{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,28]],"date-time":"2026-01-28T23:31:41Z","timestamp":1769643101022,"version":"3.49.0"},"reference-count":46,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2020,9,22]],"date-time":"2020-09-22T00:00:00Z","timestamp":1600732800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Molecules"],"abstract":"<jats:p>This study explored the biological properties of three wild growing Russula species (R. integra, R. rosea, R. nigricans) from Serbia. Compositional features and antioxidant, antibacterial, antibiofilm, and cytotoxic activities were analyzed. The studied mushroom species were identified as being rich sources of carbohydrates and of low caloric value. Mannitol was the most abundant free sugar and quinic and malic acids the major organic acids detected. The four tocopherol isoforms were found, and polyunsaturated fatty acids were the predominant fat constituents. Regarding phenolic compounds, P-hydroxybenzoic and cinnamic acids were identified in the prepared methanolic and ethanolic extracts, which displayed antioxidant activity through the inhibition of thiobarbituric acid reactive substances (TBARS) formation and oxidative hemolysis; the highest activity was attributed to the R. nigricans ethanolic extract. This is the first report on the antibacterial and antibiofilm potential of the studied species, with the most promising activity observed towards Streptococcus spp. (0.20\u20130.78 mg\/mL as the minimal inhibitory concentration, MIC). The most promising cytotoxic effect was caused by the R. integra methanolic extract on non-small cell lung cancer cells (NCI-H460). Therefore, due to the observed in vitro bioactive properties, the studied mushrooms arise as a source of functional ingredients with potential to be used in novel nutraceutical and drug formulations, which can be used in the treatment of various diseases and health conditions.<\/jats:p>","DOI":"10.3390\/molecules25184336","type":"journal-article","created":{"date-parts":[[2020,9,24]],"date-time":"2020-09-24T03:03:39Z","timestamp":1600916619000},"page":"4336","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Antioxidant Extracts of Three Russula Genus Species Express Diverse Biological Activity"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8717-6495","authenticated-orcid":false,"given":"Marina","family":"Kosti\u0107","sequence":"first","affiliation":[{"name":"Department of Plant Physiology, Institute for Biological Research \u201cSini\u0161a Stankovi\u0107\u201d-National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2480-5490","authenticated-orcid":false,"given":"Marija","family":"Ivanov","sequence":"additional","affiliation":[{"name":"Department of Plant Physiology, Institute for Biological Research \u201cSini\u0161a Stankovi\u0107\u201d-National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0157-9873","authenticated-orcid":false,"given":"\u00c2ngela","family":"Fernandes","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7523-1637","authenticated-orcid":false,"given":"Jos\u00e9","family":"Pinela","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6801-4578","authenticated-orcid":false,"given":"Ricardo C.","family":"Calhelha","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"given":"Jasmina","family":"Glamo\u010dlija","sequence":"additional","affiliation":[{"name":"Department of Plant Physiology, Institute for Biological Research \u201cSini\u0161a Stankovi\u0107\u201d-National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9050-5189","authenticated-orcid":false,"given":"Lillian","family":"Barros","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4910-4882","authenticated-orcid":false,"given":"Isabel C. F. R.","family":"Ferreira","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"given":"Marina","family":"Sokovi\u0107","sequence":"additional","affiliation":[{"name":"Department of Plant Physiology, Institute for Biological Research \u201cSini\u0161a Stankovi\u0107\u201d-National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9478-5448","authenticated-orcid":false,"given":"Ana","family":"\u0106iri\u0107","sequence":"additional","affiliation":[{"name":"Department of Plant Physiology, Institute for Biological Research \u201cSini\u0161a Stankovi\u0107\u201d-National Institute of Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade, Serbia"}]}],"member":"1968","published-online":{"date-parts":[[2020,9,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2660","DOI":"10.2174\/15680266113136660192","article-title":"Antioxidant Protective Effects of Mushroom Metabolites","volume":"13","author":"Stajic","year":"2013","journal-title":"Curr. Top. Med. Chem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"19489","DOI":"10.3390\/molecules201019489","article-title":"Antioxidants of edible mushrooms","volume":"20","author":"Kozarski","year":"2015","journal-title":"Molecules"},{"key":"ref_3","first-page":"118","article-title":"Free radicals, antioxidants and functional foods: Impact on human health","volume":"4","author":"Lobo","year":"2010","journal-title":"Pharm. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.synbio.2016.12.001","article-title":"Reactive oxygen species and antioxidant properties from mushrooms","volume":"2","year":"2017","journal-title":"Synth. Syst. Biotechnol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"757","DOI":"10.2147\/CIA.S158513","article-title":"Oxidative stress, aging, and diseases","volume":"13","author":"Liguori","year":"2018","journal-title":"Clin. Interv. Aging"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.2174\/092986709787909587","article-title":"Antioxidants in Wild Mushrooms","volume":"16","author":"Ferreira","year":"2009","journal-title":"Curr. Med. Chem."},{"key":"ref_7","first-page":"146","article-title":"Cytotoxicity through Molecular Targets Involved in Apoptosis. Where Should We Further Search for Mushrooms Functionalities in Future Cancer Treatment?","volume":"Volume 5","year":"2019","journal-title":"Frontiers in Natural Product Chemistry"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0194-5998(03)00630-2","article-title":"Free radicals and scavenging enzymes in chronic tonsillitis","volume":"129","author":"Kaygusuz","year":"2003","journal-title":"J. Otolaryngol.-Head N."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1016\/j.anl.2008.10.004","article-title":"Investigation of oxidative stress in patients with chronic tonsillitis","volume":"36","author":"Cvetkovic","year":"2009","journal-title":"Auris Nasus Larynx"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.phanu.2017.02.001","article-title":"Mushroom nutraceuticals for improved nutrition and better human health: A review","volume":"5","author":"Rathore","year":"2017","journal-title":"PharmaNutrition"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Petropoulos, S.A., Ferreira, I.C.F.R., and Barros, L. (2018). Root vegetables as a source of biologically active agents-lesson from soil, In Phytochemicals in Vegetables: A valuable source of bioactive compounds, Bentham Science Publishers Ltd.","DOI":"10.2174\/97816810873991180101"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/nbt0898-728","article-title":"Nutraceuticals: Poised for a healthy slice of the healthcare market?","volume":"16","author":"Brower","year":"1998","journal-title":"Nat. Biotechnol."},{"key":"ref_13","first-page":"496","article-title":"Mushroom as the potential source of new generation of antioxidant: A review","volume":"6","author":"Khatua","year":"2013","journal-title":"Res. J. Pharm. Technol."},{"key":"ref_14","first-page":"141","article-title":"Mushrooms as Sources of Therapeutic Foods","volume":"Volume 8","author":"Grumezescu","year":"2018","journal-title":"Therapeutic Foods Handbook of Food Bioengineering"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/21501203.2018.1500400","article-title":"A preliminary DNA barcode selection for the genus","volume":"10","author":"Li","year":"2019","journal-title":"Mycology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"7678","DOI":"10.1039\/C9FO01900F","article-title":"Comparative investigation on edible mushrooms Macrolepiota mastoidea, M. rhacodes and M. procera: Functional foods with diverse biological activities","volume":"10","author":"Fernandes","year":"2019","journal-title":"Food Funct."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.foodchem.2013.11.062","article-title":"A mini-review of chemical composition and nutritional value of edible wild-grown mushroom from China","volume":"151","author":"Wang","year":"2014","journal-title":"Food Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"C824","DOI":"10.1111\/j.1750-3841.2011.02251.x","article-title":"Toward the antioxidant and chemical characterization of mycorrhizal mushrooms from Northeast Portugal","volume":"76","author":"Reis","year":"2011","journal-title":"J. Food Sci"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/j.foodres.2012.06.013","article-title":"Chemical characterization of Agaricus bohusii, antioxidant potential and antifungal preserving properties when incorporated in cream cheese","volume":"48","author":"Reis","year":"2012","journal-title":"Food Res. Int."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1602","DOI":"10.1039\/c4fo00054d","article-title":"Cultivated strains of Agaricus bisporus and A. brasiliensis: Chemical characterization and evaluation of antioxidant and antimicrobial properties for final healthy product\u2014Natural preservatives in yoghurt","volume":"5","author":"Reis","year":"2014","journal-title":"Food Funct."},{"key":"ref_21","first-page":"73","article-title":"Edible Ectomycorrhizal mushrooms Russula spp. of Cote d\u2019Ivoire: Total phenolic content, HPLC-profiles of phenolic compounds and organic acids, antioxidant activities","volume":"5","author":"Kouassi","year":"2016","journal-title":"J. Agric. Chem. Environ."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.foodchem.2008.01.054","article-title":"Comparative study of phytochemicals and antioxidant potential of wild edible mushroom caps and stipes","volume":"110","author":"Ribeiro","year":"2008","journal-title":"Food Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s12161-012-9443-1","article-title":"Optimized analysis of organic acids in edible mushrooms from Portugal by ultra-fast liquid chromatography and photodiode array detection","volume":"6","author":"Barros","year":"2013","journal-title":"Food Anal. Method"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/s00217-017-2952-9","article-title":"Profile of phenolic and organic acids, antioxidant properties and ergosterol content in cultivated and wild growing species of Agaricus","volume":"244","author":"Magdziak","year":"2018","journal-title":"Eur. Food Res. Technol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.fct.2013.01.010","article-title":"Bioactive microconstituents and antioxidant properties of wild edible mushrooms from the island of Lesvos, Greece","volume":"55","author":"Kalogeropoulos","year":"2013","journal-title":"Food Chem. Toxicol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"20650","DOI":"10.3390\/molecules191220650","article-title":"Expanding current knowledge on the chemical composition and antioxidant activity of the genus Lactarius","volume":"19","author":"Vieira","year":"2014","journal-title":"Molecules"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3239","DOI":"10.1039\/C7FO00887B","article-title":"Chemical, nutritive composition and a wide range of bioactive properties of honey mushroom: Armillaria mellea (Vahl: Fr.) Kummer","volume":"8","author":"Barros","year":"2017","journal-title":"Food Funct."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1016\/j.foodchem.2009.09.025","article-title":"Tocopherols composition of Portuguese wild mushrooms with antioxidant capacity","volume":"119","author":"Heleno","year":"2010","journal-title":"Food Chem."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Khatua, S., Gupta, S.S., Ghosh, M., Tripathi, S., and Acharya, K. (2020). Exploration of nutritional, antioxidative, antibacterial and anticancer status of Russula alatoreticula: Towards valorization of a traditionally preferred unique mycofood. J. Food Sci. Technol.","DOI":"10.1007\/s13197-020-04723-9"},{"key":"ref_30","first-page":"6","article-title":"Antioxidant Properties of Wild Edible Mushrooms","volume":"2","author":"Koca","year":"2011","journal-title":"J. Food Process. Tehnol."},{"key":"ref_31","first-page":"194","article-title":"Biochemical and antioxidant properties of wild edible mushrooms used for food by tribal of eastern India","volume":"8","author":"Tripathy","year":"2016","journal-title":"Int. J. Pharm. Pharm. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2052","DOI":"10.1016\/j.fct.2009.05.029","article-title":"Antimicrobial and antioxidant activities of Russula delica Fr","volume":"47","author":"Yaltirak","year":"2009","journal-title":"Food Chem. Toxicol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Khatua, S., Dutta, A.K., Chandra, S., Paloi, S., Das, K., and Acharya, K. (2017). Introducing a novel mushroom from mycophagy community with emphasis on biomedical potency. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0178050"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1111\/j.1365-2672.2012.05347.x","article-title":"Antimicrobial activity of wild mushroom extracts against clinical isolates resistant to different antibiotics","volume":"113","author":"Alves","year":"2012","journal-title":"J. Appl. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Kosti\u0107, M., Ivanov, M., Babi\u0107, S.S., Petrovi\u0107, J., Sokovi\u0107, M., and \u0106iri\u0107, A. (2020). An up-to-date review on bio-resource therapeutics effective against bacterial species frequently associated with chronic sinusitis and tonsillitis. Curr. Med. Chem.","DOI":"10.2174\/0929867327666200505093143"},{"key":"ref_36","unstructured":"Ravishankar Rai, V., and Jamuna, A.B. (2020). Recent Advances in Science of Quorum Sensing: An Overview of Natural Product Inhibitors. Trends in Quorum Sensing and Quorum Quenching: New Perspectives and Applications, Taylor & Francis Ltd."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.bbagen.2010.12.005","article-title":"Ergosta-4, 6, 8 (14), 22-tetraen-3-one induces G2\/M cell cycle arrest and apoptosis in human hepatocellular carcinoma HepG2 cells","volume":"1810","author":"Zhao","year":"2011","journal-title":"Biochim. Biophys. Acta (BBA)-Gen. Subj."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1016\/j.phymed.2010.02.001","article-title":"First isolation and characterization of a novel lectin with potent antitumor activity from a Russula mushroom","volume":"17","author":"Zhang","year":"2010","journal-title":"Phytomedicine"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3012","DOI":"10.1007\/s11947-013-1248-8","article-title":"Using gamma irradiation to attenuate the effects caused by drying or freezing in Macrolepiota procera organic acids and phenolic compounds","volume":"7","author":"Fernandes","year":"2014","journal-title":"Food Bioprocess Technol."},{"key":"ref_40","unstructured":"Horwitz, W., and Latimer, G. (2016). AOAC Official Methods of Analysis of AOAC International, AOAC International."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2742","DOI":"10.1016\/j.fct.2008.04.030","article-title":"Wild and commercial mushrooms as source of nutrients and nutraceuticals","volume":"46","author":"Barros","year":"2008","journal-title":"Food Chem. Toxicol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1016\/j.foodchem.2012.02.086","article-title":"Development of a simple 96-well plate method for evaluation of antioxidant activity based on the oxidative haemolysis inhibition assay (OxHLIA)","volume":"134","author":"Takebayashi","year":"2012","journal-title":"Food Chem."},{"key":"ref_43","unstructured":"(2003). European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin. Microbiol. Infect., 9, ix\u2013xv."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1111\/j.1600-0463.2007.apm_630.x","article-title":"Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm producton by staphylococci","volume":"115","author":"Hola","year":"2007","journal-title":"Apmis"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5417","DOI":"10.1039\/C8FO01466C","article-title":"Characterization of phenolic compounds intincture of edible Nepeta nuda: Development of antimicrobial mouthwash","volume":"9","author":"Dias","year":"2018","journal-title":"Food Funct."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1038\/nprot.2006.179","article-title":"Sulforhodamine B colorimetric assay for cytotoxicity screening","volume":"1","author":"Vichai","year":"2006","journal-title":"Nat. Protoc."}],"container-title":["Molecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1420-3049\/25\/18\/4336\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:12:19Z","timestamp":1760177539000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1420-3049\/25\/18\/4336"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,22]]},"references-count":46,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2020,9]]}},"alternative-id":["molecules25184336"],"URL":"https:\/\/doi.org\/10.3390\/molecules25184336","relation":{},"ISSN":["1420-3049"],"issn-type":[{"value":"1420-3049","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,22]]}}}