See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/338632886 Exploring the powerful phytoarsenal of white grape marc against bacteria and parasites causing significant diseases Article in Environmental Science and Pollution Research · May 2021 DOI: 10.1007/s11356-019-07472-1 CITATIONS READS 4 211 8 authors, including: Natalia Mallo Marco Biddau University of Glasgow Unemployed 25 PUBLICATIONS 154 CITATIONS 24 PUBLICATIONS 101 CITATIONS SEE PROFILE SEE PROFILE Francisco Fernandes Instituto Politécnico de Bragança 2 PUBLICATIONS 4 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Mitochondrial functions in Toxoplasma View project Vermicomposting and vermicompost View project All content following this page was uploaded by A. Choupina on 16 January 2020. The user has requested enhancement of the downloaded file. Environmental Science and Pollution Research https://doi.org/10.1007/s11356-019-07472-1 WASTE AND BIOMASS MANAGEMENT & VALORIZATION Exploring the powerful phytoarsenal of white grape marc against bacteria and parasites causing significant diseases José-Luis Rodríguez Rama1 & Natalia Mallo 2 & Marco Biddau2 & Francisco Fernandes3 & Trinidad de Miguel1 & Lilach Sheiner2 & Altino Choupina3 & Marta Lores4 Received: 29 October 2019 /Accepted: 19 December 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2020 Abstract Natural extracts containing high polyphenolic concentration possess antibacterial, anti-parasitic and fungicidal activi- ties. The present research characterises two extracts based on white grape marc, a winemaking by-product, describing their physicochemical features and antimicrobial capacities. The main components of these extracts are phenolic acids, flavan-3-ols and their gallates and flavonols and their glycosides. As a result of this complex composition, the extracts showed pronounced bioactivities with potential uses in agricultural, pharmaceutical and cosmetic industries. Polyphenol compounds were extracted by using hydro-organic solvent mixtures from the by-product of Albariño white wines (Galicia, NW Spain) production. The in vitro antimicrobial activity of these extracts was evaluated on Gram- positive and Gram-negative bacteria and Apicomplexan and Oomycota parasites. Microbial species investigated are causing agents of several human and animal diseases, such as foodborne illnesses (Bacillus cereus, Escherichia coli, Salmonella enterica,andToxoplasma gondii), skin infections and/or mastitis (Staphylococcus aureus and Streptococcus uberis), malaria (Plasmodium falciparum) and plant infections as “chestnut ink” or “root rot” (Phytophthora cinnamomi). Both extracts showed activity against all the tested species, being nontoxic for the host. So, they could be used for the development of biocides to control a wide range of pathogenic agents and contribute to the enhancement of winemaking industry by-products. Keywords Antibacterial . Anti-parasitic . Enhancement of winemaking by-products . Grape marc . Natural extract . Polyphenols Introduction José Luis Rodríguez Rama and Natalia Mallo contributed equally to this work. Grapes are one of the largest fruit crops in the world. Responsible editor: Giovanni Benelli According to the Food and Agricultural Organization (FAO) of the United Nations, > 67 million tons of grapes are pro- * Trinidad de Miguel duced annually worldwide, and during the production of [email protected] wines, there is a big amount of the grapes that end up as by- products. Among the mentioned by-products, grape marc 1 Department of Microbiology and Parasitology, University of (peel, seeds and stems after wine production) constitutes a Santiago de Compostela, Santiago de Compostela, E-15782 A very non-expensive material with numerous interesting activ- Coruña, Spain ities due to its composition. That composition, in general, 2 Wellcome Centre for Integrative Parasitology. Department of depends on the variety of the grape, type of soil, climate and Infection, Immunity and Inflamation., University of Glasgow, 120 wine making techniques (Friedman 2014). University Place, Glasgow, UK Grape marc also contains several bioactive compounds 3 Department of Socioeconomical systems, I. Politécnico Bragança, which are different to those found in grapes and wine, opening 5300-253 Terras Trás-os-Montes, Portugal a new path for exploring its potential anti-pathogenic activity. 4 Department of Analytical Chemistry, Nutrition and Food Science, Activity of wine by-products against pathogenic bacteria, vi- Laboratory of Research and Development of Analytical Solutions (LIDSA), University of Santiago de Compostela, Santiago de rus, fungi toxins and parasites has been proved (Friedman Compostela, E-15782 A Coruña, Spain 2014). This fact, together with the interest risen in the last Environ Sci Pollut Res decades, about finding natural bioactive compounds against (Murphy et al. 2017; European Centre for Disease different diseases due to antimicrobial resistance among other Prevention and Control (ECDC) et al. 2017). On this issues, makes grape marc a good candidate to find new effec- way, the microbial species studied in the present work tive treatments and therapeutic strategies. Its composition is are involved in several diseases in humans and animals, very rich and complex. Some of the compounds included are such as foodborne illnesses (Bacillus cereus, Escherichia antioxidant phenolic compounds, which have been described coli, Salmonella enterica subsp. enterica), skin infections as potential agents against several pathogenic diseases. Such (Staphylococcus aureus) and mastitis (Streptococcus phenolic compounds are not well extracted into the wine dur- uberis). ing winemaking process, remaining in the grape marc, being Besides, human and animal parasite infections such as thus this by-product very rich in polyphenols (Beres et al. Malaria (Plasmodium falciparum) or Toxoplasmosis 2017;Friedman2014). (Toxoplasma gondii)havebeenconsidered.Plasmodium spe- An antioxidant agent is a molecule that delays, pre- cies causes complex diseases and constitutes a serious health vents or clears oxidative damage in a target cell problem around the world. The World Health Organization (Gutteridge and Halliwell 2010). They can act in biolog- estimated a number of 219 million people infected by ical systems by different mechanisms, including electron Plasmodium which was distributed in 87 countries, resulting donation (acting as reducing agents), metallic ion chela- to almost 500,000 deaths and a considerably large population tion (deleting potential free radicals), or by regulation of at risk of infection by this parasite in 2017 (World Health genic expression (Gutteridge and Halliwell 2010). This Organization, Malaria 2019). T. gondii is a protozoan parasite group of substances act at low concentrations and signif- belonging to the phyla Apicomplexa. It is the causing agent of icantly inhibit or retard the oxidative process while they toxoplasmosis, a zoonotic disease of worldwide distribution, are oxidized. Some examples of antioxidants are ascorbic which generates a significant problem on public health and on acid, uric acid and some polyphenols as resveratrol global economy. It is considered a high-risk zoonotic agent by (Zampelas and Micha 2015). Their employment as addi- the European Food Safety Authority (EFSA) (2019)withan tives is broadly distributed in industry field to delay, pre- estimated one third of the world’s population infected (Seeber vent or eliminate damage caused by oxidation. Recently, and Steinfelder 2016). some plant extracts have been reported to have good an- Last, to evaluate the potential of the Albariño extracts in tioxidant and antimicrobial properties due to their poly- plant infections, we chose Phytophthora cinnamomi an phenolic and protein compounds (Piscopo et al. 2019; oomycete species that causes known plant diseases as “chest- Tortora et al. 2019; Benabderrahmane et al. 2018; nut ink” in chestnuts (Castanea sativa Miller) causing a con- Benabderrahmane et al. 2019).Duetoitscomplexcom- siderable decline of this culture in Europe. P. cinnamomi is a position, containing antioxidant dietary fibre, as well as soil pathogen that has a wide range of hosts in several coun- extractable and non-extractable polyphenol content, grape tries and different climates. Since oomycetes have other path- marc extracts have a great potential to display extensive ogenicity mechanisms than fungi, they are not easily con- uses in agricultural, pharmaceutical and cosmetic indus- trolled by usual fungicides and often develop resistance tries among others (Bargiacchi et al. 2017;Plachaetal. against the rare anti-oomycete products available (Davison 2013;deORibeiroetal.2018; Tayengwa and Mapiye 2002; Judelson and Blanco 2005). 2018). The grape marc contains the following antioxida- Due to climate change and migration (Yan et al. 2016), tive polyphenolic categories: phenolic acids, flavonoids, among other factors, a large proportion of the population is lignans and stilbenes (Sagdic et al. 2011a). The health- at risk of infection with parasites and other infectious agents, promoting and disease-preventing benefits of different being, thus, the study of infectious diseases an emerging field types of grape polyphenols are well documented (Tauxe et al. 2010). Trying to find new treatments to these (Simões et al. 2009; Yadav et al. 2015). Phenolic acids, diseases becomes a relevant topic