Antibacterial Effects of Extracts of Two Types of Red Sea Algae

Abstract

Introduction: Intestinal bacteria are exposed many external influences, including drugs, causing the emergence of strains resistant to the effects of antibiotics. Consequently, the discovery of new antibiotics that affect resistant strains is required. Marine algae offer a source of renewable natural compounds with antimicrobial effects. Therefore, the aim of this study was to detect some of these compounds and examine their impact on enteric bacteria. Methodology: Escherichia coli, Salmonella typhi, Shigella dysenteriae, Klebsiella pneumoniae, and Enterobacter aerogenes were tested with extracts of Turbinaria triquetra and Halimeda opuntia extracted with methanol, ethanol, petroleum ether, or dimethyl formamide solvents. We measured bacterial growth inhibition, the minimal inhibitory concentrations (MICs), and potassium leakage, and analyzed the bacterial cells with scanning electron microscopy and energy-dispersive X-ray spectroscopy. Results: The T. triquetra extract produced with methanol strongly affected the bacteria tested. When the results for T. triquetra and H. opuntia were compared with those of omacillin, the T. triquetra and H. opuntia extracts in most solvents were more effective than the antibiotic. Differences in the bacterial growth inhibition and MICs depended on the type of alga and the solvent used. At the end of the incubation period, potassium leakage had increased by 62.98% for E. coli, 61.24% for S. typhi, 61.32% for S. dysenteriae, 64.02% for K. pneumoniae, and 63.10% for E. aerogenes when treated T. triquetra. Conclusion: Turbinaria triquetra extracted with methanol strongly affected the growth of the bacteria tested. Therefore, it is a potential source of natural antibacterial compounds.

Share and Cite:

Al-Judaibi, A. (2014) Antibacterial Effects of Extracts of Two Types of Red Sea Algae. Journal of Biosciences and Medicines, 2, 74-82. doi: 10.4236/jbm.2014.22012.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Nagshetty, K., Channappa, S.T. and Gaddad, S.M. (2010) Antimicrobial Susceptibility of Salmonella typhi in India. The Journal of Infection in Developing Countries, 4, 070-073.
[2] Poore, A.G.B., Graba-Landry, A., Favret, M., Brennand, H.S., Byrne, M. and Dworjanyn, S.A. (2013) Direct and Indirect Effects of Ocean Acidification and Warming on a Marine Plant-Herbivore Interaction. Oecologia, 173, 1113-1124.
http://dx.doi.org/10.1007/s00442-013-2683-y
[3] Chanda, S., Dave, R., Kaneria, M. and Nagani, K. (2010) Seaweeds: A Novel, Untapped Source of Drugs from Sea to Combat Infectious Diseases. In: Mendez-Vilas A., Ed., Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, 473-480.
[4] Kumar, S.R., Ramanathan, G., Subhakaran, M. and Inbaneson, S.J. (2009) Antimicrobial Compounds from Marine Halophytes for Silkworm Disease Treatment. International Journal of Medicine and Medical Sciences, 1, 184-191.
[5] Kajiwara, T., Matsui, K., Akakabe, Y., Murakawa, T. and Arai, C. (2007) Antimicrobial Browning-Inhibitory Effect of Flavor Compounds in Seaweeds. Developments in Applied Phycology, 1, 187-196.
http://dx.doi.org/10.1007/978-1-4020-5670-3_24
[6] Cox, S., Abu-Ghannam, N., and Gupta, S. (2010) An Assessment of the Antioxidant and Antimicrobial Activity of Six Species of Edible Irish Seaweeds. International Food Research Journal, 17, 205-220.
[7] Gupta, S. and Abu-Ghannam, N. (2011) Bioactive Potential and Possible Health Effects of Edible Brown Seaweeds. Trends in Food Science & Technology, 22, 315-326.
http://dx.doi.org/10.1016/j.tifs.2011.03.011
[8] Salem, W.M., Galal, H., and Nasr Eldeen, F. (2011) Screening for Antibacterial Activities in Some Marine Algae from the Red Sea (Hurghada, Egypt). African Journal of Microbiology Research, 5, 2160-2167.
http://dx.doi.org/10.5897/AJMR11.390
[9] Sire, J., Nabeth, P., Perrier-Gros-Claude, J., Bahsoun, I., Siby, T., Macondo, E., Gaye-Diallo, A., Guyomard, S., Seck, A., Breurec, S. and Garin, B.T. (2007) Antimicrobial Resistance in Outpatient Escherichia coli Urinary Isolates in Dakar, Senegal. The Journal of Infection in Developing Countries, 1, 263-268.
[10] Gangoué-Piéboji, J., Eze, N., Djintchui, A.N., Ngameni, B., Tsabang, N., Pegnyemb, D.E., Biyiti, L., Ngassam, P., Koulla-Shiro, S. and Galleni, M. (2009) The in-Vitro Antimicrobial Activity of Some Traditionally Used Medicinal Plants against Beta-Lactam-Resistant Bacteria. The Journal of Infection in Developing Countries, 3, 671-680.
http://dx.doi.org/10.3855/jidc.77
[11] Kansakar, P., Baral, P., Malla, S. and Ghimire, G.R. (2011) Antimicrobial Susceptibilities of Enteric Bacterial Pathogens Isolated in Kathmandu, Nepal, during 2002-2004. The Journal of Infection in Developing Countries, 5, 163-168.
http://dx.doi.org/10.3855/jidc.1016
[12] Reynolds, J.E.F., Parfitt, K., Parsons, A.V. and Sweetman, S.C. (1996) Martindale the Extra Pharmacopeia. 31st Edition, Royal Pharmaceutical Society, London.
[13] CLSI (2007) Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Information Supplement. CLSI Document M100-S17 (M2-A7 and M7-A7) 27(1) Clinical and Laboratory Standards Institute, Wayne, Pa.
[14] NCCLS (2006) Performance Standards for Antimicrobial Disk Susceptibility Testing; Approved Standard, Ninth Edition. NCCLS Approved Standard M2-A9 26 (1) Clinical and Laboratory Standards Institute, Wayne, Pa.
[15] NCCLS (2006) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard, Seventh Edition. NCCLS Approved Standard M7-A7 26 (2) Clinical and Laboratory Standards Institute, Wayne, Pa.
[16] NCCLS (2002) Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, Approved Standard. 2nd Edition, NCCLS Document M31-A2 22(6), Clinical and Laboratory Standards Institute, Wayne.
[17] Lambert, R.J.W., Skandamis, P.N., Coote, P.J. and Nychas, G.J.E. (2001) A Study of the Minimum Inhibitory Concentration and Mode of Action of Oregano Essential Oil, Thymol and Carvacrol. Journal of Applied Microbiology, 91, 453-462.
http://dx.doi.org/10.1046/j.1365-2672.2001.01428.x
[18] Cox, S.D., Mann, C.M., Markham, J.L., Gustafson, J.E., Warmington, J.R. and Wyllie, S.G. (2001) Determining the Antimicrobial Actions of Tea Tree Oil. Molecules, 6, 87-91.
[19] Ranjan, P., Das, M.P., Kumar, M.S., Anbarasi, P., Sindhu, S., Sagadevan, E. and Arumugam, P. (2013) Green Synthesis and Characterization of Silver Nanoparticles from Nigella sativa and Its Application against UTI Causing Bacteria. Journal of Academia and Industrial Research (JAIR), 2, 45-49.
[20] Tyagi, A.K., Bukvicki, D., Gottardi, D., Veljic, M., Guerzoni, M.E., Malik, A., and Marin, P.D. (2013) Antimicrobial Potential and Chemical Characterization of Serbian Liverwort (Porella arboris-vitae): SEM and TEM Observations. Evidence-Based Complementary and Alternative Medicine, 2013, Article ID 382927.
http://dx.doi.org/10.1155/2013/382927
[21] Coelho-Souza, S.A., Miranda, M.R., Salgado, L.T., Coutinho, R. and Guimaraes, J.R.D. (2012) Adaptation of the 3H-Leucine Incorporation Technique to Measure Heterotrophic Activity Associated with Biofilm on the Blades of the Sea-weed Sargassum spp. Microbial Ecology, 65, 424-436.
http://dx.doi.org/10.1007/s00248-012-0116-9
[22] Matsukawa, R., Dubinsky, Z., Kishimoto, E., Masaki, K., Masuda, Y., Takeuchi, T., Chihara, M., Yamamoto, Y., Niki, E. and Karube, I. (1997) A Comparison of Screening Methods for Antioxidant Activity in Seaweeds. Journal of Applied Phycology, 9, 29-35.
http://dx.doi.org/10.1023/A:1007935218120
[23] Cardozo, K.H.M., Guaratini, T., Barros, M.P., Falcão, V.R., Tonon, A.P., Lopes, N.P., Campos, S., Torres, M.A., Souza, A.O., Colepicolo, P. and Pinto, E. (2007) Metabolites from Algae with Economical Impact. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146, 60-78.
[24] Jeyaseelan, E.C., Kothai, S., Kavitha, R., Tharmila, S. and Thavaranjit, A.C. (2012) Antibacterial Activity of Some Selected Algae Present in the Costal Lines of Jaffna Peninsula. International Journal of Pharmaceutical & Biological Archives, 3, 352-356.
[25] Mearns-Spragg, A., Bregu, M., Boyd, K.G., and Burgess, J.G. (1998) Cross-Species Induction and Enhancement of Antimicrobial Activity Produced by Epibiotic Bacteria from Marine Algae and Invertebrates, after Exposure to Terrestrial Bacteria. Letters in Applied Microbiology, 27, 142-146.
http://dx.doi.org/10.1046/j.1472-765X.1998.00416.x
[26] Jeyaseelan, E.C., Kothai, S., Kavitha, R., Tharmila, S. and Thavaranjit, A.C. (2012) Antibacterial Activity of Some Selected Algae Present in the Costal Lines of Jaffna Peninsula. International Journal of Pharmaceutical & Biological Archives, 3, 352-356.
[27] Mearns-Spragg, A., Bregu, M., Boyd, K.G., and Burgess, J.G. (1998) Cross-Species Induction and Enhancement of Antimicrobial Activity Produced by Epibiotic Bacteria from Marine Algae and Invertebrates, after Exposure to Terrestrial Bacteria. Letters in Applied Microbiology, 27, 142-146.
http://dx.doi.org/10.1046/j.1472-765X.1998.00416.x
[28] Blunt, J.W., Copp, B.R., Munro, M.H.G., Northcote, P.T. and Prinsep, M.R. (2005) Marine Natural Products. Natural Product Reports, 22, 15-61.
http://dx.doi.org/10.1039/b415080p
[29] Demirel, Z., Yilmaz-Koz, F.F., Karabay-Yavasoglu, U.N., Ozdemir, G. and Sukatar, A. (2009) Antimicrobial and Antioxidant Activity of Brown Algae from the Aegean Sea. Journal of the Serbian Chemical Society, 74, 619-628.
http://dx.doi.org/10.2298/JSC0906619D
[30] Taskin, E., Ozturk, M., Taskin, E. and Kurt, O. (2007) Antibacterial Activities of Some Marine Algae from the Aegean Sea (Turkey). African Journal of Biotechnology, 6, 2746-2751.
[31] Salvador, N., Garreta, A.G., Lavelli, L. and Ribera, M. (2007) Antimicrobial Activity of Iberian Macroalgae. Scientia Marina, 71, 101-113.
[32] Kandhasamy, M. and Arunachalam, K.D. (2008) Evaluation of in Vitro Antibacterial Property of Seaweeds of Southeast Coast of India. African Journal of Biotechnology, 7, 1958-1961.
[33] Ballesteros, E., Martin, D. and Uriz, M.J. (1992) Biological Activity of Extracts from Some Mediterranean Macrophytes. Botanica Marina, 35, 481-485.
[34] Epstein, W. (2003) The Roles and Regulation of Potassium in Bacteria. Progress in Nucleic Acid Research and Molecular Biology, 75, 293-320.
http://dx.doi.org/10.1016/S0079-6603(03)75008-9
[35] Kempf, B. and Bremer, E. (1998) Uptake and Synthesis of Compatible Solutes as Microbial Stress Responses to High-Osmolality Environments. Archives of Microbiology, 170, 319-330.
http://dx.doi.org/10.1007/s002030050649
[36] McLaggan, D., Naprstek, J., Buurman, E.T. and Epstein, W. (1994) Interdependence of K+ and Glutamate Accumulation during Osmotic Adaptation of Escherichia coli. Journal of Biological Chemistry, 269, 1911-1917.
[37] Viejo-Diaz, M., Andrés, M.T., Pérez-Gil, J., Sánchez, M. and Fierro, J.F. (2003) Potassium Efflux Induced by a New Lactoferrin-Derived Peptide Mimicking the Effect of Native Human Lactoferrin on the Bacterial Cytoplasmic Membrane. Biochemistry (Moscow), 68, 217-227. Translated from Biokhimiya, 68, 260-273.
[38] Roe, A.J., Mclaggan, D., Davidson, I., O’byrne, C. and Booth, I.R. (1998) Perturbation of Anion Balance during Inhibition of Growth of Escherichia coli by Weak Acids. Journal of Bacteriology, 180, 767-772.

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.