Abstract
Previously, we reported seasonal variation in iodine contents in the seagrass Zostera marina. Herein, we sought the factors controlling this variation, and investigated relationships between iodine and carbohydrate contents, using extracts and residues of seagrass samples extracted with 0.1 N HCl. In plants, carbohydrates in HCl-extracted and residual fractions are considered to represent storage and structural carbohydrates, respectively. On average, 44% and 56% of total iodine in samples was contained in the HCl-extracted and residual fractions, respectively. Both HCl-extracted and residual iodine contents showed seasonal trends similar to that of total iodine, being high in winter–spring and low in summer. Total and HCl-extracted carbohydrate contents showed reverse seasonal trends from those of iodine, whereas residual carbohydrate contents had comparable values throughout the sampling period. In the total and HCl-extracted fractions, negative correlations between iodine and carbohydrate contents were confirmed, suggesting that carbohydrates do not play important roles in iodine accumulation. Although most monosaccharide contents were not correlated with iodine contents in these two fractions, residual galactose content was positively correlated with residual iodine. We accordingly suggest that one or more specific structural carbohydrate constituents may potentially function as an iodine store in Z. marina.
About the authors
Yuhi Satoh is a researcher at Institute for Environmental Sciences (Japan). His research fields are oceanography and radioecology, especially focused on organic matter and iodine dynamics. He has recently investigated the environmental dynamics of radionuclides released from a spent nuclear fuel reprocessing plant which is constructed in Rokkasho, Aomori, northeast Japan.
Shigeki Wada is an assistant professor in Shimoda Marine Research Center at University of Tsukuba (Japan). His research field is biological oceanography including dynamics of marine organic carbon in pelagic and benthic ecosystems. In addition, he has recently studied the effects of ocean acidification on marine ecosystems using mesocosm experiments and volcanic CO2 vents.
Shun’ichi Hisamatsu is a senior executive director of Institute for Environmental Sciences. He is originally a radio-chemist and has worked in radio-ecological research field for long years. He has supervised radioecological studies in the institute including environmental modeling and radiation dose assessment.
Acknowledgments
We wish to sincerely thank Dr. Shinji Ueda for providing insightful suggestions and advice for improving our manuscript. This study was carried out as part of a joint-research by the Japanese Association for Marine Biology (JAMBIO).
References
Alcoverro, T., M. Manzanera and J. Romero. 2001. Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Mar. Ecol. Prog. Ser. 211: 105‒116.10.3354/meps211105Search in Google Scholar
Aquino, R.S., A.M. Landeria-Fernandez, A.P. Valente, L.R. Andrade and P.A.S. Mourao. 2005. Occurrence of sulfated galactans in marine angiosperms: evolutionary implications. Glycobiology 15: 11‒20.10.1093/glycob/cwh138Search in Google Scholar PubMed
Burke, M.K., W.C. Dennison and K.A. Moore. 1996. Non-structural carbohydrate reserves of eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 137: 195‒201.10.3354/meps137195Search in Google Scholar
Caffall, K.H. and D. Mohnen. 2009. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohyd. Res. 344: 1879‒1990.10.1016/j.carres.2009.05.021Search in Google Scholar PubMed
Carpenter, L.J. 2003 Iodine in the marine boundary layer. Chem. Rev. 103: 4953‒4962.10.1021/cr0206465Search in Google Scholar PubMed
Chow, P.S. and S.M. Landhäusser. 2004. A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol. 24: 1129–1136.10.1093/treephys/24.10.1129Search in Google Scholar PubMed
Cosgrove, D.J. 2005. Growth of the plant cell wall. Nat. Rev. Mol. Cell. Biol. 6: 850‒861.10.1038/nrm1746Search in Google Scholar PubMed
Dawes, C.J. 1986. Seasonal proximate constituents and caloric values in seagrasses and algae on the West Coast of Florida. J. Coast. Res. 2: 25‒32.Search in Google Scholar
Feiters, M.C., F.C. Küpper and W. Meyer-Klaucke. 2005. X-ray absorption spectroscopic studies on model compounds for biological iodine and bromine. J. Synchrotron Rad. 12: 85–93.10.1107/S0909049504027815Search in Google Scholar PubMed
Fuge, R. and C.C. Johnson. 2015. Iodine and human health, the role of environmental geochemistry and diet, a review. Appl. Geochem. 63: 282‒302.10.1016/j.apgeochem.2015.09.013Search in Google Scholar
Hama, T. and K. Yanagi. 2001. Production and neutral aldose composition of dissolved carbohydrates excreted by natural marine phytoplankton populations. Limnol. Oceanogr. 46: 1945‒1955.10.4319/lo.2001.46.8.1945Search in Google Scholar
Harvey, G.R. 1980. A study of the chemistry of iodine and bromine in marine sediments. Mar. Chem. 8: 327‒332.10.1016/0304-4203(80)90021-3Search in Google Scholar
Hasegawa, H., H. Kakiuchi, N. Akata, Y. Ohtsuka and S. Hisamatsu. 2017. Regional and global contributions of anthropogenic iodine-129 in monthly deposition samples collected in North East Japan between 2006 and 2015. J. Environ. Radioact. 171: 65‒73.10.1016/j.jenvrad.2017.01.027Search in Google Scholar
Kalapahy, U. and A. Proctor 2001. Effect of acid extraction and alcohol precipitation conditions on the yield and purity of soy hull pectin. Food Chem. 73: 393‒396.10.1016/S0308-8146(00)00307-1Search in Google Scholar
Kikuchi, K., Y. Kawasaki and S. Sato. 2001. Effect of seasonal changes on the carbohydrate levels of eelgrass Zostera marina at Odawa Bay. Fish. Sci. 67: 755‒757.10.1046/j.1444-2906.2001.00317.xSearch in Google Scholar
Kristensen, E., R.M. Connolly, X.L. Otero, C. Marchand, T.O. Ferreira and V.H. Rivera-Monroy. 2017. Biogeochemical cycles: global approaches and perspectives. In: (Rivera-Monroy, V.H., S.Y. Lee, E. Kristensen and R.R. Twilley, eds) Mangrove ecosystems: a global biogeographic perspective. Springer, Netherlands. pp. 163–209.Search in Google Scholar
Küpper, F.C., L.J. Carpenter, G.B. McFiggans, C.J. Palmer, T.J. Waite, E. Boneberg, S. Woitsch, M. Weiller, R. Abela, D. Grolimund, P. Potin, A. Butler, G.W. Luther III, P.M.H. Kroneck, W. Meyer-Klaucke and M.C. Feiters. 2008. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc. Natl. Acad. 105: 6954–6958.10.1073/pnas.0709959105Search in Google Scholar
Hou, X., X. Yan and C. Chai. 2000. Chemical species of iodine in some seaweeds II. Iodine-bound biological macromolecules. J. Radioanal. Nucl. Chem. 245: 461‒467.10.1023/A:1006728420096Search in Google Scholar
Leblanc, C., C. Colin, A. Cosse, L. Delage, S. La Barre, P. Morin, B. Fiévet, C. Voiseux, Y. Ambroise, E. Verhaeghe, D. Amouroux, O. Donard, E. Tessier and P. Potin. 2006. Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidas. Biochimie 88: 1773‒1785.10.1016/j.biochi.2006.09.001Search in Google Scholar
Lyngby, J.E. and H. Brix. 1982. Seasonal and environmental variation in cadmium, copper, lead and zinc concentrations in eelgrass (Zostera marina L.) in the Limfjord, Denmark. Aquat. Bot. 14: 59‒74.10.1016/0304-3770(82)90086-9Search in Google Scholar
McNeil, M., A.G. Darvill, S.C. Fry and P. Albershein. 1984. Structure and function of the primary cell walls of plants. Ann. Rev. Biochem. 53: 625‒663.10.1146/annurev.bi.53.070184.003205Search in Google Scholar PubMed
Saiz-Lopez, A., J.M.C. Plane, A.R. Baker, J.L. Carpenter, R. von Glasow, J.C. Gomez-Martín, G. McFiggans and R.W. Saunders. 2012. Atmospheric chemistry of iodine. Chem. Rev. 112: 1773‒1804.10.1021/cr200029uSearch in Google Scholar PubMed
Satoh, Y. and S. Wada. 2020. Using organic compounds to assess the dominant controls on seasonal iodine variability in the brown alga Ecklonia cava in the northwestern Pacific coast of central Japan. J. Appl. Phycol. 32: 519–527.10.1007/s10811-019-01912-8Search in Google Scholar
Satoh, Y., S. Otosaka and T. Suzuki. 2014. Determination of total iodine concentration in aquatic environments using cathodic stripping voltammetry combined with sodium hypochlorite (NaClO) oxidation. J. Water Environ. Technol. 12: 201‒210.10.2965/jwet.2014.201Search in Google Scholar
Satoh, Y., S. Wada and S. Hisamatsu. 2018. Seasonal variations in iodine concentrations in a brown alga (Ecklonia cava Kjellman) and a seagrass (Zostera marina L.) in the northwestern Pacific coast of central Japan. J. Oceanogr. 74: 339‒445.10.1007/s10872-018-0479-8Search in Google Scholar
Satoh, Y., S. Ueda, H. Kakiuchi, Y. Ohtsuka and S. Hisamatsu. 2019. Concentrations of iodine-129 in coastal surface sediments around spent nuclear fuel reprocessing plant at Rokkasho, Japan, during and after its test operation. J. Radioanal. Nucl. Chem. 322: 2019‒2024.10.1007/s10967-019-06887-xSearch in Google Scholar
Shvaleva, A.L., F.C.E. Silva, E. Breia, J. Jouve, J.F. Hausman, M.H. Almeida, J.P. Maroco, M.L. Rodrigues, J.S. Pereira, M.M. Chaves. 2006. Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol. 26: 239‒248.10.1093/treephys/26.2.239Search in Google Scholar
Smith, D., G.M. Paulsen and C.A. Raguse. 1964. Extraction of total available carbohydrates from grass and legume tissue. Plant Physiol. 39: 960‒962.10.1104/pp.39.6.960Search in Google Scholar
Snyder, G., A. Aldahan and G. Possnert. 2010. Global distribution and long-term fate of anthropogenic 129I in marine and surface water reservoirs. Geochem. Geophys. Geosyst. 11: 1‒19.10.1029/2009GC002910Search in Google Scholar
Touchette, B.W. and J.M. Burkholder. 2000. Overview of the physiological ecology of carbon metabolism in seagrasses. J. Exp. Mar. Biol. Ecol. 250: 169‒205.10.1016/S0022-0981(00)00196-9Search in Google Scholar
Wang, Y.J., V.D. Trong and L. Wang. 2003. Structures and rheological properties of corn starch as affected by acid hydrolysis. Carbohyd. Polym. 52: 327‒333.10.1016/S0144-8617(02)00323-5Search in Google Scholar
Wong, G.T.F. 1982. The stability of molecular iodine in seawater. Mar. Chem. 11: 91‒95.10.1016/0304-4203(82)90051-2Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0004).
©2020 Walter de Gruyter GmbH, Berlin/Boston
