Abstract
Sea cucumbers are marine organisms with uses in food, cosmetics, and medicine. This study aimed to identify Indonesian sea cucumbers with high antioxidant and antibacterial activities. Twenty-one sea cucumber species were used for this study. Antioxidant capacity was evaluated using the 2,2-diphenyl-β-picrylhydrazine assay. Antibacterial activity was assessed using the disk diffusion assay, whereas the resazurin-based assay was employed to determine the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). Volatile compounds possibly related to the biological activity of sea cucumbers were analyzed via gas chromatography–mass spectrometry (GC–MS). Holothuria atra had the strongest antioxidant capacity (IC50 = 14.22 ± 0.87 µg µL−1). Stichopus vastus displayed the best antibacterial activity against Staphylococcus aureus, whereas Stichopus ocellatus extract was most potent against Vibrio cholerae. Holothuria albiventer, which controlled Bacillus subtilis most effectively while also being active against S. aureus and V. cholerae, was the optimal antimicrobial species. H. albiventer and Actinopyga echinites inhibited B. subtilis growth at 12.5 µg µL−1. The MBC tests indicated that the antibacterial activities of sea cucumbers at the MIC were bacteriostatic, rather than bactericidal, in nature. GC–MS analysis uncovered long-chain fatty acids that might be associated with the antibacterial activities of sea cucumbers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article.
References
Abdille MdH, Singh RP, Jayaprakasha GK, Jena BS (2005) Antioxidant activity of the extracts from Dillenia indica fruits. Food Chem 90:891–896. https://doi.org/10.1016/j.foodchem.2004.09.002
Abraham TJ, Nagarajan J, Shanmugam SA (2002) Antimicrobial substance of potential biomedicinal importance from holothurian species. Indian J Mar Sci 31:161–164
Adibpour N, Nasr F, Nematpour F, Shakouri A, Ameri A (2014) Antibacterial and antifungal activity of Holothuria leucospilota isolated from Persian gulf and Oman sea. Jundishapur J Microbiol 7:1–4. https://doi.org/10.5812/jjm.8708
Ak T, Gulcin I (2008) Antioxidant and radical scavenging properties of curcumin. Chem Biol Interact 174:27–37. https://doi.org/10.1016/j.cbi.2008.05.003
Al-Rubaye AF, Hameed IH, Kadhim MJ (2017) A review: Uses of gas chromatography-mass spectrometry (GC-MS) technique for analysis of bioactive natural compounds of some plants. Int J Toxicol Pharmacol Res 9:81–85. https://doi.org/10.25258/ijtpr.v9i01.9042
Althunibat OY, Hashim RB, Taher M, Daud JM, Ikeda M, Zali BI (2009) In vitro antioxidant and antiproliferative activities of three Malaysian sea cucumber species. Eur J Sci Res 37:376–387
Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16. https://doi.org/10.1093/jac/48.suppl_1.5
Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200. https://doi.org/10.1038/1811199a0
Bordbar S, Anwar F, Saari N (2011) High-value components and bioactives from sea cucumbers for functional foods—a review. Mar Drugs 9:1761–1805. https://doi.org/10.3390/md9101761
Chasanah E, Fawzya YN, Tarman K, Januar HI, Nursid M (2016) Fatty acid profile, carotenoid content, and in vitro anticancer activity of Karimunjawa and Lampung sea cucumber. Squalen Bull Mar Fish Postharvest Biotechnol 11:117–124. https://doi.org/10.15578/squalen.v11i3.269
Dhinakaran DI, Lipton AP (2014) Bioactive compounds from Holothuria atra of indian ocean. Springer Plus 3:1–10. https://doi.org/10.1186/2193-1801-3-673
Elshikh M, Ahmed S, Funston S, Dunlop P, McGaw M, Marchant R, Banat IM (2016) Resazurin-based 96-well plate microdilution method for the determination of minimum inhibitory concentration of biosurfactants. Biotechnol Lett 38:1015–1019. https://doi.org/10.1007/s10529-016-2079-2
Esmat AY, Said MM, Soliman AA, El-Masry KSH, Badiea EA (2013) Bioactive compounds, antioxidant potential, and hepatoprotective activity of sea cucumber (Holothuria atra) against thioacetamide intoxication in rats. Nutrition 29:258–267. https://doi.org/10.1016/j.nut.2012.06.004
Farjami B, Nematollahi MA, Moradi Y, Irajian G, Nazemi M, Ardebili A, Pournajaf A (2015) Antibacterial activity of the sea cucumber Holothuria leucospilota. Int J Mol Clin Microbiol 1:225–230
Gulcin I (2006) Antioxidant activity of caffeic acid (3,4-dihydroxycinnamic acid). Toxicology 217:213–220. https://doi.org/10.1016/j.tox.2005.09.011
Gulcin I (2011) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391. https://doi.org/10.1007/s00204-011-0774-2
Gulcin I, Kirecci E, Akkemik E, Topal F, Hisar O (2010) Antioxidant, antibacterial, and anticandidal activities of an aquatic plant: Duckweed (Lemna minor L. Lemnaceae). Turk J Biol 34:175–188. https://doi.org/10.3906/biy-0806-7
Hossain MA, Shah MD (2015) A study on the total phenols content and antioxidant activity of essential oil and different solvent extracts of endemic plant Merremia borneensis. Arab J Chem 8:66–71. https://doi.org/10.1016/j.arabjc.2011.01.007
Jones WP, Kinghom AD (2006) Extraction of plant secondary metabolites. In: Sarker SJ, Latif Z, Gray AI (eds) Natural products isolation, 2nd edition. Humana Press Inc., Totowa, New Jersey, pp 323–351
Jorgensen JH, Ferraro MJ (2009) Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Infect Dis 49:1749–1755. https://doi.org/10.1086/647952
Kasanah N, Triyanto SDS, Amalia W, Isnansetyo A (2015) Antibacterial compounds from red seaweeds (rhodophyta). Indones J Chem 15:201–209. https://doi.org/10.22146/ijc.21215
Manilal A, Sujith S, Kiran GS, Selvin J, Shakir C, Gandhimathi R, Lipton AP (2009) Antimicrobial potential and seasonality of red algae 23 collected from the southwest coast of india tested against shrimp, human and phytopathogens. Ann Microbiol 59:207–219. https://doi.org/10.1007/BF03178319
Manu D, Lupan I, Popescu O (2011) Mechanisms of pathogenesis and antibiotics resistance in Escherichia coli. Ann Rom Soc Cell Biol 16:7–19
Moran LF, Aronsson Bo, Manz C, Gyssens IC, Sob AD, Monnet DL, Cars O (2011) Critical shortage of new antibiotics in development against multidrug resistant bacteria - time to react is now. Drug Resist Update 14:118–124. https://doi.org/10.1016/j.drup.2011.02.003
Mujeeb F, Bajpai P, Pathak N (2014) phytochemical evaluation, antimicrobial activity, and determination of bioactive components from leaves of Aegle marmelos. Bio Med Res Int 497606:1–11. https://doi.org/10.1155/2014/497606
Murniasih T, Putra MY, Pangestuti R (2015) Antioxidant capacities of Holothuria sea cucumbers. Ann Bogor 19:21–26. https://doi.org/10.14203/ann.bogor.2015.v19.n2.21-26
Nemeth J, Oesch G, Kuster SP (2014) Bacteriostatic versus bactericidal antibiotics for patients with serious bacterial infections: systematic review and meta-analysis. J Antimivrobial Chemotheraphy Adv Access 10:1–14. https://doi.org/10.1093/jac/dku379
Nobsathian S, Tuchinda P, Sobhon P, Tinikul Y, Poljaroen J, Tinikul R, Sroyraya M, Poomton T, Chaichotranunt S (2017) An antioxidant activity of the whole body of Holothuria scabra. Chem Biol Technol Agric 4:1–5. https://doi.org/10.1186/s40538-017-0087-7
Omar HH, Shiekh HM, Gumgumjee NM, El-Kazan MM, El-Gendy AM (2012) Antibacterial activity of extracts of marine algae from the red sea of Jeddah, Saudi Arabia. Afr J Biotechnol 11:13576–13585. https://doi.org/10.5897/AJB12.780
Pangestuti R, Arifin Z (2017) Medicinal and health benefit effects of functional sea cucumbers. J Trad Complement Med 8:341–351. https://doi.org/10.1016/j.jtcme.2017.06.007
Pangestuti R, Murniasih T, Putra MY, Rasyid A, Wibowo JT, Ardiansyah A, Untari F (2016) Free radical scavenging activity of selected sea cucumber species from Mataram-Lombok, Indonesia. J Teknol Sci Eng 78:179–185. https://doi.org/10.11113/jt.v78.8202
Pringgenies D, Ridlo A, Sembiring N (2017) Antibacterial activity for multi drug resistance (MDR) bacteria bysea cucumber stichopus vastus extract from Karimunjawa islands—Indonesia. J Ilmu dan Teknologi Kelautan Tropis 9:695–707. https://doi.org/10.29244/jitkt.v9i2.19302
Qi H, Ji X, Liu S, Feng D, Dong X, He B, Srinivas J, Yu C (2017) Antioxidant and anti-dyslipidemic effects of polysaccharidic extract from sea cucumber processing liquor. Electron J Biotechnol 28:1–6. https://doi.org/10.1016/j.ejbt.2017.04.001
Radjasa OK, Urakawa H, Kita-Tsukamoto K, Ohwada K (2001) Characterization of psychotropic bacteria in the surface and deep-sea waters from Northwestern Pacific Ocean based on 16S ribosomal DNA approach. Mar Biotechnol 3:454–462. https://doi.org/10.1007/s10126-001-0050-1
Rasyid A, Wahyuningsih T, Ardiansyah A (2018) Profil metabolit sekunder, aktivitas antibakteri dan komposisi senyawa yang terkandung dalam ekstrak methanol teripang Stichopus horrens. J Ilmu dan Teknologi Kelautan Tropis 10:333–340. https://doi.org/10.29244/jitkt.v10i2.19480
Sanchez JGB, Kouznetsov VV (2010) Antimycobacterial susceptibility testing methods for natural products research. Brazil J Microbiol 41:270–277. https://doi.org/10.1590/S1517-83822010000200001
Sanchez-Moreno C, Larrauri JA, Saura-Calixto F (1998) A procedure to measure the antiradical efficiency of polyphenols. J Sci Food Agric 76:270–276. https://doi.org/10.1002/(SICI)1097-0010(199802)76:2%3C270::AID-JSFA945%3E3.0.CO;2-9
Sandle T (2016) Antibiotics and preservatives. Pharm Microbiol. https://doi.org/10.1016/b978-0-08-100022-9.00014-1
Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in IHE in vitro antibacterial screening of phytochemicals. Methods J 42:321–324. https://doi.org/10.1016/j.ymeth.2007.01.006
Soltani M, Baharara J (2014) Antioxidant and antiproliferative capacity of dichloromethane extract of Holoturia leucospilota sea cucumber. Int J Cell Mol Biotechnol 204:1–9. https://doi.org/10.5899/2014/ijcmb-00013
Spızek J, Novotna J, Ezanka TR, Demain AL (2010) Do we need new antibiotics? The search for new targets and new compounds. J Ind Microbiol Biotechnol 37:1241–1248. https://doi.org/10.1007/s10295-010-0849-8
Sukmiwati M, Diharmi A, Mora E, Susanti E (2018) Aktivitas antimikroba teripang kasur (Stichopus vastus Sluiter) dari Perairan Natuna Kepulauan Riau. J Pengolahan Hasil Perikanan Indonesia 21:328–335. https://doi.org/10.17844/jphpi.v21i2.23088
Sukmiwati M, Ilza M, Putri AE, Sidauruk SW (2019) Antibacterial activity of sea cucumber (Holothuria atra) against Pseudomonas aeruginosa. IOP Conf Ser Earth Environ Sci 012047:1–6. https://doi.org/10.1088/1755-1315/404/1/012047
Sveinsdottir H, Hamaguchi PY, Bakken HE, Kristinsson HG (2014) Method for assessing the antioxidative activity of aquatic food compounds. In: Hordur GK (ed) Antioxidant and functional component in aquatic foods. Wiley, New York, pp 151–174. https://doi.org/10.1002/9781118855102.ch6
Telahigue K, Ghali R, Nouiri E, Labidi A, Hajji T (2020) Antibacterial activities and bioactive compounds of the ethyl acetate extract of the sea cucumber Holothuria forskali from Tunisian coasts. J Mar Biol Assoc UK. https://doi.org/10.1017/s0025315420000016
Tuem KB, Gebre AK, Atey TM, Bitew H, Yimer EM, Berhe DF (2018) Drug resistance patterns of Escherichia coli in ethiopia: a meta-analysis. BioMed Res Int. https://doi.org/10.1155/2018/4536905
Yoon BK, Valle-González JJA, ER, Cho NJ, (2018) Antibacterial free fatty acids and monoglycerides: biological activities, experimental testing, and therapeutic applications. Int J Mol Sci 19:1–40. https://doi.org/10.3390/ijms19041114
Zheng CJ, Yoo JS, Lee TG, Cho HY, Kim YH, Kim WG (2005) Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett 579:5157–5162. https://doi.org/10.1016/j.febslet.2005.08.028
Acknowledgements
The authors would like to thank EnagoTM English Editing Service for editing a draft of this manuscript.
Funding
This research was supported by a research grant awarded to Masteria Yunovilsa Putra by the Coral Reef Rehabilitation and Management Program-Coral Triangle Initiative (COREMAP-CTI) 2019 and National Research Priority (PRN), Indonesian Institute of Sciences.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by AN, IAH, AB, ARA, AS, MYP. The first draft of the manuscript were written by AN, AB, TM and MYP and all authors reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Human and animal rights
This article does not contain any studies with human or animal subjects.
Informed consent
This article does not contain any individual person’s data in any form.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Aji Nugroho, Iskandar Azmy Harahap, and Ardi Ardiansyah are contributed equally.
Rights and permissions
About this article
Cite this article
Nugroho, A., Harahap, I.A., Ardiansyah, A. et al. Antioxidant and antibacterial activities in 21 species of Indonesian sea cucumbers. J Food Sci Technol 59, 239–248 (2022). https://doi.org/10.1007/s13197-021-05007-6
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-021-05007-6