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Antibacterial activities and bioactive compounds of the ethyl acetate extract of the sea cucumber Holothuria forskali from Tunisian coasts

Published online by Cambridge University Press:  04 March 2020

Khaoula Telahigue ,
Ridha Ghali ,
Ezzeddine Nouiri ,
Abdelbaki Labidi  and
Tarek Hajji Open the ORCID record for Tarek Hajji [Opens in a new window]
Khaoula Telahigue
Affiliation:
University of Tunis El Manar, Faculty of Sciences of Tunis, Research unit of Physiology and Aquatic Environment, 2092Tunis, Tunisia University of Manouba, Higher Institute of Biotechnology – Sidi Thabet, Laboratory of Biotechnology and Valorization of Bio-Geo-Resources LR11ES31, Biotechpole Sidi Thabet 2020 Ariana, Tunisia
Ridha Ghali
Affiliation:
University of Tunis El Manar, Laboratory of Toxicology and Environment LR12SP07 Mahmoud Yacoub Center of Urgent Medical Assistance of Tunis, Tunisia
Ezzeddine Nouiri
Affiliation:
University of Tunis El Manar, Laboratory of Toxicology and Environment LR12SP07 Mahmoud Yacoub Center of Urgent Medical Assistance of Tunis, Tunisia
Abdelbaki Labidi
Affiliation:
Chemical Analysis Service, Ministry of Agriculture, Tunis, Tunisia
Tarek Hajji*
Affiliation:
University of Manouba, Higher Institute of Biotechnology – Sidi Thabet, Laboratory of Biotechnology and Valorization of Bio-Geo-Resources LR11ES31, Biotechpole Sidi Thabet 2020 Ariana, Tunisia
*
Author for correspondence: Tarek Hajji, E-mail: tarekhaj@gmail.com; tarek.hajji@isbst.u-manouba.tn
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Abstract

Previous scientific studies have listed chemical compounds from sea cucumber species. The ability to produce bioactive metabolites derives from their response to various ecological stresses and avoidance of predation. In view of this, the present work aimed to evaluate the antibacterial activity and quantitatively assess the active components of different organs of the sea cucumber Holothuria foskali collected from the north-east of Tunisia. The antibacterial activity of ethyl acetate extracts was tested against Bacillus subtilis, Bacillus cereus, Escherichia coli and Pseudomonas aeruginosa. It was revealed that Escherichia coli and Bacillus subtilis were inhibited by the sea cucumber extracts. To identify the composition of these extracts, Gas Chromatography-Mass Spectroscopy (GC-MS) and Liquid Chromatography-Mass Spectroscopy (LC-MS) methods were used. The GC-MS revealed the presence of 25 major components, the most concentrated ones were characterized as C26H27N5O6 Morphinan-4,5-epoxy-3,6-diol, 6 amino;C17H31F3O2 3-trifluoroacetoxypentadecane; C31H50O2 Stigmasta-5,22-dien-3-ol,acetate; C11H14O2 1-Phthalanol,1,3,3-trimethyl 1-phenyl; C30H48O2 Ergosta-5,22-dien-3-ol,acetate and C25H40O2 (9E)-8-Phenyl-9-octadecenoic acid methyl ester; while the LC-MS revealed the presence of eight molecules, identified as phenolic acid, phytosterol and fat-soluble vitamins. Some molecules are interesting and deserve to be explored for their potential uses as ingredients in functional foods or as raw materials for new drug forms.

Keywords

Antibacterialbiomoleculesethyl acetateextractGC-MSHolothuria forskaliLC-MS
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 2 , March 2020 , pp. 229 - 237
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Abdul Jaffar Ali, H and Tamilselvi, M (2016) Ascidians in Coastal Water: A Comprehensive Inventory of Ascidian Fauna from the Indian Coast, 1st Edn. Cham: Springer.CrossRefGoogle Scholar
Abraham, JT, Nagarajan, J and Shanmugam, SA (2002) Antimicrobial substances of potential biomedical importance from holothurian species. Indian Journal of Marine Sciences 31, 161–164.Google Scholar
Adibpour, N, Nasr, F, Nematpour, F, Shakouri, A and Ameri, A (2014) Antibacterial and antifungal activity of Holothuria leucospilota isolated from Persian Gulf and Oman Sea. Jundishapur Journal of Microbiology 7, e8708.CrossRefGoogle ScholarPubMed
Ahmed, Q, Poot-Salazar, A, Mohammad Ali, Q and Bat, L (2018) Seasonal variation in the length-weight relationships and condition factor of four commercially important sea cucumbers species from Karachi Coast – Northern Arabian Sea Quratulan. Natural and Engineering Sciences 3, 265–281.CrossRefGoogle Scholar
Althunibat, OS, Hashim, RB, Taher, M, Daud, JM, Ikeda, M and Zali, I (2009) In vitro antioxidant and antiproliferative activities of three Malaysian sea cucumber species. European Journal of Scientific Research 37, 376–387.Google Scholar
Althunibat, OY, Ridzwan, BH, Taher, M, Daud, JM, Jauhari Arief Ichwan, S and Qaralleh, H (2013) Antioxidant and cytotoxic properties of two sea cucumbers, Holothuria edulis Lesson and Stichopus horrens Selenka. Acta Biologica Hungarica 64, 10–20.CrossRefGoogle ScholarPubMed
Anbukkarasu, S, Subramanian, B, Elayarperumal, N and Masilamani, M (2014) Antimicrobial properties of partially purified extract of starfish Luidia maculata (Muller and Troschel, 1842). International Journal of Applied Research in Natural Products 4, 100–104.Google Scholar
Benkendorff, K, Davis, AR and Bremner, JB (2001) Chemical defence in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. Journal of Invertebrate Pathology 78, 109–118.CrossRefGoogle Scholar
Blunt, JW, Copp, BR, Munro, MHG, Northcotec, PT and Prinsep, MR (2003) Marine natural products. Natural Product Reports 20, 1–48.CrossRefGoogle ScholarPubMed
Bordbar, S, Anwar, F and Saari, N (2011) High-value components and bioactives from sea cucumbers for functional foods – a review. Marine Drugs 9, 1761–1805.CrossRefGoogle ScholarPubMed
Byju, K, Anuradha, V, Vasundhara, G, Nair, SM and Kumar, NC (2014) In vitro and in silico studies on the anticancer and apoptosis-inducing activities of the sterols identified from the soft coral, Subergorgia reticulata. Pharmacognosy Magazine 10 (Suppl. 1), 65–71.Google ScholarPubMed
Caulier, G, Dyck, SV, Gerbaux, P, Eeckhaut, I and Flammang, P (2011) Review of saponin diversity in sea cucumbers belonging to the family Holothuriidae. SPC Bêche-de-mer Information Bulletin 31, 48–54.Google Scholar
Caulier, G, Mezali, K, Soualili, DL, Decroo, C, Demeyer, M, Eeckhaut, I, Gerbaux, P and Flammang, P (2016) Chemical characterization of saponins contained in the body wall and the Cuvierian tubules of the sea cucumber Holothuria (Platyperona) sanctori (Delle Chiaje, 1823). Biochemical Systematics and Ecology 68, 119–127.CrossRefGoogle Scholar
Chao, SM, Chen, CP and Alexander, PS (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Marine Biology 122, 289–295.Google Scholar
Chludil, HD, Muniain, CC, Seldes, AM and Maier, MS (2002) Cytotoxic and antifungal triterpene glycosides from the Patagonian sea cucumber Hemoiedema spectabilis. Journal of Natural Products 65, 860–865.CrossRefGoogle ScholarPubMed
Dhinakaran, DI and Lipton, AP (2014) Bioactive compounds from Holothuria atra of Indian Ocean. SpringerPlus 3, 673.CrossRefGoogle ScholarPubMed
Drazen, JC, Phleger, CF, Guest, MA and Nichols, PD (2008) Lipid, sterols and fatty acid composition of abyssal holothurians and ophiuroids from the North-East Pacific Ocean: food web implications. Comparative Biochemistry and Physiology – Part B: Biochemistry & Molecular Biology 151, 79–87.CrossRefGoogle ScholarPubMed
Enomoto, M, Nakagawa, S and Sawabe, T (2012) Microbial communities associated with holothurians: presence of unique bacteria in the coelomic fluid. Microbes and Environments 27, 300–305.CrossRefGoogle ScholarPubMed
FDA (2012) Guidance for industry: Q3C – tables and list. Silver Spring, MD: U.S. Food and Drug Administration (U.S. FDA), Center for Drug Evaluation and Research (CDER), Center for Biologics Evaluation and Research (CBER). Available at http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm073395.pdf.Google Scholar
Gao, D and Wen, Z (2016) Phthalate esters in the environment: a critical review of their occurrence, biodegradation, and removal during wastewater treatment processes. Science of the Total Environment 541, 986–1001.CrossRefGoogle ScholarPubMed
Ghadiri, M, Kazemi, S, Heidari, B and Rassa, M (2018) Bioactivity of aqueous and organic extracts of sea cucumber Holothuria leucospilota (Brandt 1835) on pathogenic Candida and Streptococci. International Aquatic Research 10, 31–43.CrossRefGoogle Scholar
González-Wangüemert, M, Roggatz, CC, Rodrigues, MJ, Barreira, L, Moreira da Silva, M and Custódio, L (2018) A new insight into the influence of habitat on the biochemical properties of three commercial sea cucumber species. International Aquatic Research 10, 361–373.CrossRefGoogle Scholar
Graham, ER and Thompson, JT (2009) Deposit and suspension feeding sea cucumbers (Echinodermata) ingest plastic fragments. Journal of Experimental Marine Biology and Ecology 368, 22–29.CrossRefGoogle Scholar
Grebe, SK and Singh, RJ (2011) LC-MS/MS in the clinical laboratory – where to from here? Clinical Biochemist Reviews 32, 5–31.Google Scholar
Gu, C, Lin, B, Pease, J, Chetwyn, N and Yehl, P (2015) Mass spectrometry in small molecule drug development. American Pharmaceutical Review 18, 1–12. Available at http://www.americanpharmaceuticalreview.com/Featured-Articles/179230-Mass-Spectrometry-in-Small-Molecule-Drug-Development/.Google Scholar
Haug, T, Kjuul, AK, Styrvold, OB, Sandsdalen, E, Olsen, ØM and Stensvåg, K (2002) Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea). Journal of Invertebrate Pathology 81, 94–102.CrossRefGoogle Scholar
Ho, JHC and Hong, CY (2011) Salvianolic acids: small compounds with multiple mechanisms for cardiovascular protection. Journal of Biomedical Science 18, 30.CrossRefGoogle ScholarPubMed
Hu, Y, Chen, J, Hu, G, Yu, J, Zhu, X, Lin, Y, Chen, S and Yuan, J (2015) Statistical research on the bioactivity of new marine natural products discovered during the 28 years from 1985 to 2012. Marine Drugs 13, 202–221.CrossRefGoogle ScholarPubMed
Kiani, N, Heidari, B, Rassa, M, Kadkhodazadeh, M and Heidari, B (2014) Antibacterial activity of the body wall extracts of sea cucumber (Invertebrata; Echinodermata) on infectious oral streptococci. Journal of Basic and Clinical Physiology and Pharmacology 25, 367–373.CrossRefGoogle Scholar
Miyamae, Y, Kurisu, M, Han, J, Isoda, H and Shigemori, H (2011) Structure-activity relationship of caffeoylquinic acids on the accelerating activity on ATP production. Chemical and Pharmaceutical Bulletin 59, 502–507.CrossRefGoogle ScholarPubMed
Mohammadizadeh, F, Ehsanpor, M, Afkhami, M, Mokhlesi, A, Khazaali, A and Montazeri, S (2013) Evaluation of antibacterial, antifungal and cytotoxic effects of Holothuria scabra from the North Coast of the Persian Gulf. Journal of Medical Mycology 23, 225–229.CrossRefGoogle ScholarPubMed
Mokhlesi, A, Saeidnia, S, Ahmad, R, Gohari Shahverdi Ahmad, R, Mollazadeh-Moghaddam, K and Eśhaghi, N (2011) Antibacterial, antifungal and cytotoxic activities of Bohadschia marmorata, a sea cucumber from the north coast of Persian Gulf. Pharmacology Online 3, 1029–1038.Google Scholar
Mokhlesi, A, Saeidnia, S, Gohari, AR, Shahverdi, AR, Nasrolahi, A, Farahani, F, Khoshnood, R and Eśhaghi, N (2012) Biological activities of the sea cucumber Holothuria leucospilota. Asian Journal of Animal and Veterinary Advances 7, 243–249.Google Scholar
Omran, NE and Allam, NG (2013) Screening of microbial contamination and antimicrobial activity of sea cucumber Holothuria polii. Toxicology and Industrial Health 29, 944–954.CrossRefGoogle ScholarPubMed
Pero, RW and Lund, H (2009) In vivo treatment of humans with quinic acid enhances DNA repair and reduces the influence of lifestyle factors on risk to disease. International Journal of Biotechnology and Biochemistry 5, 293–305.Google Scholar
Pettit, GR, Cragg, GM, Herald, DL, Schmidt, JM and Lohavanijaya, P (1982) Isolation and structure of combretastatin. Canadian Journal of Chemistry 60, 1374–1376.CrossRefGoogle Scholar
Pringgenies, D, Ridlo, A and Sembiring, N (2017) Antibacterial activity for multi drug resistance (MDR) bacteria by sea cucumber Stichopus vastus extract from Karimunjawa islands – Indonesia. Jurnal Ilmudan Teknologi KelautanTropis 9, 695–707.CrossRefGoogle Scholar
Purcell, SW, Samyn, Y and Conand, C (2012) Commercially Important Sea Cucumbers of the World. FAO Species Catalogue for Fishery Purposes No. 6. Rome: FAO.Google Scholar
Ramón, M, Jordi, L and Massutí, E (2010) Royal cucumber (Stichopus regalis) in the northwestern Mediterranean: distribution pattern and fishery. Fisheries Research 10, 21–27.CrossRefGoogle Scholar
Santafé, GG, Guzmán, MS and Torres, OL (2014) Triterpenos Holostánicos con Actividad Antifúngica Obtenidos del Pepino de Mar Holothuria floridana, Recolectado en la Bahía de Cispatá, Córdoba-Colombia. Información Tecnológica 25, 87–92.CrossRefGoogle Scholar
Sarhadizadeh, N, Afkhami, M and Ehsanpour, M (2014) Evaluation bioactivity of a sea cucumber, Stichopus hermanni from Persian Gulf. European Journal of Experimental Biology 4, 254–258.Google Scholar
Selvi, P and Murugesh, S (2017) Identification of phytoconstituents from the methanolic extracts of Cissus arnottiana using GC-MS analysis. International Journal of Pharmaceutical and Biological Archive 6, 253–262.Google Scholar
Sharifi, M, Yegdaneh, A, Sajjadi, SE and Shushizadeh, M (2017) Identification and quantification of phthalate pollution in Holothuria atra: a sea cucumber from the Persian Gulf (Iran), Jundishapur. Journal of Natural Pharmaceutical Products 12, e65055.Google Scholar
Slater, MJ, Jeffs, AG and Sewell, MA (2011) Organically selective movement and deposit-feeding in juvenile sea cucumber, Australostichopus mollis determined in situ and in the laboratory. Journal of Experimental Marine Biology and Ecology 409, 315–323.CrossRefGoogle Scholar
Subavathy, P and Thilaga, RD (2016) GC-MS analysis of bioactive compounds from whole body tissue methanolic extract of Cypraea arabica (L. 1758). World Journal of Pharmaceutical Research 5, 800–806.Google Scholar
Torres, JRD (2017) Antibacterial and antifungal property of extracts derived from the body wall and cuvierian tubules of Pearsonothuria graeffei Semper (black-spotted sea cucumber). Frontiers in Medicinal Chemistry and Drug Discovery 1, 002–009.Google Scholar
Uthicke, S and Karez, R (1999) Sediment patch selectivity in tropical sea cucumbers (Holothuroidea: Aspidochirotida) analysed with multiple choice experiments. Journal of Experimental Marine Biology and Ecology 236, 69–87.CrossRefGoogle Scholar
Van Dyck, S, Gerbaux, P and Flammang, P (2009) Elucidation of molecular diversity and body distribution of saponins in the sea cucumber Holothuria forskali (Echinodermata) by mass spectrometry. Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology 152, 124–134.CrossRefGoogle ScholarPubMed
Vignaroli, C, Luna, GM, Rinaldi, C, Di Cesare, A, Danovaro, R and Biavasco, F (2012) New sequence types and multidrug resistance among pathogenic Escherichia coli isolates from coastal marine sediments. Applied and Environmental Microbiology 78, 3916–3922.CrossRefGoogle ScholarPubMed
Wargasetia, TL and Widodo, (2017) Mechanisms of cancer cell killing by sea cucumber-derived compounds. Investigational New Drugs 35, 820–826.CrossRefGoogle ScholarPubMed
Wolkenhauer, SM, Uthicke, S, Burridge, C, Skewes, T and Pitcher, R (2010) The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds. Journal of the Marine Biological Association of the United Kingdom 90, 215–223.CrossRefGoogle Scholar
Yang, J, Wang, C, Shu, C, Liu, L, Geng, J, Hu, S and Feng, J (2013) Marine sediment bacteria harbor antibiotic resistance genes highly similar to those found in human pathogens. Microbial Ecology 65, 975–981.CrossRefGoogle ScholarPubMed
Yeo, YL, Chia, YY, Lee, CH, Sow, HS and Yap, WS (2014) Effectiveness of maceration periods with different extraction solvents on in-vitro antimicrobial activity from fruit of Momordica charantia L. Journal of Applied Pharmaceutical Science 4, 016–023.Google Scholar
Zanwar, AA, Badole, SL, Shende, PS, Hegde, MV and Bodhankar, SL (2014) Antioxidant role of catechin in health and disease. In Watson, RR, Preedy, VR and Zibadi, S (eds), Polyphenols in Human Health and Disease. San Diego, CA: Elsevier, pp. 1045–1047.CrossRefGoogle Scholar
Zhang, SY, Yi, YH and Tang, HF (2006) Bioactive triterpene glycosides from the sea cucumber Holothuria fuscocinerea. Journal of Natural Products 69, 1492–1495.CrossRefGoogle ScholarPubMed
Zhang, H, Qing, W, Shilin, L, Da, H, Jianmin, Z, Libin, Z, Ye, Z, Lina, S and Hongsheng, Y (2019) Genomic and metagenomic insights into the microbial community in the regenerating intestine of the sea cucumber Apostichopus japonicas. Frontiers in Microbiology 10, 1165.CrossRefGoogle Scholar