Effect of environmental parameters on the content and sugar composition of sulfated polysaccharides in some tropical seagrass

Vy Xuan Nguyen; Nhu Thuy Nguyen Nhat; Xuan Thuy Nguyen; Khanh Hy Le Ho; Duc Thinh Pham; Viet Ha Dao

doi:10.15625/1859-3097/18053

Author affiliations

Authors

Xuan-Vy Nguyen Institute of Oceanography, VAST, Vietnam; Graduate University of Science and Technology, VAST, Vietnam https://orcid.org/0000-0002-7260-5127
Nhu-Thuy Nguyen-Nhat Institute of Oceanography, VAST, Vietnam
Xuan-Thuy Nguyen Institute of Oceanography, VAST, Vietnam
Khanh-Hy Le-Ho Institute of Oceanography, VAST, Vietnam
Duc-Thinh Pham Nha Trang Institute of Technology Research and Aplication, Nha Trang city, Khanh Hoa, Vietnam
Viet-Ha Dao Institute of Oceanography, VAST, Vietnam; Graduate University of Science and Technology, VAST, Vietnam

DOI:

https://doi.org/10.15625/1859-3097/18053

Keywords:

Functional groups, salinity, seagrass, sulfated polysaccharides.

Abstract

Seagrasses are a paraphyletic group of marine angiosperms that evolved three to four times from land plants and returned to the sea. Halophila ovalis, Thalassia hemprichii and Enhalus acoroides (Hydrocharitaceae) are species that can occur in wide salinity ranges. Sulfated polysaccharides (SPs) comprise a complex group of macromolecules with many critical biological functions. We assume that SP may play a role in salt tolerance in seagrass. In this study, three seagrass species collected in both rainy and dry seasons from the fields were analyzed to determine the total SP contents and different functional groups of SP. Quantification of total SP was done by photometric assays. High-performance anion-exchange chromatography with Pulsed Electrochemical Detection (HPAEC) determined different functional groups of SPs. The results indicated higher total SP contents in seagrass are present in plants at higher salinities and environmental temperatures. The percent of functional groups of SPs are present in the following order: glucose > galactose > arabinose > mannose > rhamnose > fucose. The order is not different between the two seasons.

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References

Les, D. H., Cieland, M. A., and Vvaycott, M., 1997. Phylogenetic Studies in Alismatidae, II: Evolution of Marine Angiosperms (Seagrasses) and Hydrophily. Systematic Botany, 22(3), 443–463. DOI: https://doi.org/10.2307/2419820

Papenbrock, J., 2012. Highlights in Seagrasses’ Phylogeny, Physiology, and Metabolism: What Makes Them Special?. ISRN Botany, 2012(7), 103892. DOI: https://doi.org/10.5402/2012/103892

Papazian, S., Parrot, D., Burýšková, B., Weinberger, F., and Tasdemir, D., 2019. Surface chemical defence of the eelgrass Zostera marina against microbial foulers. Scientific Reports, 9(1), 3323. DOI: https://doi.org/10.1038/s41598-019-39212-3

Zidorn, C., 2016. Secondary metabolites of seagrasses (Alismatales and Potamogetonales; Alismatidae): Chemical diversity, bioactivity, and ecological function. Phytochemistry, 124, 5–28. DOI: https://doi.org/10.1016/j.phytochem.2016.02.004

Lee, H., Golicz, A. A., Bayer, P. E., Severn-Ellis, A. A., Chan, C. K. K., Batley, J., Kendrick, G. A., and Edwards, D., 2018. Genomic comparison of two independent seagrass lineages reveals habitat-driven convergent evolution. Journal of experimental botany, 69(15), 3689–3702. DOI: https://doi.org/10.1093/jxb/ery147

Olsen, J. L., Rouzé, P., Verhelst, B., Lin, Y. C., Bayer, T., Collen, J., Dattolo, E., De Paoli, E., Dittami, S., Maumus, F., Michel, G., Kersting, A., Lauritano, C., Lohaus, R., Töpel, M., Tonon, T., Vanneste, K., Amirebrahimi, M., Brakel, J., Boström, C., Chovatia, M., Grimwood, J., Jenkins, J. W., Jueterbock, A., Mraz, A., Stam, W. T., Tice, H., Bornberg-Bauer, E., Green, P. J., Pearson, G. A., Procaccini, G., Duarte, C. M., Schmutz, J., Reusch, T. B. H., and Van de Peer, Y., 2016. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 530(7590), 331–335. DOI: https://doi.org/10.1038/nature16548

Cock, J. M., Sterck, L., Rouzé, P., Scornet, D., Allen, A. E., Amoutzias, G., Anthouard, V., Artiguenave, F., Aury, J. M., Badger, J. H., Beszteri, B., Billiau, K., Bonnet, E., Bothwell, J. H., Bowler, C., Boyen, C., Brownlee, C., Carrano, C. J., Charrier, B., Cho, G. Y., Coelho, S. M., Collén, J., Corre, E., Silva, C. D., Delage, L., Delaroque, N., Dittami, S. M., Doulbeau, S., Elias, M., Farnham, G., Gachon, C. M. M., Gschloessl, B., Heesch, S., Jabbari, K., Jubin, C., Kawai, H., Kimura, K., Kloareg, B., Küpper, F. C., Lang, D., Bail, A. L., Leblanc, C., Lerouge, P., Lohr, M., Lopez, P. J., Martens, C., Maumus, F., Michel, G., Miranda-Saavedra, D., Morales, J., Moreau, H., Motomura, T., Nagasato, C., Napoli, C. A., Nelson, D. R., Nyvall-Collén, P., Peters, A. F., Pommier, C., Potin, P., Poulain, J., Quesneville, H., Read, B., Rensing, S. A., Ritter, A., Rousvoal, S., Samanta, M., Samson, G., Schroeder, D. C., Ségurens, B., Strittmatter, M., Tonon, T., Tregear, J. W., Valentin, K., von Dassow, P., Yamagishi, T., Van de Peer, Y., and Wincker, P., 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465(7298), 617–621. DOI: https://doi.org/10.1038/nature09016

Nguyen, X. V., Klein, M., Riemenschneider, A., and Papenbrock, J., 2014. Distinctive features and role of sulfur-containing compounds in marine plants, seaweeds, seagrasses and halophytes, from an evolutionary point of view. Sabkha Ecosystems: Volume IV: Cash Crop Halophyte and Biodiversity Conservation, 299–312. DOI: https://doi.org/10.1007/978-94-007-7411-7_21

Patel, S., 2012. Therapeutic importance of sulfated polysaccharides from seaweeds: updating the recent findings. 3 Biotech, 2(3), 171–185. DOI: https://doi.org/10.1007/s13205-012-0061-9

Coombe, D. R., and Parish, C. R., 1988. Sulfated Polysaccharide-Mediated Sponge Cell Aggregation: The Clue to Invertebrate Self/Nonself-Recognition?. In Invertebrate historecognition (pp. 31–54). Boston, MA: Springer US. doi: 10.1007/978-1-4613-1053-2_3 DOI: https://doi.org/10.1007/978-1-4613-1053-2_3

Yamada, S., Sugahara, K., and Özbek, S., 2011. Evolution of glycosaminoglycans: Comparative biochemical study. Communicative & integrative biology, 4(2), 150–158. DOI: https://doi.org/10.4161/cib.4.2.14547

Patel, S., 2018. Seaweed-derived sulfated polysaccharides: scopes and challenges in implication in health care. In Bioactive seaweeds for food applications (pp. 71–93). Academic Press. DOI: https://doi.org/10.1016/B978-0-12-813312-5.00004-2

Aquino, R. S., Landeira-Fernandez, A. M., Valente, A. P., Andrade, L. R., and Mourao, P. A., 2005. Occurrence of sulfated galactans in marine angiosperms: evolutionary implications. Glycobiology, 15(1), 11-20. DOI: https://doi.org/10.1093/glycob/cwh138

Dantas-Santos, N., Gomes, D. L., Costa, L. S., Cordeiro, S. L., Costa, M. S. S. P., Trindade, E. S., Franco, C. R. C., Scortecci, K. C., Leite, E. L., and Rocha, H. A. O., 2012. Freshwater plants synthesize sulfated polysaccharides: heterogalactans from water hyacinth (Eicchornia crassipes). International Journal of Molecular Sciences, 13(1), 961–976. DOI: https://doi.org/10.3390/ijms13010961

Aquino, R. S., Grativol, C., and Mourão, P. A., 2011. Rising from the sea: correlations between sulfated polysaccharides and salinity in plants. PloS one, 6(4), e18862. DOI: https://doi.org/10.1371/journal.pone.0018862

Ciancia, M., Fernández, P. V., and Leliaert, F., 2020. Diversity of sulfated polysaccharides from cell walls of coenocytic green algae and their structural relationships in view of green algal evolution. Frontiers in plant science, 11, 554585. DOI: https://doi.org/10.3389/fpls.2020.554585

Nader, H. B., Medeiros, M. G., Paiva, J., Paiva, V. M., Jerônimo, S. M., Ferreira, T. M., and Dietrich, C. P., 1983. A correlation between the sulfated glycosaminoglycan concentration and degree of salinity of the “habitat” in fifteen species of the classes Crustacea, Pelecypoda and Gastropoda. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 76(3), 433–436. DOI: https://doi.org/10.1016/0305-0491(83)90271-7

Dittami, S. M., Gravot, A., Goulitquer, S., Rousvoal, S., Peters, A. F., Bouchereau, A., Boyen, C., and Tonon, T., 2012. Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae). The Plant Journal, 71(3), 366–377. DOI: https://doi.org/10.1111/j.1365-313X.2012.04982.x

Ferreira, A. S., Mendonça, I., Povoa, I., Carvalho, H., Correia, A., Vilanova, M., Silva, T. H., Coimbra, M. A., and Nunes, C., 2021. Impact of growth medium salinity on galactoxylan exopolysaccharides of Porphyridium purpureum. Algal Research, 59, 102439. DOI: https://doi.org/10.1016/j.algal.2021.102439

Bunsom, C., and Prathep, A., 2012. Effects of salinity, light intensity and sediment on growth, pigments, agar production and reproduction in Gracilaria tenuistipitata from Songkhla lagoon in Thailand. Phycological research, 60(3), 169–178. DOI: https://doi.org/10.1111/j.1440-1835.2012.00648.x

Sfriso, A. A., Gallo, M., and Baldi, F., 2017. Seasonal variation and yield of sulfated polysaccharides in seaweeds from the Venice lagoon. Botanica marina, 60(3), 339–349. DOI: https://doi.org/10.1515/bot-2016-0063

Yuvaraj, N., and Arul, V., 2018. Sulfated polysaccharides of seagrass Halophila ovalis suppresses tumor necrosis factor-α-induced chemokine interleukin-8 secretion in HT-29 cell line. Indian Journal of Pharmacology, 50(6), 336–343. DOI: https://doi.org/10.4103/ijp.IJP_202_18

Mettwally, W. S., Ragab, T. I., Hamdy, A. H. A., Helmy, W. A., and Hassan, S. A., 2021. Preliminary study on the possible impact of Thalassodendron ciliatum (Forss.) den Hartog acidic polysaccharide fractions against TAA induced liver failure. Biomedicine & Pharmacotherapy, 138, 111502. DOI: https://doi.org/10.1016/j.biopha.2021.111502

Kolsi, R. B. A., Fakhfakh, J., Krichen, F., Jribi, I., Chiarore, A., Patti, F. P., Blecker, C., Allouche, N., Belghith, H., and Belghith, K., 2016. Structural characterization and functional properties of antihypertensive Cymodocea nodosa sulfated polysaccharide. Carbohydrate Polymers, 151, 511–522. DOI: https://doi.org/10.1016/j.carbpol.2016.05.098

Silva, J., Dantas-Santos, N., Gomes, D. L., Costa, L. S., Cordeiro, S. L., Costa, M. S., Silva, N. B., Freitas, M. L., Scortecci, K. C., Leite, E. L., and Rocha, H. A., 2012. Biological activities of the sulfated polysaccharide from the vascular plant Halodule wrightii. Revista Brasileira de Farmacognosia, 22, 94–101. DOI: https://doi.org/10.1590/S0102-695X2011005000199

Pfeifer, L., Shafee, T., Johnson, K. L., Bacic, A., and Classen, B., 2020. Arabinogalactan-proteins of Zostera marina L. contain unique glycan structures and provide insight into adaption processes to saline environments. Scientific reports, 10(1), 8232. DOI: https://doi.org/10.1038/s41598-020-65135-5

Pfeifer, L., 2021. “Neptune balls” polysaccharides: Disentangling the wiry seagrass detritus. Polymers, 13(24), 4285. DOI: https://doi.org/10.3390/polym13244285

Pfeifer, L., and Classen, B., 2020. The cell wall of seagrasses: Fascinating, peculiar and a blank canvas for future research. Frontiers in plant science, 11, 588754. DOI: https://doi.org/10.3389/fpls.2020.588754