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

Journal of Applied Phycology volume 32, pages519–527(2020)Cite this article

Abstract

Brown algal species are among the most efficient iodine accumulators and thus heavily influence the biogeochemical cycling of iodine in coastal environments. Previously, we reported seasonal variability in iodine concentrations in the brown alga Ecklonia cava collected from the Japanese coast over a 2-year period. In this study, we sought to identify the factors controlling this observed variability by investigating the relationships between the concentrations of iodine and major organic compounds (carbohydrates and fatty acids). The concentrations of total carbohydrates and individual constituent monosaccharides showed no significant correlations with iodine concentration, implying that carbohydrate concentration and composition are not the dominant controls on iodine concentration in E. cava. However, fucose concentrations were significantly correlated when data points of highest iodine concentrations were removed, potentially suggesting some influence of structural carbohydrate on iodine variability. Significant positive correlations with iodine concentration were only observed in odd-chain fatty acids, which are known to be bacterial biomarkers; in particular, the C17:1 fatty acid showed the highest correlation (r = 0.83). The concentrations of the remaining fatty acids, as well as total concentration of fatty acids, did not correlate significantly with iodine concentrations. Our results suggest that, in general, the concentration and composition of fatty acids do not directly influence iodine variability and that iodine concentrations in E. cava are predominantly controlled by bacteria living on its surface.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Amachi S, Mishima Y, Shinoyama H, Muramatsu Y, Fujii T (2005) Active transport and accumulation of iodide by newly isolated marine bacteria. Appl Environ Microbiol 71:741–745

    CAS  Article  Google Scholar 

  2. Ar Gall E, Küpper FC, Kloareg B (2004) A survey of iodine content in Laminaria digitata. Bot Mar 47:30–37

    CAS  Google Scholar 

  3. Armstrong E, Rogerdon A, Leftley JW (2000) The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar Coast Shelf Sci 50:415–424

    Article  Google Scholar 

  4. Barbeyron T, L’Haridon S, Michel G, Czjzek M (2008) Mariniflexile fucanivorans sp. nov., a marine member of the Flavobacteriaceae that degrades sulphated fucans from brown algae. Iut J Syst Evol Micr 58:2107–2113

    CAS  Article  Google Scholar 

  5. Bengtsson MM, Sjotub K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83

    Article  Google Scholar 

  6. Bianchi TS, Cannuel EA (2011) Chemical biomarkers in aquatic ecosystems. Princeton University Press, Princeton, p 396

    Google Scholar 

  7. Bisgrove SR, Kropf DL (2001) Cell wall deposition during morphogenesis in fucoid algae. Planta 212:648–658

    CAS  Article  Google Scholar 

  8. Carpenter LJ (2003) Iodine in the marine boundary layer. Chem Rev 103:4953–4962

    CAS  Article  Google Scholar 

  9. Charpy-Roubaud C, Sournia A (1990) The comparative estimation of phytoplanktonic, microphytobenthic and microphytobenthic primary production in the oceans. Mar Microb food webs 4:31–57

    Google Scholar 

  10. Dalsgaard J, John MS, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

  11. Descamps V, Colin S, Lahaye M, Jam M, Richard C, Potin P, Barbeyron T, Yvin JC, Kloareg B (2005) Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar Biotechnol 8:27–39

    Article  Google Scholar 

  12. Fleurence J, Gutbier G, Mabeau S, Leray C (1994) Fatty acids from 11 marine macroalgae of the French Brittany coast. J Appl Phycol 6(5–6):527–532. https://doi.org/10.1007/BF02182406

  13. Fuge R, Johnson CC (2015) Iodine and human health, the role of environmental geochemistry and diet, a review. Appl Geochem 63:282–302

    CAS  Article  Google Scholar 

  14. Hama T, Yanagi K (2001) Production and neutral aldose composition of dissolved carbohydrates excreted by natural marine phytoplankton populations. Limnol Oceanogr 46:1945–1955

    CAS  Article  Google Scholar 

  15. Haroun R, Yokohama Y, Aruga Y (1989) Annual growth cycle of the brown alga Ecklonia cava in central Japan. Sci Mar 53:349–356

    Google Scholar 

  16. Hasegawa H, Kakiuchi H, Akata N, Ohtsuka Y, Hisamatsu S (2017) Regional and global contributions of anthropogenic iodine-129 in monthly deposition samples collected in Northeast Japan between 2006 and 2015. J Environ Radioact 171:65–73

    CAS  Article  Google Scholar 

  17. Hou X, Yan X (1998) Study on the concentration and seasonal variation of inorganic elements in 35 species of marine algae. Sci Total Environ 222:141–156

    CAS  Article  Google Scholar 

  18. Kayama M, Araki S, Sato S (1989) Lipids of marine plants. In: Ackman RG (ed) Marine biogenic lipids, fats and oils. CRC Press, Boca Raton, p 348

    Google Scholar 

  19. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific coast of North California. Bot Mar 45:17–22

    CAS  Article  Google Scholar 

  20. Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ et al (2008) Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad 105:6954–6958

    Article  Google Scholar 

  21. Küpper FC, Carrano CJ (2019) Key aspects of the iodine metabolism in brown algae: a brief critical review. Metallomics 11:756–764

    Article  Google Scholar 

  22. Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Annu Rev Mar Sci 26:259–315

    Google Scholar 

  23. Leblanc C, Colin C, Cosse A, Delage L, la Barre S, Morin P, Fiévet B, Voiseux C, Ambroise Y, Verhaeghe E, Amouroux D, Donard O, Tessier E, Potin P (2006) Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidas. Biochimie 88:1773–1785

    CAS  Article  Google Scholar 

  24. Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80

    CAS  Article  Google Scholar 

  25. Nitschke U, Dixneuf S, Ruth AA, Schmid M, Stengel DB (2013) Molecular iodine (I2) emission from two Laminaria species (Phaeophyceae) and impact of irradiance and temperature on I2 emission into air and iodide release into seawater from Laminaria digitata. Mar Environ Res 92:102–109

    CAS  Article  Google Scholar 

  26. Nitschke U, Stengel DB (2014) Iodine contributes to osmotic acclimatisation in the kelp Laminaria digitata (Phaeophyceae). Planta 239:521–530

    CAS  Article  Google Scholar 

  27. Nitschke U, Stengel DB (2015) A new HPLC method for the detection of iodine applied to natural samples of edible seaweeds and commercial seaweed food products. Food Chem 172:326–334

    CAS  Article  Google Scholar 

  28. Nitschke U, Walsh P, McDaid J, Stengel DB (2018) Variability in iodine in temperate seaweeds and iodine accumulation kinetics of Fucus vesiculosus and Laminaria digitata (Phaeophyceae, Ochrophyta). J Phycol 54:114–125

    CAS  Article  Google Scholar 

  29. Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria—a dogma rewritten. Microbiol 145:767–779

    CAS  Article  Google Scholar 

  30. Saenko GN, Kravtsova YY, Ivanenko VV, Sheludko S (1978) Concentration of iodine and bromine by plants in the seas of Japan and Okhotsk. Mar Biol 47:243–250

    Article  Google Scholar 

  31. Saiz-Lopez A, Plane JMC, Baker AR, Carpenter JL, von Glasow R, Gomez-Martín JC, McFiggans G, Saunders RW (2012) Atmospheric chemistry of iodine. Chem Rev 112:1773–1804

    CAS  Article  Google Scholar 

  32. Satoh Y, Wada S, Hisamatsu S (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

    Article  Google Scholar 

  33. Snyder G, Aldahan A, Possnert G (2010) Global distribution and long-term fate of anthropogenic 129I in marine and surface water reservoirs. Geochem Geophys Geosyst 11:1–19

    Article  Google Scholar 

  34. Stiger-Pouvreau V, Bourgougnon N, Deslandes E (2016) Carbohydrates from seaweeds. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, NY pp, pp 223–274

    Google Scholar 

  35. Suzuki T, Otosaka S, Kuwabara J, Kawamura H, Kobayashi T (2013) Iodine-129 concentration in seawater near Fukushima before and after the accident at the Fukushima Daiichi Nuclear Power Plant. Biogeosciences 10:3839–3847

    Article  Google Scholar 

  36. Verhaeghe EF, Fraysse G-KJ, Wu T, Deves G et al (2008) Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem 13:257–269

    CAS  Article  Google Scholar 

  37. Yokohama Y, Tanaka J, Chihara M (1987) Productivity of the Ecklonia cava community in a bay of Izu Peninsula on the Pacific coast of Japan. Bot Mag Tokyo 100:129–141

    Article  Google Scholar 

  38. Yoshimura K, Ogawa T, Hama T (2009) Degradation and dissolution properties of photosynthetically-produced phytoplankton lipid materials in early diagenesis. Mar Chem 114:11–18

    CAS  Article  Google Scholar 

  39. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359

    Article  Google Scholar 

Download references

Acknowledgments

We wish to sincerely thank Dr. Shinji Ueda and Dr. Shun’ichi Hisamatsu for providing insightful suggestions and advice for improving our manuscript. This study was carried out as part of a joint research with the Japanese Association for Marine Biology (JAMBIO).

Author information

Affiliations

  1. Department of Radioecology, Institute for Environmental Sciences (IES), 1-7 Rokkasho, Aomori, 039-3212, Japan

    Yuhi Satoh

  2. Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda, Shizuoka, 422-0015, Japan

    Shigeki Wada

Authors
  1. Yuhi Satoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shigeki Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuhi Satoh.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 41 kb)

ESM 2

(DOCX 171 kb)

ESM 3

(DOCX 25.2 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Satoh, Y., Wada, S. 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 (2020). https://doi.org/10.1007/s10811-019-01912-8

Download citation

Keywords

  • Iodine
  • Phaeophyta
  • Ecklonia cava
  • Carbohydrate
  • Fatty acid
  • Bacteria