Comparison of Antimicrobial Activities of Sparus aurata Skin and Mucus Extracts with Laurencia papillosa and Carollina officinalis Algae Dry Extracts

Öz

The present study aimed to determine the antimicrobial activity of methanol, acetone, ethanol, or heptane ex-tracts from L. papillosa or C. officinalis with the skin and mucus extracts from S. aurata. The inhibition zone (IZ) and minimum inhibitory concentration (MIC) of the extracts against Acinetobacter baumannii, Klebsiella pneumoniae, Staphylococcus aureus, Enterococcus faecalis, Candida tropicalis, and C. parapsilosis were de-termined by well diffusion and spectrophotometric broth microdilution methods, respectively. The highest an-timicrobial activity of L. papillosa was against C. tropicalis with 4.98 mm, and the highest activity of C. offic-inalis was against E. faecalis with 7.84 mm. Among S. aurata mucus and skin extracts, the highest activity was on C. parapsilosis with 13.82 mm. The antimicrobial effect of S. aurata mucus extract on E. faecalis was found to be almost the same as L. papillosa extracts (6.14 mm and 6.43 mm). The inhibitions of S. au-rata aqueous phase extract on K. pneumoniae and C. parapsilosis (7.09 mm) were much greater than the ef-fects of L. papillosa and C. officinalis extraction. That S. aurata mucus and skin extracts were very effective, especially on K. pneumoniae, A. baumannii and Candida sp., was showed for the first time with this study. As a result, S. aurata mucus content is more effective on K. pneumoniae and C. parapsilosis than the phenol-ic content of both algae.

Anahtar Kelimeler

• Sparus aurata
• Laurencia papillosa
• Carollina officinalis
• Antimicrobial activity

Kaynakça

1. Adamek, M., Syakuri, H., Harris, S., Rakus, K., Brogden, G., Matras, M., Steinhagen, D. (2013) Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpioL.). Veterinary Microbiology,162:456-470.
2. Akyıl, S., İlter, I., Koç, M., Kaymak-Ertekin, F. (2016) Alglerden Elde Edilen Yüksek Değerlikli Bileşiklerin Biyoaktif/Biyolojik Uygulama Alanları. Akademik Gıda, 14:418-423.
3. Alçay, A. Ü., Bostan, K., Dinçel, E., Varlık, C. (2017) Alglerin insan gıdası olarak kullanımı. Aydın Gastronomy,1:47-59.
4. Austin, B., McIntosh, D. (1988) Natural antibacterial compounds on the surface of rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases, 11: 275-277.
5. Baytaşoğlu, H., Başusta, N. (2015) Deniz canlılarının tıp ve eczacılık alanlarında kullanılması. Aquaculture Studies, 15: 71-80.
6. Bergsson, G., Agerberth, B., Jörnvall, H., Gudmundsson, G. H. (2005) Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). The FEBS journal, 272:4960-4969.
7. Carvalho, J., Ribeiro, A., Castro, J. D. F. D., Vilarinho, C., Castro, F. (2011) Biodiesel production by microalgae and macroalgae from north littoral portuguese coast. Wastes: Solutions, Treatments,and Opportunities, 1. International Conference, September 12-14 th.
8. Cassani, L., Gomez-zavaglia, A., Jimenez-lopez, C., Prieto, M.A., Simal-gandara, J. (2020) Seaweed-based natural ingredients: Stability of phlorotannins during extraction, storage, passage through the gastrointestinal tract and potential incorporation into functional foods. Food Research, 109676.

9. Chapman, R. L. (2013) Algae: the world’s most important ‘plants’ an intoduction. Mitigation and Adaptation Strategies for Global Change, 18:5-12.
10. Cordero, H., Cuesta, A., Meseguer, J., Esteban, M. Á. (2016) Changes in the levels of humoral immune activities after storage of gilthead seabream (Sparus aurata) skin mucus. Fish & Shellfish Immunology, 58:500-507.
11. Cunha, F. M., Coscueta, E. R., Brassesco, M. E., Almada, F., Gonçalves, D., & Pintado, M. (2023) Methods for the Collection of Fish Mucus: A Systematic Review. Reviews in Fisheries Science & Aquaculture, 1-35.
12. Dash, S., Das, S. K., Samal, J., Thatoi, H. N. (2018) Epidermal mucus, a major determinant in fish health: a review. Iranian Journal of Veterinary Research, 19:72.
13. Dhaouafi, J., Abidi, A., Nedjar, N., Romdhani, M., Tounsi, H., Sebai, H., Balti, R. (2023) Protective Effect of Tunisian Red Seaweed (Corallina officinalis) Against Bleomycin-Induced Pulmonary Fibrosis and Oxidative Stress in Rats. Dose-Response, 21:1-13.
14. Durmaz, Y., Işık, O., Bandarrra, N.M., Cirik, S., Turan, G., Gökpınar, Ş. (2002) Porphyridium cruentum (Rhodophyceae) yağ asitleri kompozisyonuna kurutma yöntemlerinin etkisi. Ege Journal of Fisheries and Aquatic Sciences, 19: 189-195.
15. El-Sheekh, M.M., Osman, M.E.H., Dyab, M.A., Amer, M.S. (2006) Production and characterization of antimicrobial active substance from the Cyanobacterium Nostoc muscorum. Environmental Toxicology and Pharmacology, 21:42–50.
16. Erdoğan Eliuz, E. A. (2021) Antimicrobial Activity and Mechanism of Essential Oil of Endemic Salvia hypargeia Finc. & Mey. in Turkey. Indian Journal of Microbiology, 61:291-297.
17. Fast, M. D., Sims, D. E., Burka, J. F., Mustafa, A., Ross, N. W. (2002) Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 132: 645-657.
18. Goksen, G. (2023) Elucidation and quantification health-promoting phenolic compounds, antioxidant properties and sugar levels of ultrasound assisted extraction, aroma compositions and amino acids profiles of macroalgae. Laurencia papillosa. Ultrasonics Sonochemistry, 98: 106527.
19. Gómez-Guzmán, M., Rodríguez-Nogales, A., Algieri, F., Gálvez, J. (2018) Potential role of seaweed polyphenols in cardiovascular-associated disorders. Marine Drugs, 16:250.
20. Guardiola, F. A., Cuesta, A., Arizcun, M., Meseguer, J., Esteban, M. A. (2014) Comparative skin mucus and serum humoral defence mechanisms in the teleost gilthead seabream (Sparus aurata). Fish & shellfish immunology, 36: 545-551.
21. Guardiola, F. A., Dioguardi, M., Parisi, M. G., Trapani, M. R., Meseguer, J., Cuesta, A., Cammarata, M., Esteban, M. A. (2015) Evaluation of waterborne exposure to heavy metals in innate immune defences present on skin mucus of gilthead seabream (Sparus aurata). Fish & shellfish immunology, 45:112-123.
22. Gustafsson, J. K., Navabi, N., Rodriguez-Piñeiro, A. M., Alomran, A. H., Premaratne, P., Fernandez, H. R., Lindén, S.K. (2013) Dynamic changes in mucus thickness and ion secretion during Citrobacter rodentium infection and clearance. PloS one, 8:e84430.
23. Hellio, C., Bremer, G., Pons, A. M., Le Gal, Y., Bourgougnon, N. (2000) Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Applied Microbiology and Biotechnology, 54:543-549.
24. Hellio, C., Pons, A. M., Beaupoil, C., Bourgougnon, N., Le Gal, Y. (2002) Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. International Journal of Antimicrobial Agents, 20:214-219.
25. Johansson, M.E., Holmen Larsson, J.M., Hansson, G.C. (2010) Microbes and Health Sackler Colloquium: The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Biological sciences, 108:14659–4665.
26. Jurado, J., Fuentes-Almagro, C. A., Guardiola, F. A., Cuesta, A., Esteban, M. Á., Prieto-Álamo, M. J. (2015) Proteomic profile of the skin mucus of farmed gilthead seabream (Sparus aurata). Journal of proteomics, 120:21-34.
27. Kaba, N., Çağlak, E. (2006) Deniz Alglerinin İnsan Beslenmesinde Kullanılması. Su Ürünleri Dergisi, 23:243-246. Kandhasamy, M., Arunachalam, K.D. (2008) Evaluation of in vitro antibacterial property of seaweeds of southeast coast of India. African Journal of Biotechnology, 7:1958-1961.
28. Kavita, K., Singh, V. K., Jha, B. (2014) 24-Branched Δ5 sterols from Laurencia papillosa red seaweed with antibacterial activity against human pathogenic bacteria. Microbiological research 169: 301-306.
29. Kolanjinathan, K., Stella, D. (2009b) Antibacterial activity of marine macro algae against human pathogens. Recent Research in Science and Technology, 1:020-022.
30. Nørskov, N.P., Bruhn, A., Cole, A., Nielsen, M.O. (2021) Targeted and untargeted metabolic profiling to discover bioactive compounds in seaweeds and hemp using gas and liquid chromatography-mass spectrometry Metabolites, 11:259.
31. Özdemir, N., Erkmen, J. (2013) Yenilenebilir biyoplastik üretiminde alglerin kullanımı. Karadeniz Fen Bilimleri Dergsisi, 3: 89-104.
32. Polat, S., Özoğul, Y. (2008) Biochemical composition of some red and brown macroalgae from the Northeastern Mediterranean Sea. International Jounal of Food Science and Nutrition, 59: 566-572.
33. Rajauria, G., Foley, B., Abu-Ghannam, N. (2016) Identification and characterization of phenolic antioxidant compounds from brown Irish seaweed Himanthalia elongata using LC-DAD–ESI-MS/MS Innovative Food Science & Emerging Technologies, 37:261-268.
34. Reid, K. M., Patel, S., Robinson, A. J., Bu, L., Jarungsriapisit, J., Moore, L. J., Salinas, I. (2017) Salmonid alphavirus infection causes skin dysbiosis in Atlantic salmon (Salmo salar L.) post-smolts. PloS one, 12:e0172856.
35. Reverter, M., Tapissier-Bontemps, N., Lecchini, D., Banaigs, B., Sasal, P. (2018) Biological and ecological roles of external fish mucus: a review. Fishes, 3:41.
36. Salem, W. M., Galal, H., Nasr El-deen, F. (2011) Screening for antibacterial activities in some marine algae from the red sea (Hurghada, Egypt). African Journal of Microbiology Research, 5: 2160-2167.
37. Silva, A., Silva, S. A., Carpena, M., Garcia-Oliveira, P., Gullón, P., Barroso, M. F., Prieto, M.A., Simal-Gandara, J. (2020) Macroalgae as a source of valuable antimicrobial compounds: Extraction and applications. Antibiotics, 9: 642.
38. Spitzer, R. H., Koch, E. A. (1998) Hagfish skin and slime glands. In The biology of hagfishes Springer, pp.109-132.
39. Subramanian, S., Ross, N. W., MacKinnon, S. L. (2008) Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 150: 85-92.
40. Taib, M. N. A. M., Anuar, N., Hanafiah, K. M., Al-Shammary, A. A. K., Saaid, M., Awang, K. (2020) Chemicals constituents isolated from cultivate Alpinia conchigera Griff. and antimicrobial activity. Tropical Life Sciences Research 31:159.
41. Taskin, E., Ozturk, M., Kurt, O. (2007) Antibacterial activities of some marine algae from the Aegean Sea (Turkey). African journal of Biotechnology, 6: 2746-2751.
42. Uyan, A., Turan, C., Erdogan-Eliuz, E. A., Sangun, M. K. (2020) Antimicrobial properties of bioactive compounds isolated from epidermal mucus in two Ray species (Dasyatis marmorata and Gymnura altavela). Tropical Journal of Pharmaceutical Research 19:2115-2121.
43. Van der Marel, M., Caspari, N., Neuhaus, H., Meyer, W., Enss, M. L., Steinhagen, D. (2010) Changes in skin mucus of common carp, Cyprinus carpio L., after exposure to water with a high bacterial load. Journal of fish diseases, 33:431-439.
44. Vasta, G. R., Nita-Lazar, M., Giomarelli, B., Ahmed, H., Du, S., Cammarata, M., (2011) Amzel, L. M. Structural and functional diversity of the lectin repertoire in teleost fish: relevance to innate and adaptive immunity. Developmental & Comparative Immunology, 35: 1388-1399.
45. Xu T, Sutour S, Casabianca H, Tomi, F., Paoli, M., Garrido, M., Pasqualini, V., Aiello, A., Castola, V., Bighelli, A. (2015) Rapid Screening of chemical compositions of Gracilaria dura and Hypnea mucisformis (Rhodophyta) from corsican lagoon. International Journal of Phytocosmetics and Natural Ingredients, 2,1-5.
46. Zhong, B., Robinson, N.A., Warner, R.D., Barrow, C.J., Dunshea, F.R., Suleria H.A.R. (2020) LC-ESI-QTOF-MS/MS characterization of seaweed phenolics and their antioxidant potential Marine Drugs, 18:331-352.