Inhibition of Pathogenic Bacteria Isolated from Nuts and Seeds by Natural and Commercial Coumarins

(Munirah Fahad Aldayel)

---

Abstract

The antibacterial potential of a natural coumarin compound that was extracted from the root of Lotus lalambensis Schweinf and several commercial coumarin compounds (herniarin, xanthotoxin, umbelliferone and scopoletin) were investigated against five pathogenic bacteria (Staphylococcus epidermidis, Bacillus mycoides, Escherichia coli, Staphylococcus aureus and Bacillus cereus) that were isolated from different nut products. The natural coumarin showed the best antibacterial potential against the most sensitive bacteria (Staphylococcus aureus and Bacillus cereus) with a minimum inhibitory concentration of 62.5 μg ml-1. The antibacterial mechanism of different coumarin compounds was investigated by assessing the effect of coumarin on the membrane potential to quantify the alkaline phosphatase and lactate dehydrogenase activities of tested bacteria. The membrane potential of Staphylococcus aureus was higher in natural coumarin than in the control and commercial coumarin, followed by Bacillus cereus. The concentration of extracellular protein and the activity of lactate dehydrogenase and alkaline phosphtase were evaluated, and the bacteria that was treated with the natural coumarin had the highest antibacterial activity. The results showed the significant potential of coumarin in isolated DNA cleavage reactions. Our data also showed that the addition of natural coumarin and commercial coumarins resulted in a higher discharge of membrane potential in the supernatant. The conclusion revealed that the natural coumarin of Lotus lalambensis is potentially a significant source of useful molecules for the expansion of new antibacterial agents and the promising manipulation of natural coumarin to protect contaminated nuts and other foods against the pathogenic bacteria.

KEYWORDS
Lotus lalambensis schweinf, staphylococcus epidermidis and staphylococcus aureus

PDF

References

A Hood, M., E Ness, G. and J Blake, N. (1983). Relationship among fecal coliforms, Escherichia coli, and Salmonella spp. in shellfish. Applied and Environmental Microbiology, 45(1), 122–6. 
Al-Moghazy, M., Boveri, S. and Pulvirenti, A. (2014). Microbiological safety in pistachios and pistachio containing products. Food Control, 36(1) ,88–93.
Al-Rifai, A.a.A., Ayoub, M.T., Shakya, A.K., Abu Safieh, K.A. and Mubarak, M.S. (2012). Synthesis, characterization, and antimicrobial activity of some new coumarin derivatives. Medicinal Chemistry Research, 21(4), 468–76.
Alice, C.B., Vargas, VM., Silva, GA., de Siqueira, NC., Schapoval, EE., Gleye, J., Henriques, JA. and Henriques, AT. (1991). Screening of plants used in south Brazilian folk medicine. Journal of Ethnopharmacology, 35(2), 165–71.
Arokiyaraj, S.,  Choi, S.H., Lee, Y., Bharanidharan, R., Hairul-Islam, VI., Vijayakumar, B., Oh, YK., Dinesh-Kumar, V., Vincent, S. and Kim, KH. (2014). Characterization of ambrette seed oil and its mode of action in bacteria. Molecules, 20(1), 384–95.
Arshad, A.,  Osman, H., Bagley, M., KitLam ,C., Mohamad, S.  and Mohd Zahariluddin, A. (2011). Synthesis and antimicrobial properties of some new thiazolyl coumarin derivatives. Eur J Med Chem, 46(9), 3788–94.
Basanagouda, M., Shivashankar, K.,  V.Kulkarni, M., Vijaykumar, P., Harishch,R., Sumit, S., Mutha, S. and  Mohite, A . (2010). Synthesis and antimicrobial studies on novel sulfonamides containing 4-azidomethyl coumarin. Eur J Med Chem, 45(3), 1151–7.
Beuchat, L.R., Komitopoulou, E., Beckers, H., Betts, RP., Bourdichon, F., Fanning, S., Joosten, HM. and Ter, Kuile BH. (2013). Low-water activity foods: increased concern as vehicles of foodborne pathogens. J Food Prot, 76(1), 150–72.
Beuchat, L.R. and Mann, D.A. (2010). Factors affecting infiltration and survival of Salmonella on in-shell pecans and pecan nutmeats. J Food Prot, 73(7), 1257–68.
Beuchat, L.R. and Mann, D.A. (2011). Inactivation of Salmonella on in-shell pecans during conditioning treatments preceding cracking and shelling. J Food Prot, 74(4), 588–602.
Beuchat, L.R. and Scouten, A.J. (2002). Combined effects of water activity, temperature and chemical treatments on the survival of Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J Appl Microbiol, 92(3), 382–95.
Bhat, R. and Siruguri, V. (2003). Mycotoxin food safety risk in developing countries. Food Safety in Food Security and Food Trade, 10(3), 1–2.
Blessington, T., Theofel, C. and Harris, L. (2013). A dry-inoculation method for nut kernels. Food Microbiology, 33(2), 292–7.
Brar, P.K., Proano, L.G., Friedrich, L.M., Harris, L.J. and Danyluk, M.D. (2015). Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on raw peanut and pecan kernels stored at -24, 4, and 22 degrees C. J Food Prot, 78(2), 323–32.
Curini, M., Epifano, F., Maltese, F., Marcotullio, MC., Tubaro, A., Altinier, G., Gonzales, SP. and Rodriguez, JC. (2004). Synthesis and anti-inflammatory activity of natural and semisynthetic geranyloxycoumarins. Bioorg Med Chem Lett, 14(9), 2241–3.
Danyluk, M.D., Uesugi, A.R. and Harris, L.J. (2005). Survival of Salmonella enteritidis PT 30 on inoculated almonds after commercial fumigation with propylene oxide. J Food Prot, 68(8), 1613–22.
Das, T., Das, MC., Das, A., Bhowmik, S., Sandhu, P., Akhter, Y., Bhattacharjee, S., De, UC . (2018). Modulation of S. aureus and P. aeruginosa biofilm: an in vitro study with new coumarin derivatives. World J Microbiol Biotechnol, 34(11), 170.
de Souza, S.M., Delle Monache, F. and Smania, A., Jr. (2005). Antibacterial activity of coumarins. Z Naturforsch C, 60(9–10), 693–700.
Dekic, B.R., Radulovic, N.S., Dekic, V.S., Vukicevic, R.D. and Palic, R.M. (2010). Synthesis and antimicrobial activity of new 4-heteroarylamino coumarin derivatives containing nitrogen and sulfur as heteroatoms. Molecules, 15(4), 2246–56.
Dua, R., Shrivastava, S., K Sonwane, S., K Srivastava, S. and Gour, H. (2011). Pharmacological Significance of Synthetic Heterocycles Scaffold: A Review. Advances in Biological Research, 5(3), 120–44.
Eglezos, S., Huang, B. and Stuttard, E. (2008). A survey of the bacteriological quality of preroasted peanut, almond, cashew, hazelnut, and brazil nut kernels received into three Australian nut-processing facilities over a period of 3 years. J Food Prot, 71(2), 402–4.
Freire, F. and Kozakiewicz, Z. (2005). Filamentous fungi, bacteria and yeasts associated with cashew kernels in Brazil. Revista Ciência Agronômica, 36(2), 249–54.
Garrard, W. and Lascelles, J. (1968). Regulation of Staphylococcus aureus lactate dehydrogenase. J Bacteriol, 95(1), 152–6.
Golus, J., Sawicki, R., Widelski, J. and Ginalska, G. (2016). The agar microdilution method: A new method for antimicrobial susceptibility testing for essential oils and plant extracts. J Appl Microbiol, 121(5), 1291–99.
Helianti, I., Okubo, T., Morita, Y. and Tamiya, E. (2007). Characterization of thermostable native alkaline phosphatase from an aerobic hyperthermophilic archaeon, Aeropyrum pernix K1. Appl Microbiol Biotechnol, 74(1), 107–12.
Hyndman, J.B. (1963). Comparison of enterococci and coliform microorganisms in commercially produced pecan nut meats. Appl Microbiol, 11(3), 268–72.
Jadhav, V.B., Nayak, S.K., Row, T.N. and Kulkarni, M.V. (2010). Synthesis, structure and DNA cleavage studies of coumarin analogues of tetrahydroisoquinoline and protoberberine alkaloids. Eur J Med Chem, 45(9), 3575–80.
Jurd, L., Corse, J., King, A.D., Bayne, H. and Mihara, K. (1971). Antimicrobial properties of 6,7-dihydroxy-, 7,8-dihydroxy-, 6-hydroxy- and 8-hydroxycoumarins. Phytochemistry, 10(12), 2971–4.
Kayser, O. and Kolodziej, H. (1999). Antibacterial activity of simple coumarins: structural requirements for biological activity. Z Naturforsch C, 54(3-4), 169–74.
Kimber, M.A., Kaur, H., Wang, L., Danyluk, M.D. and Harris, L.J. (2012). Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated almonds and pistachios stored at -19, 4, and 24 degrees C. J Food Prot, 75(8), 1394–403.
King, A.D., Jr., Miller, M.J. and Eldridge, L.C. (1970). Almond harvesting, processing, and microbial flora. Appl Microbiol, 20(2), 208–14.
Li, J., Sui, Yun-Peng., Xin, Jia-Ji., Du, Xin-Liang., Li, Jiang-Tao., Huo, Hai-Ru.,Ma, Hai., Wang, Wei-Hao., Yu Zhou, Hai., Zhan, Hong-Dan., Wang, Zhu-Ju., Li, Chun., Sui, Feng., and Li, Xia. (2015). Synthesis of Biscoumarin and Dihydropyran Derivatives and Evaluation of Their Antibacterial Activity. Molecules, 20(9), 17469–82.
M de Souza, S., Delle Monache, F. and Smania Junior, A. (2005). Antibacterial Activity of Coumarins. Zeitschrift für Naturforschung C, 60(9–10), 693–700.
Ma, J., Jones, S.H. and Hecht, S.M. (2004). A coumarin from Mallotus resinosus that mediates DNA cleavage. J Nat Prod, 67(9), 1614–6.
Manolov, I., Maichle-Moessmer, C. and Danchev, N. (2006). Synthesis, structure, toxicological and pharmacological investigations of 4-hydroxycoumarin derivatives. Eur J Med Chem, 41(7), 882–90.
Nazzaro, F., Fratianni, F., De Martino, L., Coppola, R. and De Feo, V. (2013). Effect of essential oils on pathogenic bacteria. Pharmaceuticals (Basel), 6(12), 1451–74.
Ojala, T., Remes, S., Haansuu, P., Vuorela, H., Hiltunen, R., Haahtela, K., Vuorela, P. (2000). Antimicrobial activity of some coumarin containing herbal plants growing in Finland. J Ethnopharmacol, 73(1-2), 299–305.
Ozaktan, H., Erdal, M., Akköprü, A. and Aslan, E. (2012). Biological control of bacterial blight of walnut by antagonistic bacteria. Journal of Plant Pathology, 94(1), 53-56.
Patil, S.A., Kamble, U.V. and Badami, P.S. (2010). Antimicrobial and DNA-cleavage studies of 22-membered N4 tetraaza macrocyclic triazoles: template synthesis and physicochemical characterization. Nucleosides Nucleotides Nucleic Acids, 29(9), 658–75.
Rauckman, B.S., Tidwell, M.Y., Johnson, J.V. and Roth, B. (1989). 2,4-Diamino-5-benzylpyrimidines and analogues as antibacterial agents. 10. 2,4-Diamino-5-(6-quinolylmethyl)- and -[(tetrahydro-6-quinolyl) methyl] pyrimidine derivatives. Further specificity studies. J Med Chem, 32(8), 1927–35.
Sanchez, E., Garcia, S. and Heredia, N. (2010). Extracts of edible and medicinal plants damage membranes of Vibrio cholerae. Appl Environ Microbiol, 76(20), 6888–94.
Sang Sung, W. and Gun Lee, D. (2010). Antifungal action of chlorogenic acid against pathogenic fungi, mediated by membrane disruption. 
Pure and Applied Chemistry, 82(1), 219–26.
Sarwar, T., Rehman, S.U., Husain, M.A., Ishqi, H.M. and Tabish, M. (2015). Interaction of coumarin with calf thymus DNA: Deciphering the mode of binding by in vitro studies. Int J Biol Macromol, 73(n/a), 9–16.
Schinkovitz, A., Gibbons, S., Stavri, M., Cocksedge, M.J. and Bucar, F. (2003). Ostruthin: an antimycobacterial coumarin from the roots of Peucedanum ostruthium. Planta Med, 69(4), 369–71.
Shikishima, Y., Takaishi, Y., Honda, G., Ito, M., Takfda, Y., Kodzhimatov, OK., Ashurmetov, O., Lee KH. (2001). Chemical constituents of Prangos tschiniganica; structure elucidation and absolute configuration of coumarin and furanocoumarin derivatives with anti-HIV activity. Chem Pharm Bull (Tokyo), 49(7), 877–80.
Stavri, M. and Gibbons, S. (2005). The antimycobacterial constituents of dill (Anethum graveolens). Phytother Res, 19(11), 938–41.
Tan, N., Yazici-Tutunis, S., Bilgin, M., Tan, E. and Miski, M. (2017). Antibacterial Activities of Pyrenylated Coumarins from the Roots of Prangos hulusii. Molecules, 22(7), 1098–2005.
Uesugi, A.R., Danyluk, M.D., Mandrell, R.E. and Harris, L.J. (2007). Isolation of Salmonella Enteritidis phage type 30 from a single almond orchard over a 5-year period. J Food Prot, 70(8), 1784–9.
Walasek, M., Grzegorczyk, A., Malm, A. and Skalicka-Wozniak, K. (2015). Bioactivity-guided isolation of antimicrobial coumarins from Heracleum mantegazzianum Sommier and Levier (Apiaceae) fruits by high-performance counter-current chromatography. Food Chem, 186(n/a), 133–8.
Wolde, A.T. and Seifu, E. (2011). Microbial quality of raw cow’s milk collected from farmers and dairy cooperatives in Bahir Dar Zuria and Mecha district, Ethiopia, 2(1), 29–33.
Zhang, G., Hu, L., Melka, D., Wang, H., Laasri, A., Brown, EW., Strain, E., Allard, M., Bunning, VK., Musser, SM., Johnson, R., Santillana, S., Scott, VN., Pouillot, R., Doren, JM. and Hammack, TS . (2017). Prevalence of salmonella in cashews, hazelnuts, macadamia nuts, pecans, pine nuts, and walnuts in the United States. J of Food Protection, 80(3), 459–66.