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Antimicrobial Properties and Mechanism of Action of Some Plant Extracts Against Food Pathogens and Spoilage Microorganisms fmicb-09-01639 July 23, 2018 Time: 16:42 # 1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Directory of Open Access Journals ORIGINAL RESEARCH published: 24 July 2018 doi: 10.3389/fmicb.2018.01639 Antimicrobial Properties and Mechanism of Action of Some Plant Extracts Against Food Pathogens and Spoilage Microorganisms Faraja D. Gonelimali1,2†, Jiheng Lin3†, Wenhua Miao1, Jinghu Xuan1, Fedrick Charles1, Meiling Chen1* and Shaimaa R. Hatab1,4* 1 College of Food Science and Pharmaceutics, Zhejiang Ocean University, Zhoushan, China, 2 Department of Food Science and Technology, College of Agricultural Science and Fisheries Technology, University of Dar es Salaam, Dar es Salaam, Tanzania, 3 Zhoushan Institute of Food and Drug Inspection, Zhoushan, China, 4 Faculty of Environmental Agricultural Science, Arish University, North Sinai, Egypt This work aims to evaluate the antimicrobial potential of ethanolic and water extracts of roselle (Hibiscus sabdariffa), rosemary (Rosmarinus officinalis), clove (Syzygium aromaticum), and thyme (Thymus vulgaris) on some food pathogens and spoilage microorganisms. Agar well diffusion method has been used to Edited by: determine the antimicrobial activities and minimum inhibitory concentrations (MIC) of Fatih Ozogul, different plant extracts against Gram-positive bacteria (Bacillus cereus, Staphylococcus Çukurova University, Turkey aureus), Gram-negative bacteria (Escherichia coli, Salmonella enteritidis, Vibrio Reviewed by: parahaemolyticus, and Pseudomonas aeruginosa), and one fungus (Candida albicans). Abderrahmane Houicher, University of Laghouat, Algeria The extracts exhibited both antibacterial and antifungal activities against tested Mehmet Tolga Dincer, microorganisms. Ethanolic roselle extract showed significant antibacterial activity Ege University, Turkey (P < 0.05) against all tested bacterial strains, while no inhibitory effect on Candida *Correspondence: Meiling Chen albicans (CA) was observed. Only the ethanolic extracts of clove and thyme showed [email protected] antifungal effects against CA with inhibition zones ranging from 25.2 ± 1.4 to Shaimaa R. Hatab 15.8 ± 1.2 mm, respectively. Bacillus cereus (BC) appears to be the most sensitive strain [email protected] to the aqueous extract of clove with a MIC of 0.315%. To enhance our understanding †These authors have contributed equally to this work. of antimicrobial activity mechanism of plant extracts, the changes in internal pH (pHint), and membrane potential were measured in Staphylococcus aureus (SA) and Specialty section: Escherichia coli (EC) cells after exposure to the plant extracts. The results indicated This article was submitted to Food Microbiology, that the plant extracts significantly affected the cell membrane of Gram-positive and a section of the journal Gram-negative bacteria, as demonstrated by the decline in pHint as well as cell Frontiers in Microbiology membrane hyperpolarization. In conclusion, plant extracts are of great value as natural Received: 25 May 2018 Accepted: 02 July 2018 antimicrobials and can use safely as food preservatives. Published: 24 July 2018 Keywords: plant extract, ultrasound-assisted extraction, antimicrobial properties, internal pH (pHint), membrane Citation: potential, spoilage, pathogenic microorganism Gonelimali FD, Lin J, Miao W, Xuan J, Charles F, Chen M and Hatab SR (2018) Antimicrobial INTRODUCTION Properties and Mechanism of Action of Some Plant Extracts Against Food Globally, food spoilage caused by microorganisms still widely affects all types of food and causes Pathogens and Spoilage Microorganisms. food waste and loss, even in developed countries. It has been estimated that the yearly losses Front. Microbiol. 9:1639. of global food reach up to 40% due to various factors including spoilage by microorganisms doi: 10.3389/fmicb.2018.01639 (Gustavsson et al., 2011). Bacteria, yeast, and molds are the common types of microorganisms Frontiers in Microbiology| www.frontiersin.org 1 July 2018| Volume 9| Article 1639 fmicb-09-01639 July 23, 2018 Time: 16:42 # 2 Gonelimali et al. Antimicrobial Mechanism of Plant Extracts responsible for the spoilage of a considerable number of food and (Thymus vulgaris) against seven common food pathogens and food products (Lianou et al., 2016). Once these microorganisms spoilage microorganisms, (3) to understand the mechanisms reach food products, they grow by utilizing the nutrients and of action of tested plant extracts with respect to the potential produce metabolites that cause food spoilage (Parlapani et al., disruption in the membrane of microorganisms and changes in 2017). Foodborne disease is another pervasive food safety cytoplasmic pH (pHint). problem caused by consumption of contaminated food products, which has been a significant safety concern to public health (Azziz-Baumgartner et al., 2005; Kirk et al., 2017). MATERIALS AND METHODS Microorganisms are available naturally in the surrounding environment; therefore they can easily reach food during Extraction harvesting, slaughtering, processing, and packaging (Hatab In this work, four plants were selected based on their traditional et al., 2016). These microorganisms can survive under adverse usage as folk medicine. The plants were purchased, in dried form, conditions used in the food preservation such as low temperature, from the local market in Zhoushan, China. Table 1 shown the modified atmosphere packaging, vacuum packaging, as well plant species and the parts evaluated in this study. Two solvents as resist conventional pasteurization (Dimitrijevic´ et al., 2007; (water and ethanol), and two extraction methods (conventional Provincial et al., 2013; Saraiva et al., 2016; Säde et al., 2017). Thus, extraction and ultrasound techniques) were used to evaluate their there is a considerable concern among consumers regarding effect on the extraction yield. the risk of using synthetic additives for human health, that For conventional extraction, 20 g powder of each tested plant led to decrease the use of these chemicals in food preservation material (Table 1) was soaked in 180 ml of distilled water in (Gyawali and Ibrahim, 2014; Caleja et al., 2016; Kalem et al., a round bottom flask and heated for 30 min at 90◦C, before 2017). Therefore, new eco-friendly methodologies are required the overnight incubation at 37◦C, and 150 rpm in a shaking to reduce the growth of pathogenic bacteria and prolong the incubator (Xu et al., 2008). Similarly, 10 g powder of each tested shelf-life of food products, without using chemical preservatives. plant material was mixed with ethanol (9:1) separately in round Recently, many researchers investigated the possible utilization of bottom flasks and incubated at 37◦C and 150 rpm for overnight. some plant extracts as effective natural preservatives (Fernández- Liquid extracts obtained were separated from the solid residue López et al., 2005; Suppakul et al., 2016; Clarke et al., 2017). by filtration using Whatman No. 1 filter, and then concentrated Traditionally, the crude extracts of different parts of medical using a rotary evaporator (EYELA N-1100, China). plants, including root, stem, flower, fruit, and twigs, were widely For ultrasound techniques, 10 g powder of each tested plant used for treatments of some human diseases (Khan et al., material was mixed with 180 ml of distilled water, or ethanol (9:1) 2013). Medicinal plants contain several phytochemicals such separately in beakers. Each beaker was placed in an ultrasonic as flavonoids, alkaloids, tannins, and terpenoids, which possess bath (KUDOS, SK8210HP, China) for 30 min at 53 kHz. antimicrobial and antioxidant properties (Talib and Mahasneh, Afterward, the two beakers were transferred to incubator shaker 2010). The antimicrobial activities of some plant species have and kept for overnight at 37◦C and 150 rpm. The supernatant been widely researched. For example, the crude extracts of was similarly processed as described in conventional extraction cinnamon, garlic, basil, curry, ginger, sage, mustard, and other to get dried extracts of selected plants as described by (Dhanani herbs exhibit antimicrobial properties against a wide range et al., 2017). Dried extracts were dissolved in 10% DMSO for of Gram-positive and Gram-negative bacteria (Alzoreky and ethanolic extracts or in distal water for water extracts (Gurnani Nakahara, 2003; Castro et al., 2008). In addition, it has been et al., 2016). The final concentration of different extracts was reported that the extracts from Chinese chives and cassia can 20% w/v. The crude extract was then stored at −20◦C for further effectively reduce the growth of Escherichia coli and other bacteria study. The extraction yield of selected plants has been calculated during storage of meat, juices, and milk (Mau et al., 2001). In a by the following equation (Felhi et al., 2017): similar study, Doddanna et al.(2013) investigated the effect of ∗ some plant extracts on the growth of Candida albicans, the results Yield.%/ D .X1 100/=X0 indicated that the alcoholic extract of curry leaves effectively inhibit the growth of C. albicans with 24.05 ± 0.07 after 48 h. Where X1 refers to the weight of extract after evaporation of Moreover, Nzeako et al.(2006) reported that thyme oil extract solvent and X0 refers to the dry weight of the plant powder before could decrease the growth of C. albicans and Pseudomonas extraction. aeruginosa. The understanding of the mechanism of antimicrobial action Preparation of Inoculum of medicinal plants extracts
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