Antibacterial mechanism of the action of Enteromorpha linza L. essential oil against Escherichia coli and Salmonella Typhimurium
© Patra et al.; licensee Springer. 2015
Received: 10 February 2015
Accepted: 14 May 2015
Published: 23 May 2015
Identification of natural antibacterial agents from various sources that can act effectively against disease causing foodborne bacteria is one of the major concerns throughout the world. However, the natural antibacterial agents identified to date are primarily effective against Gram positive bacteria, but less effective against Gram negative bacteria. In the present study, Enteromorpha linza L. essential oil (EEO) was evaluated for antibacterial activity against Escherichia coli and Salmonella Typhimurium along with the mode of their antibacterial action.
The chemical composition of EEO revealed high amounts of acids (54.6 %) and alkenes (21.1 %). EEO was effective against both E. coli and S. Typhimurium. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) values of EEO for both pathogens were 12.5 mg/ml and 25.0 mg/mL, respectively. EEO at the MIC acted on the loss in viability of E. coli ATCC 43890, which was used as the model system for evaluation of the antibacterial mode of action of EEO against Gram negative bacteria. Significant increase in relative electrical conductivity and K+ concentration were recorded with respect to time, indicating the disruption of tested E. coli cells owing to the controlling effect of EEO. Alternation of the morphology of the cell surface, increase in the release of 260 nm absorbing materials and loss of high salt tolerance were observed.
The results suggest that EEO induced a bactericidal effect via structural membrane damage caused by deposition of EEO in the cytosol or through enzymatic degradation of bacterial intracellular enzymes that resulted in cellular lysis. Accordingly, EEO can be used as a strong natural antibacterial agent against Gram negative foodborne pathogens such as E. coli and S. Typhimurium.
KeywordsCell membrane Enteromorpha linza Escherichia coli Essential oil Salmonella Typhimurium Seaweed
Foodstuffs of animal and plant origin along with sea products are always subjected to spoilage and decaying phenomena that occur due to various microorganisms, mainly bacteria (Kim et al. ; Faid ). These phenomena often lead to heavy loss of food products and raw materials, ultimately resulting in health problems caused by the occurrence of food poisoning and infections (Kim et al. ). Contamination of food by different types of microorganisms is a matter of great concern for this world with increasing human population day by day (Acharya et al. ). Various foodborne microorganisms negatively affect food via two possible pathway, direct growth in food products and the release of microbial toxins while handling the food before processing. However, it is always difficult to find solutions to control food contamination.
The use of chemicals to protect meat, fruits, vegetables and drinks can be harmful to human health and the environment (Acharya et al. ; Khwaldia ). However, the application of chemical antimicrobials has been approved by different medical authorities worldwide to maintain food security. Owing to increased awareness, the use of synthetic chemicals has been rejected by consumers because of their adverse side effects that in many cases led to deadly diseases (Goni et al. ). As a result, the demand for natural preservatives in food has increased, leading many food industries to search for natural antimicrobial agents for use in packaging and preservation. Indeed, the demand for natural antimicrobial agents is high as they are more effective and generally recognized as safe (GRAS) (Acharya et al. ).
More than 150,000 algae and seaweed species exist in the ocean, many of which possess components with antibacterial, antifungal and antiviral properties (Salvador et al. ; Souhaili et al. ; Lategan et al. ; Plaza et al. ; Faid ). Several chemical compounds from marine seaweeds such as agar, carrageenan, alginates and pigments like beta carotene have been used widely in food industries and pharmacology. Marine algae/seaweeds have become a part of the human diet in many countries, and many ingredients from these seaweeds have also being used in drinks, snacks, soups and beverages (Faid ). Various natural antimicrobial agents that have the potential for food processing and preservation are effective against Gram positive foodborne bacteria, but they are very less effective and sometimes not effective against the Gram negative foodborne bacteria (Trombetta et al. ; Bassole and Juliani ; Sfeir et al. ; Nazzaro et al. ).
Enteromorpha linza (L.) is a common edible seaweed that is abundant in coastal areas of Asian and European countries (Say et al. ) and consumed as food by people worldwide (Demirel et al. ). Therefore, in this study, we evaluated the antibacterial potential of essential oil extracted from E. linza against two dominant Gram negative foodborne pathogenic bacteria, Escherichia coli and Salmonella Typhimurium, as well as its mode of antibacterial action.
Extraction of essential oil from E. linza
Fresh seaweed (E. linza L.) was purchased from a local market at Gyeongsan, Republic of Korea, washed thoroughly and put into a specially designed glass container. Five liters of water were then added to a glass container containing 500 g seaweed and subjected to hydro-distillation to extract essential oils using a micro-wave assisted extraction machine manufactured by KMD Engineering (Paju, Republic of Korea) for 4 h. The temperature of the chamber was maintained by a thermo controller (oven power capacity of 40 W and frequency of 15 gkH). Approximately 500 mL of the distillate was then collected from the collecting nozzle of the apparatus with a conical flask, mixed with an equal volume of dichloromethane in a separating funnel, vigorously shaken, and allowed to stand until the two layers separated. Next, the lower layer was taken and concentrated using a rotary evaporator (N-1110, Eyela, Tokyo Rikakikai Co., Ltd., Japan) at 40 °C. The extracted E. linza L. essential oil (EEO) was then kept in a tightly closed vial at 4 °C until further use.
Chemical analysis of EEO
A detailed analysis of the chemical composition of EEO was conducted using a gas chromatography–mass spectrometry system (JMS 700 Mstation, Jeol Ltd., Japan) equipped with an Agilent 6890 N GC DB-5 MS fused silica capillary column (Agilent Technologies, Santa Clara, USA) according to the method described by Patra et al. ().
Determination of antibacterial activity of EEO
The antibacterial potential of EEO was evaluated against four foodborne bacteria belonging to two species, S. Typhimurium ATCC 19586 and ATCC 43174 and E. coli ATCC 43889 and ATCC 43890. The pathogens were obtained from the American Type Culture Collection (ATCC, Manassas, VA, USA). Prior to use, EEO was diluted two times in 5 % dimethylsulphoxide (DMSO), then filter-sterilized using a 0.22 μm micro syringe filter (Chemco Scientific, Chungbuk, Republic of Korea). The standard disc diffusion method described by Diao et al. () was employed to evaluate the antibacterial activity of EEO. EEO and rifampicin (Duchefa Biochemie, Haarlem, The Netherlands) at 25 mg/disc and at 20 μg/disc, respectively, were used as the test sample and the positive control, while 5 % DMSO was used as the negative control. The inhibition zone was measured in mm for each pathogen.
The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of EEO against the four pathogens was determined by the two-fold dilution method described by Kubo et al. (), with slight modification. The lowest concentration of EEO without any visible growth of test organism was taken as the MIC value, and the concentration not showing any growth of bacterial colony on nutrient agar (NA) was selected as the MBC. Both the MIC and MBC were expressed in mg/mL. All experiments were repeated three times.
Effect of EEO on the viability of E. coli
The effects of EEO on the viability of Gram negative foodborne bacteria were investigated according to the procedure described by Joray et al. (). Only one foodborne bacterium, E. coli ATCC 43890, was selected as the model organism for all the subsequent assays. Overnight grown bacterial culture treated with EEO at the MIC served as the treatment, while those treated with 5 % DMSO served as the control. Both treatment and control samples were incubated at 37 °C for 8 h, during which time samples were collected every 2 h, appropriately diluted in phosphate buffer saline, spread on the surface of NA plates and incubated further at 37 °C for 24 h. After incubation, the number of bacterial colonies in terms of colony forming unit (cfu) was determined by multiplying it with the appropriate dilution factor. The results were expressed in terms of log10 (cfu/mL).
Effect of EEO on surface morphology of E. coli
The effects EEO treatment on the morphology of E. coli ATCC 43890 were determined by scanning electron microscopy (SEM). Both a control treated with 5 % DMSO and sample treated with EEO were prepared according to the procedure described by Bajpai et al. (). The specimens were then sputter-coated with platinum in an ion coater for 120 s and observed under SEM (S-4100, Hitachi, Japan).
Effect of EEO on cell membrane permeability of E. coli
where, L0 was the electrical conductivity of the bacteria in 5 % glucose killed by being treated in boiling water for 5 min, L1 was the electrical conductivity of the bacteria in 5 % glucose with the EEO at the MIC and L2 was the electrical conductivity of the EEO-bacteria mixtures in 5 % glucose collected at 2 h intervals during 8 h of incubation.
Effect of EEO on E. coli cell membrane integrity
The effect of EEO on the cell membrane integrity of E. coli ATCC 43890 were measured by the standard procedure described by Carson et al. (). Both the control treated with DMSO and the sample treated with EEO at the MIC were incubated at 37 °C. After 60 and 120 min, samples were centrifuged at 3500 rpm for 10 min and the absorbance of the supernatant at 260 nm was measured using a spectrophotometer (ASP 3700, ACTGene Inc., NJ, USA).
Effect of EEO on the leakage of potassium ion from E. coli
The leakage of potassium ion (K+) in the suspension culture of E. coli ATCC 43890 treated with EEO at the MIC was measured according to the method described by Lee et al. () using a Kalium/Potassium kit (Quantofix, Macherey-Nagel GmbH & Co., Germany). All measurements were carried at 2 h time intervals during 8 h of incubation and expressed as the amount of free K+ ion (mg/L) in the bacterial suspension at each time interval. Bacterial culture treated with DMSO was used as a control.
Effect of EEO on salt tolerance capacity of E. coli
The effect of EEO on the salt tolerance capacity of E. coli ATCC 43890 were determined by growing the bacterial cultures on NA plates supplemented with different concentrations of NaCl (0, 2.5, 5.0 and 10.0 %) (Miksusanti et al. ). Bacterial cultures amended with 5 % DMSO and EEO at the MIC were plated on NA plates and incubated at 37 °C for 24 h. After determining the CFU, the results were expressed in terms of Log10 (cfu/mL).
The results of all experiments were expressed as the mean ± standard deviation (SD). Statistical analyses consisted of one way ANOVA and Duncan’s multiple range tests, with P < 0.05 considered to indicate significance. Statistical Analysis Software (SAS) version 9.4 (SAS Inc., Cary, USA) was used for all analyses.
Results and discussion
For years, pathogenic bacteria have been known to be the primary cause of foodborne illness and food poisoning throughout the world (Kim et al. ). The use of natural antibacterial agents in food processing and food preservation has played a vital role in controlling the adverse effect of bacteria in food. However, the natural antibacterial agents currently used as preservatives are primarily effective against Gram positive foodborne pathogens, whereas they are not much effective against the Gram negative foodborne pathogens (Trombetta et al. ; Bassole and Juliani ; Sfeir et al. ; Nazzaro et al. ). The reason for the failure of most natural antibacterial agents against Gram negative pathogens is that they are unable to penetrate the strong cell wall of a Gram negative bacterium and thus do not affect it (Trombetta et al. ).
There have been many reports of the bioactive potential of marine algae and seaweeds, and many novel compounds have been isolated from them (Kamat et al. ; Crasta et al. ; Bhosale et al. ; Salvador et al. ; Lategan et al. ; Patra et al. ; Plaza et al. ). However, there have been limited reports on the extraction and evaluation of bioactive potential of essential oils from marine algae and seaweeds on antibacterial capacity. In this study, we evaluated the marine resource E. linze as a source of essential oil for use as a strong antibacterial agent that can efficiently control against the Gram negative bacteria E. coli and S. Typhimurium.
Percentage composition of functional groups present in Enteromorpha linza essential oil
Efficacy of Enteromorpha linza essential oil (EEO) against four strains of the two Gram negative foodborne pathogens, E. coli and S. Typhimurium
Foodborne bacterial pathogen
Zone of inhibition (mm)
E. coli ATCC 43889
13.33 ± 0.58a
32.33 ± 1.52a
E. coli ATCC 43890
10.00 ± 0.00b
32.66 ± 0.57a
S. Typhimurium ATCC 19586
10.66 ± 1.15ab
21.50 ± 4.94b
S. Typhimurium ATCC 43174
10.66 ± 0.57ab
31.66 ± 2.08a
MIC and MBC values of Enteromorpha linza essential oil against four strains of two Gram negative foodborne pathogens
Foodborne bacterial pathogen
E. coli ATCC 43889
E. coli ATCC 43890
S. Typhimurium ATCC 19586
S. Typhimurium ATCC 43174
Only a few studies have investigated the antibacterial effects of algal essential oil on pathogenic bacteria (Koz et al. ; Demirel et al. ; Gressler et al. ). However, the results of the present study clearly demonstrated that EEO exerted antibacterial effects on Gram negative bacteria. The outer membrane of Gram negative bacteria is always impermeable to various antibacterial agents owing to their strong lipolysaccharide molecules (Bezic et al. ; Sharma et al. ). In this study, however, the positive results of antibacterial activity of EEO against the two Gram negative bacteria suggested an hypothesis that, although essential oil is hydrophobic in nature, it might have slowly entered into the bacterial cell through the general bacterial porins owing to its small size, after which it might have affected the bacterial enzymes, causing cellular lysis and death (Nikaido ; Kotzekidou et al. ). The antibacterial activity of the EEO against the tested pathogenic bacteria might be due to the presence of various active compounds such as n-hexanal, 2-chloro-5-methyl-4-(2-thienyl) pyrimidine, tetradecanoic acid, pentadecanoic acid, (z,z)-6,9-cis-3,4-epoxy-nonadecadiene, 13-octadecenal and azetidine in the EEO that might have individually of synergistically altogether inhibited the growth of the pathogenic bacteria.
The increase in the relative electrical conductivity, leakage of 260 nm absorbing materials and leakage of K+ ions to the incubating culture indicated that EEO after being escaped into the bacterial cells through the general porins might have been accumulated in the cytosol, resulting in loss of plasma membrane integrity. This caused the cells to become permeable to protons and ions from outside, which eventually caused cellular lysis and cell death (Bajpai et al. ). The loss of 260 nm absorbing materials along with the leakage of K+ ions to the outside of the bacteria might have been due to the structural damage caused by the action of EEO (Cox et al. ). In addition, the loss of membrane permeability, release of 260 nm absorbing material, and leakage of K+ ions to the outside can be sensitive indicators of the disruption of membrane integrity (Cox et al. ). Any type of minor changes to the structural integrity of the cell membrane could adversely affect the normal metabolic functioning of the bacterial cell and result in complete lysis (Hugo and Snow ; Davidson and Branen ).
EEO from the edible marine seaweed E. linza was found to have a potential inhibitory effect on two Gram negative foodborne bacteria. This effect of EEO was associated with its ability to disrupt the bacterial membrane and probably the bacterial enzymes by accumulation inside the cytosol, causing loss of membrane integrity and leakage of 260 nm absorbing material along with K+ ions. Since EEO is extracted from the edible seaweed widely available around the coastal belt of many countries worldwide, it can be an inexpensive but valuable source of natural mixtures of antibacterial compounds that exhibit the potential for use in food systems. EEO could prevent the growth of foodborne bacteria, particularly Gram negative bacteria, and extend the shelf life of the processed food.
Jayanta Kumar Patra and Gitishree Das were the combined first authors to the manuscript.
This work was supported by a grant from the Systems and Synthetic Agro-biotech Center through the Next-Generation BioGreen 21 Program (PJ011117012015), Rural Development Administration, Korea.
- Acharya D, Rios JL, Rai M: Naturally occurring biocides in the food industry. In Natural antimicrobials in food safety and quality. Edited by: Rai M, Chikindas M. CAB International, United Kingdom; 2011.Google Scholar
- Agoramoorthy G, Chandrasekaran M, Venkatesalu V, Hsu MJ: Antibacterial and antifungal activities of fatty acid methyl esters of the blind-your-eye mangrove from India. Braz J Microbiol 2007, 38: 739–42. 10.1590/S1517-83822007000400028View ArticleGoogle Scholar
- Bajpai VK, Al-reza SM, Choi UK, Lee JH, Kang SC: Chemical composition, antibacterial and antioxidant activities of leaf essential oil and extracts of Metaseqoia glyptostroboides Miki ex Hu. Food Chem Toxicol 2009, 47: 1876–83. 10.1016/j.fct.2009.04.043View ArticlePubMedGoogle Scholar
- Bajpai VK, Sharma A, Baek KH: Antibacterial mechanism of action of Texus cuspidate stem essential oil against selected foodborne pathogens. J Food Safety 2013, 33: 348–59. 10.1111/jfs.12059View ArticleGoogle Scholar
- Bassole IHN, Juliani HR: Essential oils in combination and their antimicrobial properties. Molecules 2012, 17: 3989–4006. 10.3390/molecules17043989View ArticlePubMedGoogle Scholar
- Bezic N, Skocibusic M, Dinkic V, Radonic A: Composition and antimicrobial activity of Achillea clavennae L. essential oil. Phytother Res 2003, 17: 1037–40. 10.1002/ptr.1290View ArticlePubMedGoogle Scholar
- Bhosale SH, Nagle VI, Jagtap TG: Antifouling potential of some marine organisms from Indian species of Bacillus and Pseudomonas . Marine Biotechnol 2002, 4: 111–8. 10.1007/s10126-001-0087-1View ArticleGoogle Scholar
- Carson CF, Mee BJ, Riley TV: Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob Agent Chemother 2002, 46: 1914–20. 10.1128/AAC.46.6.1914-1920.2002View ArticleGoogle Scholar
- Cox SD, Mann CM, Markhan JL, Gustafson JE, Warmington JR, Wyllie SG: Determining the antimicrobial action of tea tree oil. Molecules 2001, 6: 87–91. 10.3390/60100087View ArticleGoogle Scholar
- Crasta PJ, Raviraja NS, Sridhar KR: Antimicrobial activity of some marine algae of southwest coast of India. Indian J Marine Sci 1997, 26: 201–5.Google Scholar
- Davidson PM, Branen AL: Food antimicrobials - an introduction. In Antimicrobial in food. Edited by: Davidson PM, Sofos JN, Branen AL. CRC Press, Boca Raton, FL; 2005. 10.1201/9781420028737Google Scholar
- Deep A, Phogat P, Kumar M, Kakkar S, Mittal SK, Malhotra M: New tetradecanoic acid hydrazones in the search for antifungal agents: synthesis and in vitro evaluations. Acta Poloniae Pharmaceut Drug Res 2012, 69: 129–33.Google Scholar
- Demirel Z, Yilmaz-Koz FF, Karabay-Yavasoglu NU, Ozdemir G, Sukatar A: Antimicrobial and antioxidant activities of solvent extracts and the essential oil composition of Laurencia obtusa and Laurencia obtusa var. pyramidata . Romanian Biotechnol Lett 2011, 16: 5927–36.Google Scholar
- Diao WR, Hu QP, Feng SS, Li WQ, Xu JG: Chemical composition and antibacterial activity of the essential oil from green huajiao ( Zanthoxylum schinifolium ) against selected foodborne pathogens. J Agric Food Chem 2013, 61: 6044–9. 10.1021/jf4007856View ArticlePubMedGoogle Scholar
- Faid M: Antimicrobials from marine algae. In Natural antimicrobials in food safety and quality. Edited by: Rai M, Chikindas M. CAB international, United Kingdom; 2011.Google Scholar
- Ghannoum MA: Studies on the anticandidal mode of action of Allium sativum (garlic). J Gen Microbiol 1988, 134: 2917–24.PubMedGoogle Scholar
- Goni P, Lopez P, Sanchez C, Gomez-Lus R, Becerril R, Nerin C: Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chem 2009, 116: 982–9. 10.1016/j.foodchem.2009.03.058View ArticleGoogle Scholar
- Gressler V, Stein EM, Dorr F, Fujii MT, Colepicolo P, Pinto E: Sesquiterpenes from the essential oil of Laurencia dendroidea (Ceramiales, Rhodophyta): isolation, biological activities and distribution among seaweeds. Brazilian J Pharmacog 2011, 21: 248–54.Google Scholar
- Gutierrez A, Rio JCD, Martinez-Inigo MJ, Martinez MJ, Martinez AT: Production of new unsaturated lipids during wood decay by Ligninolytic basidiomycetes . Appl Environ Microbiol 2002, 68: 1344–50. 10.1128/AEM.68.3.1344-1350.2002PubMed CentralView ArticlePubMedGoogle Scholar
- Hugo W, Snow G: Biochemistry of antibacterial action. Chapman & Hall, London; 1981.Google Scholar
- Jemaa JMB: Essential oil as a source of bioactive constituents for the control of insect pests of economic importance in Tunisia. Med Aromatic Plants 2014, 3: 1–7.Google Scholar
- Joray MB, del-Rollan MR, Ruiz GM, Palacios SM, Carpinella MC: Antibacterial activity of extracts from plants of central Argentina- isolation of an active principle from Achyrocline satureioides . Plant Med 2011, 77: 95–100. 10.1055/s-0030-1250133View ArticleGoogle Scholar
- Kamat SY, Wahidulla S, D’Souza L, Naik CG, Ambiye V, Bhakuni DS, et al.: Bioactivity of marine organisms-Vl. Antiviral evaluation of marine algal extracts from the Indian coast. Bot Mar 1992, 35: 161–4. 10.1515/botm.19184.108.40.206View ArticleGoogle Scholar
- Khwaldia K: Antimicrobial films and coatings from milk proteins. In Natural antimicrobials in food safety and quality. Edited by: Rai M, Chikindas M. CAB International, United Kingdom; 2011.Google Scholar
- Kim J, Marshall MR, Wei C: Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem 1995, 43: 2839–45. 10.1021/jf00059a013View ArticleGoogle Scholar
- Kong M, Chen XG, Liu CS, Meng XH, Yu LJ: Antibacterial mechanism of chitosan microspheres in a solid dispersing system against E. coli . Colloid Surface B 2008, 65: 197–202. 10.1016/j.colsurfb.2008.04.003View ArticleGoogle Scholar
- Kotzekidou P, Giannakidis P, Boulamatsis A: Antimicrobial activity of some plant extracts and essential oils against foodborne pathogens in vitro and on the fate of inoculated pathogens in chocolate. LWT- Food Sci Technol 2008, 41: 119–27. 10.1016/j.lwt.2007.01.016View ArticleGoogle Scholar
- Koz FFY, Yavasoglu NUK, Demirel Z, Sukatar A, Ozdemir G: Antioxidant and antimicrobial activities of Codium fragile (Suringar) Hariot (Chlorophyta) essential oil and extracts. Asian J Chem 2009, 21: 1197–209.Google Scholar
- Kubo I, Fujita K, Kubo A, Nihei K, Ogura T: Antibacterial activity of coriander volatile compounds against Salmonella choleraesuis . J Agric Food Chem 2004, 52: 3329–32. 10.1021/jf0354186View ArticlePubMedGoogle Scholar
- Lategan C, Kellerman T, Afolayan AF, Mann MG, Antunes EM, Smith PJ, et al.: Antiplasmodial and antimicrobial activities of South African marine algal extracts. Pharm Biol 2009, 47: 408–13. 10.1080/13880200902758832View ArticleGoogle Scholar
- Lee JY, Kim YS, Shin DH: Antimicrobial synergistic effect of linolenic acid and monoglyceride against Bacillus cereus and Staphylococcus aureus . J Agric Food Chem 2002, 50: 2193–9. 10.1021/jf011175aView ArticlePubMedGoogle Scholar
- Miksusanti JB, Priosoeryanto B, Syarief R, Rekso G: Mode of action Temu kunci ( Kaempferia pandurata ) essential oil on E. coli K1.1 cell determined by leakage of material cell and salt tolerance assays. Hayati J Biosci 2008, 15: 56–60.Google Scholar
- Nazzaro F, Fratianni F, Martina LD, Coppola R, De-Feo V: Effect of essential oils on pathogenic bacteria. Pharmaceuticals 2013, 6: 1451–74. 10.3390/ph6121451PubMed CentralView ArticlePubMedGoogle Scholar
- Nikaido H: Outer membrane. In Escherichia coli and Salmonella: cellular and molecular biology. Edited by: Neidhardt FC. ASM Press, Washington, DC; 1996.Google Scholar
- Patra JK, Kim SH, Baek KH: Antioxidant and free radical scavenging potential of essential oil from Enteromorpha linza L. prepared by microwave assisted hydrodistillation. J Food Biochem 2015, 39: 80–90. 10.1111/jfbc.12110View ArticleGoogle Scholar
- Patra JK, Patra AP, Mohapatra NK, Das S, Thatoi H, Sahu RK, et al.: Biomolecular constituents and antibacterial activity of some marine algae from Chilika Lake (Orissa, India). Int J Algae 2009, 11: 222–35. 10.1615/InterJAlgae.v11.i3.30View ArticleGoogle Scholar
- Plaza M, Santoyo S, Jaime L, Garcia-Blairsy Reina G, Herrero M, Senorans MJ, et al.: Screening for bioactive compounds from algae. J Pharma Biomed Anal 2010, 51: 450–5. 10.1016/j.jpba.2009.03.016View ArticleGoogle Scholar
- Salvador N, Garreta AG, Lavelli L, Ribera MA: Antimicrobial activity of Iberian macroalgae. Scientia Marina 2007, 71: 101–13. 10.3989/scimar.2007.71n1101View ArticleGoogle Scholar
- Say PJ, Burrows IG, Whitton BA: Enteromorpha as a monitor of heavy metals in estuarine and coastal intertidal waters: A method for the sampling, treatment and analysis of the seaweed Enteromorpha to monitor heavy metals in estuaries and coastal waters. Northern Environmental Consultants Ltd, Durham DH8 6SS, UK; 1986.Google Scholar
- Sfeir J, Lefrancois C, Baudoux D, Derbre S, Licznar P: In vitro antibacterial activity of essential oils against Streptococcus pyogenes . Evid based Complement Altern Med 2013, 2013: 1–9. 10.1155/2013/269161View ArticleGoogle Scholar
- Sharma A, Bajpai VK, Baek KH: Determination of antibacterial mode of action of Allium sativum essential oil against foodborne Pathogens using membrane permeability and Surface characteristic parameters. J Food Safety 2013, 33: 197–208. 10.1111/jfs.12040View ArticleGoogle Scholar
- Sharma V, Chitranshi N, Agarwal AK: Significance and biological importance of pyrimidine in the microbial world. Int J Med Chem 2014, 2014: 1–31.Google Scholar
- Souhaili Z, Mohammadi H, Habti N, Faid M: Lethal effect of the aqueous extract of the brown marine algae ( Cystoseira tamariscifolia ) on the mouse and the myelom cells. Afrique Sci 2008, 4: 580–90.Google Scholar
- Trombetta D, Castelli F, Sarpietro MG, Venuti V, Cristani M, Daniele C, et al.: Mechanisms of antibacterial action of three monoterpenes. Antimicrob Agents Chemother 2005, 49: 2474–8. 10.1128/AAC.49.6.2474-2478.2005PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.