Abstract
Application of antimicrobial botanical extracts and other natural products is receiving increasing attention. The present study aimed to evaluate the antifungal activities of some macroalgae collected from Alexandria beach, Egypt for treatment of fungal urinary tract infections (UTIs). Methanol extracts of Ulva lactuca showed the highest recorded antifungal activity against Aspergillus flavus and Aspergillus niger, while Enteromorpha linza showed the highest antifungal activity against Candida tropicalis. In addition, methanol extracts of both macroalgae showed a significant urease inhibition of the corresponding fungi. Lineweaver–Burk plots indicated a reversible non-competitive mechanism for U. lactuca extract, whereas E. linza extract showed a reversible competitive inhibition. Fatty acids profile of methanol extracts of U. lactuca and E. linza showed predominance of octadecanoic acid and hexadecanoic acid (48.4% and 62.9% of total fatty acids, respectively). In addition, GC/MS results showed significant proportions of the biologically active compounds; benzodioxoles such as piperonylbutoxide, organochlorines such as p,p’-dichlorodiphenyltrichloroethane (DDT) in U. lactuca and phytosterols such as stigmastan derivatives in E. linza. The present study represents an advancement in the knowledge of the chemistry and antifungal potential of macroalgae against UTIs and offers promising trend for drug discovery from marine macroalgae.
Similar content being viewed by others
References
Abd Elmegeed D, Ghareeb D, Elsayed M, El-Saadani M (2014) Phytochemical constituents and bioscreening activities of green algae (Ulva Lactuca). Int J Agric Policy Res 2:373–378
Abomohra A, El-Naggar A, Baeshen A (2018) Potential of macroalgae for biodiesel production: screening and evaluation studies. J Biosci Bioeng 125:231–237
Aleem A (1993) The marine algae of Alexandria. Egyptian Books House, Egypt
Ali S, Shaaban M, Abomohra A, El-Safity K (2016) Macroalgal activity against multiple drug resistant Aeromonas hydrophila: a novel treatment study towards enhancement of fish growth performance. Microb Pathog 101:89–95
Amin M, Anwar F, Janjua M, Iqbal M, Rashid U (2012) Green synthesis of silver nanoparticles through reduction with Solanum xanthocarpum L. berry extract: characterization, antimicrobial and urease inhibitory activities against Helicobacter pylori. Int J Mol Sci 13:9923–9941
Amin M, Anwar F, Naz F, Mehmood T, Saari N (2013) Anti-Helicobacter pylori and urease inhibition activities of some traditional medicinal plants. Molecules 18:2135–2149
Bhat R, Katy T, Place F (2011) Pediatric urinary tract infections. Emerg Med Clin N Am 29:637–653
Boero F (2015) The future of the Mediterranean Sea Ecosystem: towards a different tomorrow. Rend Fis Acc Lincei 26(1):3–12
Cao B, Wang S, Hu Y, Abomohra AEF, Qian L, He Z, Wang Q, Uzoejinwa BB, Esakkimuthu S (2019) Effect of washing with diluted acids on Enteromorpha clathrata pyrolysis products: towards enhanced bio-oil from seaweeds. Renew Energy 138:29–38
Cattaneo-Vietti R (2018) Structural changes in Mediterranean marine communities: lessons from the Ligurian Sea. Rend Fis Acc Lincei 29(3):515–524
Christensen W (1946) Urea decomposition as a means of differentiating Proteus and Paracolon cultures from each other and from Salmonella and Shigella types. J Bacteriol 52:461–466
Chu CM, Lowder JL (2018) Diagnosis and treatment of urinary tract infections across age groups. Am J Obstet Gynecol. https://doi.org/10.1016/j.ajog.2017.12.231
Cox GM, Mukherjee J, Cole GT, Casadevall A, Perfect JR (2000) Urease as a virulence factor in experimental Cryptococcosis. Infect Immun 68:443–448
Demirel Z, Yilmaz F, Karabay-Yavasoglu U, Ozdemir G, Sukatar A (2009) Antimicrobial and antioxidant activity of brown algae from the Aegean Sea. J Serb Chem Soc 74:619–628
El Zawawy N, Ali S (2016) Pyocyanin as anti-tyrosinase and anti tinea corporis: a novel treatment study. Microb Pathog 100:213–220
El Zawawy N, Hafez E (2017) Efficacy of Pluchea dioscoridis leaf extract against pathogenic Candida albicans. J Infect Dev Ctries 11:334–342
Ertürk O, Tas B (2011) Antibacterial and antifungal effects of some marine algae. Kafkas Univ Vet Fak Derg 17:S121–S124
Follmer C (2010) Ureases as a target for the treatment of gastric and urinary infections. J Clin Pathol 63:424–430
Hamouda RA, Sherif SA, Dawoud GT, Ghareeb MM (2016) Enhancement of bioethanol production from Ulva fasciata by biological and chemical saccharification. Rend Fis Acc Lincei 27(4):665–672
Hellio C, Bremer G, Pons A, Gal N (2000) Bourgougnon. Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Appl Microbiol Biotechnol 54:543–549
Hooton T (2012) Uncomplicated urinary tract infection. N Engl J Med 366:1028–1037
Indira K, Balakrishnan S, Srinivasan M, Bragadeeswaran S, Balasubramanian T (2013) Evaluation of in vitro antimicrobial property of seaweed (Halimeda tuna) from Tuticorin coast, Tamil Nadu, Southeast coast of India. Afr J Biotechnol 12:284–289
Ismail MM, Gheda SF, Pereira L (2016) Variation in bioactive compounds in some seaweeds from Abo Qir bay, Alexandria, Egypt. Rend Fis Acc Lincei 27(2):269–279
Jain M, Dogra V, Mishra B, Thakur A, Loomba P, Bhargava A (2011) Candiduria in catheterized intensive care unit patients: emerging microbiological trends. Indian J Pathol Microbiol 54:552–555
Jha R, Zi-rong X (2004) Biomedical compounds from marine organisms. Mar Drugs 2:123–146
Klich M (2002) Identification of common Aspergillus species. Centraalbureau voor Schimmelculture, Utrecht, Netherland
Kolsi R, Frikha D, Jribi I, Hamza A, Feki L, Belghith K (2015) Screening of antibacterial and antifongical activity in marine macroalgae and Magnoliophytea from coast of Tunisia. Int J Pharm Pharm Sci 7:47–51
Kosikowska P, Berlicki L (2011) Urease inhibitors as potential drugs for gastric and urinary tract infections: a patent review. Expert Opin Ther Pat 21:945–957
Kurtzman C, Fell J, Boekhout T (2011) The yeasts, fifth edition: a taxonomic study, 5th edn. Elsevier Science Publishers, Amsterdam
Lagrouh F, Dakka N, Bakri Y (2017) The antifungal activity of Moroccan plants and the mechanism of action of secondary metabolites from plants. J Mycol Med 27:303–311
Lineweaver H, Burk D (1934) The determination of enzyme dissociation constants. J Am Chem Soc 56:658–666
Manilal A, Sujith S, Selvin J, Shakir C, Kiran G (2009) Antibacterial activity of Falkenbergia hillebrandii (Born) from the Indian coast against human pathogens. Phyton 78:161–166
Mobley H, Island M, Hausinger R (1995) Molecular biology of microbial urease. Microbiol Mol Biol Rev 59:451–480
Naidu K, Tewari A, Joshi H, Viswanath S, Rao S (1993) Evaluation of nutritional quality and food safety of seaweeds of India. J Food Saf 13:77–90
Nguyen P, Strub C, Durand N, Alter P, Fontana A, Schorr-Galindo S (2017) Biocontrol of Fusarium verticillioides using organic amendments and their actinomycete isolates. Biol Control 118:55–66
Pérez M, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:52–90
Pfaller M, Diekema D, Messer S, Boyken L, Hollis R (2003) Activities of fluconazole and voriconazole against recent clinical isolate of Candida species determined by broth microdilution, disc diffusion and Etest method: report from the ARTEMIS Global Antifungal Susceptibility Program, 2001. J Clin Microbiol 41:1440–1446
Rossi Y, Palacios S (2015) Insecticidal toxicity of Eucalyptus cinereal essential oil and 1,8-cineole against Musca domestica and possible uses according to the metabolic response of flies. Ind Crops Prod 63:133–137
Stirk W, Reinecke D, Staden J (2007) Seasonal variation in antifungal, antibacterial and acetylcholinesterase activity in seven South African seaweeds. J Appl Phycol 19:271–276
Wang S, Jiang D, Cao B, Hu Y, Yuan C, Wang Q, He Z, Hui CW, Abomohra AEF, Liu X, Feng Y (2018) Study on the interaction effect of seaweed bio-coke and rice husk volatiles during co-pyrolysis. J Anal Appl Pyrolysis 132:111–122
Watson S, Cruz-Rivera E (2003) Algal chemical ecology: an introduction to the special issue. Phycologia 42:319–323
Weatherburn M (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974
Yang R, Li C, Lin Y, Peng G, She Z, Zhou S (2006) Lactones from a brown alga endophytic fungus (No. ZZF36) from the South China Sea and their antimicrobial activities. Bioorg Med Chem Lett 16:4205–4208
Yücesoy M, Marol S (2003) Performance of CHROMAGAR Candida and BIGGY agar for identification of yeast species. Ann Clin Microbiol Antimicrob 2:1–7
Acknowledgments
The authors are thankful to the Head of Urology and Venereology Department, Tanta University Hospital, Tanta, Egypt for providing the necessary help for carrying out the research work.
Author information
Authors and Affiliations
Contributions
NAZ and SME contributed in experimental design and raw data collection and drawing figures/tables besides writing the draft of the paper. AEA organized the data, critical reading of the manuscript and submitted the paper to the journal. All authors have read and approved the manuscript in its present form.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval and consent to participate
All study procedures were implemented at Tanta University and urine sample collection was approved by the Institutional Ethics Committee.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
El Zawawy, N., El Shafay, S. & Abomohra, A.EF. Macroalgal activity against fungal urinary tract infections: in vitro screening and evaluation study. Rend. Fis. Acc. Lincei 31, 165–175 (2020). https://doi.org/10.1007/s12210-019-00856-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12210-019-00856-y