Chemical characterization and biochemical activity of polysaccharides isolated from Egyptian Ulva fasciata Delile

Moawad, Madelyn N.; El-Sayed, Abeer A.M.; Abd El Latif, Hala H.; El-Naggar, Naglaa A.; El-Din, Nihal G. Shams; Tadros, Hermine R.Z.

doi:10.1016/j.oceano.2021.09.008

Artykuł - szczegóły

Tytuł artykułu

Chemical characterization and biochemical activity of polysaccharides isolated from Egyptian Ulva fasciata Delile

Autorzy

Moawad Madelyn N. , El-Sayed Abeer A.M. , Abd El Latif Hala H. , El-Naggar Naglaa A. , El-Din Nihal G. Shams , Tadros Hermine R.Z.

Wybrane pełne teksty z tego czasopisma

Identyfikatory

DOI

10.1016/j.oceano.2021.09.008

Warianty tytułu

Języki publikacji

Abstrakty

This study gives updated information on the isolation of ulvan from green alga Ulva fasciata Delile in Egypt through isolation and chemical characterization of sulfate polysaccharides by two sequential extraction steps using different solvents; distilled water, HCl and Na2EDTA forming fraction I (F-I). Fraction II (F-II) was obtained from remaining seaweeds using NaOH to give FDWNaOH, FHClNaOH, and FEDTANaOH. All products obtained were tested for their biological activities. The highest polysaccharides total extraction yield was 11.8% for water extract (F-I and F-II). The highest protein content was found in FEDTANaOH (2.44%). The highest sulfate content was recorded for F-I (HCl) (21.38%). Total carbohydrates range was 11.99–63.90% for F-I and 15.06–76.65% for F-II. Monosaccharides; galactose, rhamnose, and uronic acid were detected at all fractions, with concentrations varying from 0.11 to 1.34%, from 0.61 to 1.81% and from 11.06 to 19.30%, respectively. 1H NMR of F-II demonstrated the signals of ring and methyl protons of polysaccharide. The appearance of the stretching bands of the sulfate ester (C-O-S) and sulfate groups (S=O) in the FT-IR spectrum of FHClNaOH confirmed the presence of sulfated polysaccharides, typical of ulvan. The microbial species Vibrio damsela was the most susceptible to FDWNaOH, followed by Aeromonas hydrophila and Vibrio fluvialis with inhibition zones of 30, 22, 22 mm at 150 mg/ml, respectively. FDWNaOH was the most effective fraction having antifouling property. The highest antioxidant activity was observed for F-IHCl followed by FDWNaOH. At concentrations 25 and 50 mg/l, FEDTANaOH displayed the highest anti-inflammatory activity (94.0 and 91.40%, respectively).

Słowa kluczowe

ulvan chemical composition biological activities FT-IR 1H NMR

Wydawca

Polish Academy of Sciences, Institute of Oceanology
Elsevier

Czasopismo

Oceanologia

Rocznik

2022

Tom

No. 64 (1)

Strony

117--130

Opis fizyczny

Bibliogr. 70 poz., rys., tab., wykr.

Twórcy

autor

Moawad Madelyn N.

National Institute of Oceanography and Fisheries, NIOF, Egypt

https://orcid.org/0000-0003-1751-8060

autor

El-Sayed Abeer A.M.

National Institute of Oceanography and Fisheries, NIOF, Egypt

https://orcid.org/0000-0002-8720-086X

autor

Abd El Latif Hala H.

National Institute of Oceanography and Fisheries, NIOF, Egypt

https://orcid.org/0000-0002-0543-3863

autor

El-Naggar Naglaa A.

National Institute of Oceanography and Fisheries, NIOF, Egypt
Department of Chemistry, College of Science, University of Hafr Al Batin, Hafr Al Batin, Saudi Arabia

https://orcid.org/0000-0001-6032-5606

autor

El-Din Nihal G. Shams

National Institute of Oceanography and Fisheries, NIOF, Egypt

autor

Tadros Hermine R.Z.

herminetadros@gmail.com

National Institute of Oceanography and Fisheries, NIOF, Egypt

https://orcid.org/0000-0002-2230-764X

Bibliografia

1. Abou El Azm, N., Fleita, D., Dalia, R.D., Mpingirika, E.Z., Amleh, A., Mayyada, El-S., MM, H., 2019. Production of bioactive compounds from the sulfated polysaccharides extracts of Ulva lactuca: post-extraction enzymatic hydrolysis followed by ion-exchange chromatographic fractionation. Molecules 24 (11), 2132. https://doi.org/10.3390/molecules24112132
2. Aleem, A.A., 1993. The marine algae of Alexandria, Egypt. Priv. Publ., Alexandria, 139 pp.
3. Alves, A., Sousa, R.A., Reis, R.L., 2013. A practical perspective on ulvan extracted from green algae. J. Appl. Phycol. 25, 407-424. https://doi.org/10.1007/s10811-012-9875-4
4. Arciola, C.R., Bustanji, Y., Conti, M., Campoccia, D., Baldassarri, L., Samori, B., Montanaro, L., 2003. Staphylococcus epidermidis — fibronectin binding and its inhibition by heparin. Biomaterials 24, 3013-3019. https://doi.org/10.1016/S0142-9612(03)00133-9
5. Boisvert, C., Beaulieu, L., Bonnet, C., Pelletier, É., 2015. Assessment of the antioxidant and antibacterial activities of three species of edible seaweeds. J. Food Biochem. 39, 377-387. https://doi.org/10.1111/jfbc.12146
6. Capo, X., Pettit, M.E., Conlan, S.L., Wagner, W., Ho, A.D., Clare, A.S., Callow, J.A., Callow, M.E., Grunze, M., Rosenhahn, A., 2009. Resistance of polysaccharide coatings to proteins, hematopoietic cells, and marine organisms. Biomacromolecules 10, 907-916. https://doi.org/10.1021/bm8014208
7. Costa, L.S., Fidelis, G.P., Cordeiro, S.L., Oliveira, R.M., Sabry, D.A., Câmara, R.B.G., Nobre, L.T.D.B., Costa, M.S.S.P., Almeida-Lima, J., Farias, E.H.C., Leite, E.L., Rocha, H.A.O., 2010. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed. Pharmacother. 64, 21-28.
8. Courtois, J., 2009. Oligosaccharides from land plants and algae: production and applications in therapeutics and biotechnology. Curr. Opin. Microbiol. 12, 261-273. https://doi.org/10.1016/j.mib.2009.04.007
9. Damsgard, B., Sorum, U., Ugelstad, I., Eliassen, R.A., Mortensen, A., 2004. Effects of feeding regime on susceptibility of Atlantic salmon (Salmosalar) to cold water vibriosis. Aquaculture 239, 37-46.
10. De Jesus Raposo, M.F., de Morais, A.M.B., de Morais, R.M.S.C., 2015. Marine polysaccharides from algae with potential biomedical applications. Mar. Drugs 13, 2967-3028. https://doi.org/10.3390/md13052967
11. De Jesus Raposo, M.F., de Morais, A.M.M.B., de Morais, R.M.S.C., 2014. Bioactivity and Applications of polysaccharides from marine microalgae. In: Merillon, J.-M., Ramawat, K.G. (Eds.), Polysaccharides: Bioactivity and Biotechnology. Springer, Cham.
12. https://doi.org/10.1007/978-3-319-03751-6_47-1
13. Del Olmo, A., Picon, A., Nuñez, M., 2018. The microbiota of eight species of dehydrated edible seaweeds from North West Spain. Food Microbiol. 70, 224-231. https://doi.org/10.1016/j.fm.2017.10.009
14. Dodgson, K.S., Price, R.C., 1962. A Note on the Determination of the Ester Sulfate Content of Sulfated Polysaccharides. Biochem. J. 84, 106-110. https://doi.org/10.1042/bj0840106
15. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956. Colorimetric method for the determination of sugars and related substances. Anal. Chem. 18, 350-356. https://doi.org/10.1021/ac60111a017
16. El-Baky, H.H.A., Baz, F.K.E., Baroty, G.S.E., 2009. Potential biological properties of sulphated polysaccharides extracted from the macroalgae Ulva lactuca L. Acad. J. Cancer Res. 2 (1), 1-11.
17. El-Masry, H.A., Fahmy, H.H., Abdelwahed, A.S.H., 2000. Synthesis and antimicrobial activity of some new benzimidazole derivatives. Molecules 5 (12), 1429-1438. https://doi.org/10.3390/51201429
18. Faradila, R.C.M., Gofarana, W., Hari, P.D., Nasrul, W., 2020. Ulvan, a polysaccharide from macroalgaUlva sp.: areview of chemistry, biological activities and potential for food and biomedical applications. Appl. Sci. 10 (16), 5488. https://doi.org/10.3390/app10165488
19. Faury, G., Molinari, J., Rusova, E., Mariko, B., Raveaud, S., Huber, P., Velebny, V., Robert, A.M., Robert, L., 2011. Receptors and aging: structural selectivity of the rhamnose-receptor on fibroblasts as shown by Ca2+ — mobilization and gene-expression profiles. Arch. Gerontol. Geriat. 53, 106-112. https://doi.org/10.1016/j.archger.2010.05.017
20. FDA, 1992. Bacteriological Analytical Manual, 7 edn., Food and Drug Administration (FDA), USA, 111-140.
21. Gadenne, V., Lebrun, L., Jouenne, T., Thebault, P., 2013. Antiadhesive activity of ulvan polysaccharides covalently immobilized onto titanium surface. Colloids Surf. B 112, 229-236. https://doi.org/10.1016/j.colsurfb.2013.07.061
22. Glasson, C.R.K., Sims, I.M., Carnachan, S.M., de Nys, R., Magnusson, M., 2017. A cascading biorefinery process targeting sulfated polysaccharides (ulvan) from Ulva ohnoi. Algal Res. 27, 383-391. https://doi.org/10.1016/j.algal.2017.07.001
23. Gomez, K.A., Gomez, A.A., 1984. Statistical procedures for agricultural research, 2nd. Edition John Wiley & Sons, New York, USA. ISBN: 978-0-471-87092-0
24. Guedes, É.A.C., da Silva, T.G., Aguiar, J.S., de Barros, L.D., Pinotti, L.M., Sant’Ana, A.E.G., 2013. Cytotoxic activity of marine algae against cancerous cells. Braz. J. Pharmacogn. 23, 668-673. https://doi.org/10.1590/S0102-695X2013005000060
25. Hernández-Garibay, E., Zertuche-González, J.A., Pacheco-Ruíz, I., 2010. Isolation and chemical characterization of algal polysaccharides from the green seaweed Ulva clathrata (Roth) C. Agardh. J. Appl. Phycol. 23, 537-542. https://doi.org/10.1007/s10811-010-9629-0
26. Huimin, Q., Quanbin, Z., Tingting, Z., Rong, C.H., Hong, Z., Xizhen, N., Zhien, L., 2005. Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. Int. J. Biol. Macromol. 37 (4), 195-199. https://doi.org/10.1016/j.ijbiomac.2005.10.008
27. Hussein, M.H., Hamouda, R.A., El-Naggar, N.El., Karim-Eldeen, M.A., 2015. Characterization, antioxidant, potentiality, and biological activities of the polysaccharideulvan extracted from the marine macroalga Ulva spp. J. Agric. Chem. Biotechn. Mansoura Univ. 6 (9), 373-392. https://doi.org/10.21608/jacb.2015.48435
28. Jiao, G., Yu, G., Wang, W., Zhao, X., Zhang, J., Ewart, S.H., 2012. Properties of polysaccharides in several seaweeds from Atlantic Canada and their potential anti-influenza viral activities. J. Ocean. Univ. China 11 (2), 205-212. https://doi.org/10.1007/s11802-012-1906-x
29. Kaeffer, B., Benard, C., Lahaye, M., Blottiere, H.M., Cherbut, C., 1999. Biological properties of ulvan, a new source of green seaweed sulfated polysaccharides, on cultured normal and cancerous colonic epithelial cells. Planta Med. 65, 527-531. https://doi.org/10.1055/s-1999-14009
30. Kellogg, J., Lila, M.A., 2013. Chemical and in vitro assessment of Alaskan coastal vegetation antioxidant capacity. J. Agric. Food Chem. 61 (46), 11025-11032. https://doi.org/10.1021/jf403697z
31. Kidgell, J.T., Magnussonb, M., de Nys, R., Glasson, C.R.K., 2019. Ulvan: A systematic review of extraction, composition and function. Algal Res. 39, 101422. https://doi.org/10.1016/j.algal.2019.101422
32. Kosanić., M., Ranković., B., Stanojković., T., 2015. Biological activities of two macroalgae from Adriatic coast of Montenegro. Saudi J. Biol. Sci. 22, 390-397. https://doi.org/10.1016/j.sjbs.2014.11.004
33. Kumaran, S., Radhakrishnan, M., Balagurunathan, R., 2011. Biofouling inhibitory substances from marine actinomycetes isolated from Palk Strait, India. Adv. Biotech. 12, 22-26.
34. Lahaye, M., 1998. NMR spectroscopic characterization of oligosaccharides from two Ulva rigidaulvan samples (Ulvales, Chlorophyta) degraded by a lyase. Carbohyd. Res. 314, 1-12.
35. Lahaye, M., Alvarez-Cabal Cimadevilla, E., Kuhlenkamp, R., Quemener, B., Lognone, V., Dion, P., 1999. Chemical composition and 13C NMR spectroscopic characterization of ulvans from Ulva (Ulvales, Chlorophyta). J. Appl. Phycol. 11, 1-7. https://doi.org/10.1023/A:1008063600071
36. Lahaye, M., Brunel, M., Bonnin, E., 1997. Fine chemical structure analysis of oligosaccharides produced by an ulvan-lyase degradation of the water-soluble cell wall polysaccharides from Ulva sp. (Ulvales, Chlorophyta). Carbohyd. Res. 304, 325-333. https://doi.org/10.1016/s0008-215(97)00270-x
37. Lahaye, M., Robic, A., 2007. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8, 1765-1774.
38. Leiro, J.M., Castro, R., Arranz, J.A., Lamas, J., 2007. Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh. Int. Immunopharmacol. 7, 879-888. https://doi.org/10.1016/j.intimp.2007.02.007
39. Li, Q., Luo, J., Wang, C., Tai, W., Wang, H., Zhang, X., Liu, K., Jia, Y., Lyv, X., Wang, L., He, H., 2018. Ulvan extracted from green seaweeds as new natural additives in diets for laying hens. J. Appl. Phycol. 30. https://doi.org/10.1007/s10811-017-1365-2
40. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., 1951. Protein measurement with folin phenol reagent. J. Biol. Chem. 193, 265-275. https://doi.org/10.1016/S0021-9258(19)52451-6
41. Massironi, A., Morelli, A., Grassi, L., Puppi, D., Braccini, S., Maisetta, G., Esin, S., Batoni, G., Della Pina, C., Chiellini, F., 2019. Ulvan as novel reducing and stabilizing agent from re-newable algal biomass: application to green synthesis of silver nanoparticles. Carbohyd. Polym. 203, 310-321. https://doi.org/10.1016/j.carbpol.2018.09.066
42. Matloub, A.A., El-Sherbini, M., Borai, I.H., Ezz, M.K., Rizk, M.Z., Aly, H.F., Fouad, G.I., 2013. assessment of anti-hyperlipidemic effect and physico-chemical characterization of water soluble polysaccharides from Ulva
43. Mizushima, Y., Kobayashi, M., 1968. Interaction of anti-inflammatory drugs with serum proteins, especially with some biologically active proteins. J. Pharm. Pharmacol. 20 (3), 169-173. https://doi.org/10.1111/j.2042-7158.1968.tb09718.x
44. Monsur, H.A., Jaswir, J., Simsek, S., Amid, A., Alam, Z., 2017. Chemical structure of sulfated polysaccharides from brown seaweed (Turbinariaturbinata). Int. J. Food Prop. 20 (7),1457-1469.
45. Morra, M., 2005. Engineering of biomaterials surfaces by hyaluronan. Biomacromolecules 6, 1205-1223. https://doi.org/10.1021/bm049346i
46. Mtolera, M.S.P., Semesi, A.K., 1996. Antimicrobial activity of extracts from six green algae from Tanzania. Curr. Trends Mar. Bot. Res. East Afr. Regul. 211-217. http://hdl.handle.net/1834/469
47. Murata, M., Nakazoe, J.I., 2001. Production and Use of Marine Algaein Japan. JARQ-Jpn. Agr. Res. Q. 35 (4), 281-290.
48. Paradossi, G., Cavalieri, F., Pizzoferrato, L., Liquori, A.M., 1999. A physico-chemical study on the polysaccharide ulvan from hot water extraction of the macroalga Ulva. Int. J. Biol. Macromol. 25, 309-315. https://doi.org/10.1016/s0141-8130(99)00049-5
49. Paulert, R., Junior, A.S., Stadnik, M.J., Pizzolatti, M.G., 2007. Antimicrobial properties of extracts from the green seaweed Ulva fasciata Delile against pathogenic bacteria and fungi. J. Algol. Stud. 123, 123-130. https://doi.org/10.1127/1864-1318/2007/0123-0123
50. Pengzhan, Y., Quanbin, Z., Ning, L., Zuhong, X., Yanmei, W., Zhi, L., 2003. Polysaccharides from Ulva pertusa (Chlorophyta) and preliminary studies on their antihyperlipidemia activity. J. Appl. Phycol. 15, 21-27. https://doi.org/10.1023/A:1022997622334
51. Plouguerné, E., da Gama, B.A.P., Pereira, R.C., Barreto-Bergter, E., 2014. Glycolipids from seaweeds and their potential biotechnological applications, Front. Cell. Infect. Microbiol. 4, 1-5. https://doi.org/10.3389/fcimb.2014.00174
52. Prieto, P., Pineda, M., Miguel Aguilar, M., 1999. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the de-termination of vitamin E. J. Anal. Biochem. 269 (2), 337-341. https://doi.org/10.1006/abio.1999.4019
53. Raja, R., Hemaiswarya, S., Arunkumar, K., Carvalho, I.S., 2016. Antioxidant activity and lipid profile of three seaweeds of Faro, Portugal. A Review, Bras. Bot. 39, 9-17. https://doi.org/10.1007/s40415-015-0200-8
54. Rashidi, B., Trindade, L.M., 2018. Detailed biochemical and morphologic characteristics of the green microalga Neochloris oleoabundans cell wall. Algal Res. 35, 152-159. https://doi.org/10.1016/j.algal.2018.08.033
55. Ray, B., Lahaye, M., 1995. Cell-wall polysaccharides from the marine green alga Ulva “rigida” (Ulvales, Chlorophyta). Chemical structure of ulvan, Carbohyd. Res. 274, 313-318. https://doi.org/10.1016/0008-6215(95)00059-3
56. Robic, A., Bertrand, D., Sassi, J.F., Lerat, Y., Lahaye, M., 2009a. Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. J. Appl. Phycol. 21, 451-456. https://doi.org/10.1007/s10811-008-9390-9
57. Robic, A., Gaillard, C., Sassi, J.F., Lerat, Y., Lahaye, M., 2009b. Ultrastructure of ulvan: a polysaccharides from green seaweed. Biopolymers 91, 652-664. https://doi.org/10.1002/bip.21195
58. Robic, A., Sassi, J.F., Lahaye, M., 2008. Impact of stabilization treatments of the green seaweed Ulva rotundata (Chlorophyta) on the extraction yield, the physico-chemical and rheological properties of ulvan. Carbohyd. Polym. 74, 344-352. https://doi.org/10.1016/j.carbpol.2008.02.020
59. Sakat, S., Juvekar, A.R., Gambhire, M.N., 2010. In vitro antioxidant and anti-inflammatory activityof methanol extract of Oxalis corniculata Linn, Inter. J. Pharm. Pharm. Sci. 2 (1), 146-155.
60. SAS, 2007. SAS Technical Report SAS/STAT software: Changes and Enhancements. Users’ Guide. Vol. 2, version 9.1.3, 4th edn., SAS Institute, Inc., Cary, NC. http://support.sas.com/thirdpartylicenses
61. Scoglio, M.E., Di Pietro, A., Picerno, I., Delia, S., Mauro, A., Lagana, P., 2001. Virulence factors in Vibrios and Aeromonads isolated from seafood. New Microbiolgy 24 (3), 273-280.
62. Selvin, J., Lipton, A.P., 2004. Biopotentials of Ulva fasciata and Hypnea musciformis collected from the peninsular coast of India. J. Mar. Sci. Technol. 12, 1-6. https://www.researchgate.et/publication/228766271
63. Silva, A., Silva, S.A., Carpena, M., Garcia-Oliveira, P., Gullón, P., FátimaBarroso, M., Prieto, M.A., Simal-Gandara, J., 2020. Macroalgae as a source of valuable antimicrobial compounds: extraction and applications. Antibiotics 9, 642. https://doi.org/10.3390/antibiotics9100642
64. Smit, A.J., 2004. Medicinal and pharmaceutical uses of seaweed natural products: a review. J. Appl. Phycol. 16, 245-262. https://doi.org/10.1023/B:JAPH.0000047783.36600.ef
65. Tabarsa, M., You, S.G., Dabaghian, E.H., Surayot, U., 2018. Watersoluble polysaccharides from Ulva intestinalis, Molecular properties, structural elucidation and immunomodulatory activities. J. Food Drug Anal. 26, 599-608. https://doi.org/10.1016/j.jfda.2017.07.016
66. Tako, M., Tamanaha, M., Tamashiro, Y., Uechi, S., 2015. Structure of Ulvan isolated from the edible green seaweed, Ulva pertusa. Adv. Biosci. Biotechnol. 6 (10), 645-655. https://doi.org/10.4236/abb.2015.610068
67. Wahlström, N., Nylander, F., Malmhäll-Bah, E., Sjövold, K., Edlund, U., Westman, G., Albers, E., 2020. Composition and structure of cell wall ulvans recovered from Ulva spp. along the Swedish west coast. Carbohyd. Polym. 233, 115852. https://doi.org/10.1016/j.carbpol.2020.115852
68. Wang, J., Zhang, Q., Zhang, Z., Li, Z., 2008. Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int. J. Biol. Macromol. 42 (2), 127-132. https://doi.org/10.1016/j.ijbiomac.2007.10.003
69. Wijesekara, I., Pangestuti, R., Kim, S.K., 2011. Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohyd. Polym. 84 (1), 14-21. https://doi.org/10.1016/j.carbpol.2010.10.062
70. Yaich, H., Amira, A.B., Abbes, F., Bouaziz, M., Besbes, S., Richel, A., Blecker, C., Attia, H., Garna, H., 2017. Effect of extraction procedures on structural, thermal and antioxidant properties of ulvan from Ulva lactuca collected in Monastir coast. Int. J. Biol. Macromol. 105 (2), 1430-1439. https://doi.org/10.1016/j.ijbiomac.2017.07.141

Uwagi

Opracowanie rekordu ze środków MEiN, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2022-2023).

Typ dokumentu

Bibliografia

Identyfikator YADDA

bwmeta1.element.baztech-845844a5-baa9-4800-982c-57756a1aa10d