacte- epidermidis accepted August 22, 2012 ria. Among all the mushrooms, Lentinus edodes is PABA: para-aminobenzoic acid the most studied species and seems to have a PRSP: penicillin-resistant Streptococcus Bibliography DOI http://dx.doi.org/ broad antimicrobial action against both gram- pneumonia 10.1055/s-0032-1315370 postive and gram-negative bacteria. Plectasin VREF: vancomycin-resistant Enterococcus Published online September 21, peptide, obtained from Pseudoplectania nigrella, faecium 2012 is the isolated compound with the highest antimi- Planta Med 2012; 78: 1707–1718 © Georg Thieme Verlag KG Stuttgart · New York · ISSN 0032‑0943 Introduction The psychedelic and consciousness expansion ! properties of some species have pushed mush- Correspondence Prof. Isabel C. F. R. Ferreira, Mushroom bioactivity rooms to become part of some religions. Even PhD For a long time, mushrooms have been playing an toxic mushrooms have found a place of relevance, Instituto Politécnico de Bragança important role in several aspects of human activ- because of the uniqueness of their compounds Campus de Santa Apolónia, apartado 1172 ity. Edible mushrooms, for example, are used ex- that evolved naturally as a protection against con- 5301–855 Bragança tensively in cooking and make up part of low-cal- sumption [1]. Portugal orie diets. Mythology is extensively garnished by Wild and cultivated mushrooms contain a huge Phone: + 351273303219 Fax: + 351273325405 mushrooms and is typically associated with diversity of biomolecules with nutritional [2] [email protected] gnomes, fairies, and other fairytale personages. and/or medicinal properties [3–5]. Due to these Alves MJ et al. A Review on… Planta Med 2012; 78: 1707–1718 1708 Reviews properties, they have been recognized as functional foods, and as are widely used for medicinal purposes. Their pharmacological a source for the development of medicines and nutraceuticals. action and therapeutic interest in promoting human health have Fruiting bodies, mycelia, and spores accumulate a variety of bio- been known for thousands of years [5,15,16]. active metabolites with immunomodulatory, cardiovascular, liver In particular, mushrooms could be a source of natural antibiotics, protective, antifibrotic, anti-inflammatory, antidiabetic, antiviral, which can be LMW and HMW, respectively, compounds. LMW antioxidant, antitumor, and antimicrobial properties [3–14]. compounds are mainly secondary metabolites such as sesquiter- The frequent use of mushrooms is based on three main assump- penes and other terpenes, steroids, anthraquinone and benzoic tions: first, they are used as part of a regular diet for their nutri- acid derivatives, and quinolines, but also primary metabolites tional value (since they are rich in water, minerals, proteins, fi- such as oxalic acid (l" Fig. 1). HMW compounds mainly include bers, and carbohydrates, and are low-caloric foods due to a low peptides and proteins. content in fat [2]); secondly, fruiting bodies are also appreciated It is estimated that there are about 140 000 species of mush- for their delicacy (they are palatability enhancers of flavor and rooms on earth, and of these only 22 000 are known and only a aroma when associated to other foods); and thirdly, mushrooms small percentage (5%) has been investigated. Therefore, there is Fig. 1 Chemical structure of the low-molecular weight (LMW) compounds with antimicrobial potential found in mushrooms. Alves MJ et al. A Review on… Planta Med 2012; 78: 1707–1718 Reviews 1709 much to explore about mushroom properties and potential ap- Antimicrobial Activity Against Gram-Positive Bacteria plications [4]. ! Methodologies Bacteria and drug discovery Different methodologies have been used to assess antimicrobial The development of antibiotics has been one of the most impor- activity of mushroom extracts and compounds, including the mi- tant scientific achievements of the last seventy years. These com- crodilution method, the disk diffusion method, the agar streak di- pounds act in several ways, by interfering in metabolic processes lution method based on radial diffusion, and a method with the or in the organism structures [17]. The mechanism of action is incorporation of the extract in the culture medium and further mostly related with interferences in the synthesis of the cell wall, determination of colonies. Therefore, the results for antimicrobial modification of plasmatic membrane permeability, interferences activity are expressed in different unities (l" Tables 1 and 2). in chromosome replication, or in protein synthesis [18]. The cell The microdilution method comprises microdilutions of the ex- wall is responsible for the shape and rigidity of bacterial cells, act- tract in liquid medium using microplates to determine MIC or ing as an osmotic barrier [19]. The peptidoglycan content in the IC50 values. In the disk difusion method, the extract is incorpo- cell wall varies between 10% and 60% for gram-negative and rated in disks at different concentrations, and the halo of growth gram-positive bacteria, respectively [20,21]. inhibition is determined and represented by IZD (internal zone Antiparietal antibiotics act in one of the phases of peptidoglycan diameter) values. The agar streak dilution method based on radial synthesis, being classified according to that phase. Phosphomy- diffusion is most widely used in extracts and implies the extract cin, D-cycloserine, glycopeptides (bacitracin, vancomycin, teico- application in circular holes made in solid medium. The result planin), and beta-lactams (penicillins, cephalosporins, carbape- might be expressed in IZD or MIC values. Regarding the fourth nemics, monobactamics) are some examples of this group [22]. method, the extract is incorporated in the culture medium and Otherwise, other antibiotics such as ascolistin and daptomycin then CFU are determined. act at the cell membrane level. Aminoglycosides and tetracy- clines, macrolides, oxazolidines, quinupristin and dalfopristin, Mushroom extracts with antimicrobial activity clindamycin, and chloramphenicol inhibit protein synthesis by Numerous mushroom extracts have been reported as having interfering with 30 s or 50 s ribosomal subunits. Quinolones, ri- antimicrobial activity against gram-positive bacteria (l" Table 1). fampicin, and metronidazol inhibit nucleic acid synthesis. Sulfon- Agaricus bisporus, the most cultivated mushroom in the world, amides and trimetoprim are antimetabolic antibiotics that inhib- should be highlighted. Its methanolic extract revealed MIC = it the metabolic chain of PABA, essential to cell growth [23]. 5 µg/mL against Bacillus subtilis, even lower than the standard Despite the huge diversity of antibacterial compounds, bacterial ampicillin (MIC = 12.5 µg/mL) [31], and also showed activity resistance to first-choice antibiotics has been drastically increas- against Bacillus cereus, Micrococcus luteus, Micrococcus flavus, ing. Some examples are microorganisms such as Klebsiella spp. Staphylococcus aureus,andStaphylococcus epidermidis [15,32, and Escherichia coli, which produce broad-spectrum