Iodine, bromine and arsenic uptake, accumulation and efflux in three ecologically important Southern Hemisphere brown algae: Durvillaea antarctica, Macrocystis pyrifera and Lessonia trabeculata
-
Abstract
With a few exceptions, knowledge about halogen and arsenic metabolism is limited to Northern Hemisphere taxa. This study explores the uptake, accumulation and efflux of iodine in three of the most common Southern Hemisphere brown algae: Durvillaea antarctica, Macrocystis pyrifera and Lessonia trabeculatα. All three brown algal species investigated here showed measurable iodine uptake in steady state conditions and, conversely, iodine efflux during oxidative stress. The two species of Laminariales, Lessonia (6.7–19 mmol I kg−1 DW) and Macrocystis (6.1–17 mmol I kg−1 DW), both contained more iodine than Durvillaea (0.46–4 mmol I kg−1 DW; Fucales), but all three species contain much less iodine than previously studied Laminaria species. The studied algae also contain bromine and arsenic levels typical of brown algae reported from elsewhere, which are not affected by physiological conditions such as oxidative stress resulting in efflux of iodine.
Funding source: Directorate-General XII, Science, Research, and Development
Award Identifier / Grant number: ASSEMBLE TA (grant no. 227788)
Acknowledgments
We are grateful for the support of the European Community research infrastructure action under the FP7 ‘capacities’ specific programme ASSEMBLE (grant no. 227788), enabling FCK, TMT and MM to work at the Estación Costiera de Investigaciones Marinas (ECIM) of the Pontificia Universidad Catolica (PUC) de Chile. At ECIM/PUC, we would especially like to thank Randy Finke, Santiago Andrade, Ricardo Calderón, and Sylvain Faugeron for their support of our research activities during our visit. Finally, we would like to express our deep gratitude to our friend and coauthor Carl J. Carrano, who untimely passed away during the writing of this article (Küpper et al. 2025).
-
Research ethics: This work is fully compliant with the ethical standards of the University of Aberdeen, San Diego State University and the University of Graz.
-
Informed consent: Not applicable.
-
Author contributions: FCK and CJC designed this study, raised the funding and organized the expedition to Chile. FCK, TMT, MM, AR and JF performed experiments. FCK, TMT and MM performed scientific diving work. EPM and TMT analysed data. FCK and EPM wrote the manuscript. The authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Use of Large Language Models, AI and Machine Learning Tools: None declared.
-
Conflict of interest: There is no conflict of interest to declare.
-
Research funding: This work was supported by the European Community research infrastructure action under the FP7 ‘capacities’ specific programme ASSEMBLE (grant no. 227788).
-
Data availability: All data are available from the corresponding author (FCK) upon request.
References
Al-Adilah, H., Al-Bader, D., Elkotb, M., Kosma, I., Kumari, P., and Küpper, F.C. (2021). Trace element concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes. Bot. Mar. 64: 327–338, https://doi.org/10.1515/bot-2021-0027.Search in Google Scholar
Ar Gall, E., Küpper, F.C., and Kloareg, B. (2004). A survey of iodine contents in Laminaria digitata. Bot. Mar. 47: 30–37, https://doi.org/10.1515/bot.2004.004.Search in Google Scholar
Carpenter, L.J. and Liss, P.S. (2000). On temperate sources of bromoform and other reactive organic bromine gases. J. Geophys. Res.: Atmos. 105: 20539–20547, https://doi.org/10.1029/2000jd900242.Search in Google Scholar
Carpenter, L.J., Malin, G., Küpper, F.C., and Liss, P.S. (2000). Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal East Atlantic. Global Biogeochem. Cycles 14: 1191–1204, https://doi.org/10.1029/2000gb001257.Search in Google Scholar
Carrano, M.W., Yarimizu, K., Gonzales, J.L., Cruz-Lopez, R., Edwards, M.S., Tymon, T.M., Küpper, F.C., and Carrano, C.J. (2020). The influence of marine algae on iodine speciation in the coastal ocean. Algae 35: 167–176, https://doi.org/10.4490/algae.2020.35.5.25.Search in Google Scholar
Carrano, M.W., Carrano, C.J., Al-Adilah, H., Fontana, Y., Sayer, M.D.J., Katsaros, C., Raab, A., Feldmann, J., and Küpper, F.C. (2021). Laminaria kelps impact iodine speciation chemistry in coastal seawater. Estuarine, Coastal Shelf Sci. 262: 107531.10.1016/j.ecss.2021.107531Search in Google Scholar
Castilla, J.C., Campo, M.A., and Bustamante, R.H. (2007). Recovery of Durvillaea antarctica (Durvilleales) inside and outside Las Cruces marine reserve, Chile. Ecol. Appl. 17: 1511–1522, https://doi.org/10.1890/06-1285.1.Search in Google Scholar PubMed
Chance, R., Baker, A.R., Küpper, F.C., Hughes, C., Kloareg, B., and Malin, G. (2009). Release and transformations of inorganic iodine by marine macroalgae. Estuarine, Coastal Shelf Sci. 82: 406–414.10.1016/j.ecss.2009.02.004Search in Google Scholar
Delépine, R. and Asensi, A.O. (1976). Quelques données expérimentales sur l’écophysiologie de Durvillea antarctica (Cham.) Hariot (Phéophycées). Soc. Psychol. Fr. Bull. 21: 65–80.Search in Google Scholar
Ender, E., Subirana, M.A., Raab, A., Krupp, E.M., Schaumlöffel, D., and Feldmann, J. (2019). Why is NanoSIMS elemental imaging of arsenic in seaweed (Laminaria digitata) important for understanding of arsenic biochemistry in addition to speciation information? J. Anal. At. Spectrom. 34: 2295–2302, https://doi.org/10.1039/c9ja00187e.Search in Google Scholar
Francesconi, K.A. (2010). Arsenic species in seafood: origin and human health implications. Pure Appl. Chem. 82: 373–381, https://doi.org/10.1351/pac-con-09-07-01.Search in Google Scholar
Gonzales, J., Tymon, T., Küpper, F.C., Edwards, M.S., and Carrano, C.J. (2017). The potential role of kelp forests on iodine speciation in coastal seawater. PLoS One 12: e0180755, https://doi.org/10.1371/journal.pone.0180755.Search in Google Scholar PubMed PubMed Central
Graham, M.H., Vasquez, J.A., and Buschmann, A.H. (2007). Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. In: Gibson, R.N., Atkinson, R.J.A., and Gordon, J.D.M. (Eds.), Oceanography and marine biology, Vol. 45. Crc Press-Taylor & Francis Group, Boca Raton.Search in Google Scholar
Harley, C.D.G., Anderson, K.M., Demes, K.W., Jorve, J.P., Kordas, R.L., Coyle, T.A., and Graham, M.H. (2012). Effects of climate change on global seaweed communities. J. Phycol. 48: 1064–1078, https://doi.org/10.1111/j.1529-8817.2012.01224.x.Search in Google Scholar PubMed
Heal, K.R., Maloney, A.E., Ingalls, A.E., and Bundy, R.M. (2022). Diverse arsenic-containing lipids in the surface ocean. Limnol. Oceanogr. Lett. 7: 43–51, https://doi.org/10.1002/lol2.10216.Search in Google Scholar
Huovinen, P., Leal, P., and Gomez, I. (2010). Interacting effects of copper, nitrogen and ultraviolet radiation on the physiology of three south Pacific kelps. Mar. Freshwater Res. 61: 330–341, https://doi.org/10.1071/mf09054.Search in Google Scholar
Kirby, J., Maher, W., Ellwood, M., and Krikowa, F. (2004). Arsenic species determination in biological tissues by HPLC-ICP-MS and HPLC-HG-ICP-MS. Aust. J. Chem. 57: 957–966, https://doi.org/10.1071/ch04094.Search in Google Scholar
Küpper, F.C. and Carrano, C.J. (2019). Key aspects of the iodine metabolism in brown algae: a brief critical review. Metallomics 11: 756–764, https://doi.org/10.1039/c8mt00327k.Search in Google Scholar PubMed
Küpper, F.C. and Kroneck, P.M.H. (2015). Iodine bioinorganic chemistry: physiology, structures, and mechanisms. In: Kaiho, T. (Ed.), Iodine chemistry and applications. John Wiley & Sons Inc, Hoboken.10.1002/9781118909911.ch32Search in Google Scholar
Küpper, F.C., Schweigert, N., Ar Gall, E., Legendre, J.M., Vilter, H., and Kloareg, B. (1998). Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta 207: 163–171, https://doi.org/10.1007/s004250050469.Search in Google Scholar
Küpper, F.C., Kloareg, B., Guern, J., and Potin, P. (2001). Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 125: 278–291, https://doi.org/10.1104/pp.125.1.278.Search in Google Scholar PubMed PubMed Central
Küpper, F.C., Carpenter, L.J., Mcfiggans, G.B., Palmer, C.J., Waite, T.J., Boneberg, E.M., Woitsch, S., Weiller, M., Abela, R., Grolimund, D., et al.. (2008). Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc. Natl. Acad. Sci. U. S. A. 105: 6954–6958, https://doi.org/10.1073/pnas.0709959105.Search in Google Scholar PubMed PubMed Central
Küpper, F.C., Feiters, M.C., Olofsson, B., Kaiho, T., Yanagida, S., Zimmermann, M.B., Carpenter, L.J., Luther Iii, G.W., Lu, Z., Jonsson, M., et al.. (2011). Commemorating two centuries of iodine research: an interdisciplinary overview of current research. Angew. Chem., Int. Ed. 50: 11598–11620, https://doi.org/10.1002/anie.201100028.Search in Google Scholar PubMed
Küpper, F.C., Carpenter, L.J., Leblanc, C., Toyama, C., Uchida, Y., Verhaeghe, E., Maskrey, B., Robinson, J., Boneberg, E.-M., Malin, G., et al.. (2013). Speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps. J. Exp. Bot. 64: 2653–2664, https://doi.org/10.1093/jxb/ert110.Search in Google Scholar PubMed PubMed Central
Küpper, F.C., Leblanc, C., Meyer-Klaucke, W., Potin, P., and Feiters, M.C. (2014). Different speciation for bromine in brown and red algae, revealed by in vivo X-ray absorption spectroscopic studies. J. Phycol. 50: 652–664, https://doi.org/10.1111/jpy.12199.Search in Google Scholar PubMed
Küpper, F.C., Miller, E.P., Andrews, S.J., Hughes, C., Carpenter, L.J., Meyer-Klaucke, W., Toyama, C., Muramatsu, Y., Feiters, M.C., and Carrano, C.J. (2018). Emission of volatile halogenated compounds, speciation and localization of bromine and iodine in the brown algal genome model Ectocarpus siliculosus. J. Biol. Inorg. Chem. 23: 1119–1128, https://doi.org/10.1007/s00775-018-1539-7.Search in Google Scholar PubMed
Küpper, F.C., Carrano, E., Raymond, K.N., Miller, E., Cruz-López, R., Mijovilovich, A., Yarimizu, K., Cooksy, A., Harris, W., Amin, S.A., et al.. (2025). In memoriam- Carl J. Carrano. July 14, 1950 – January 26, 2022. BioMetals, in press.10.1007/s10534-024-00651-9Search in Google Scholar
Manley, S.L. (1984). Micronutrient uptake and translocation by Macrocystis pyrifera (Phaeophyta). J. Phycol. 20: 192–201, https://doi.org/10.1111/j.0022-3646.1984.00192.x.Search in Google Scholar
Manley, S.L. and Barbero, P.E. (2001). Physiological constraints on bromoform (CHBr3) production by Ulva lactuca (Chlorophyta). Limnol. Oceanogr. 46: 1392–1399, https://doi.org/10.4319/lo.2001.46.6.1392.Search in Google Scholar
Manley, S.L. and Dastoor, M.N. (1987). Methyl halide (CH3X) production from the giant kelp, Macrocystis, and estimates of global CH3X production by kelp. Limnol. Oceanogr. 32: 709–715, https://doi.org/10.4319/lo.1987.32.3.0709.Search in Google Scholar
Manley, S.L. and Dastoor, M.N. (1988). Methyl iodide (CH3I) production by kelp and associated microbes. Mar. Biol. 98: 477–482, https://doi.org/10.1007/bf00391538.Search in Google Scholar
Manley, S.L. and Lowe, C.G. (2012). Canopy-forming kelps as California’s coastal dosimeter: I-131 from damaged Japanese reactor measured in Macrocystis pyrifera. Environ. Sci. Technol. 46: 3731–3736, https://doi.org/10.1021/es203598r.Search in Google Scholar PubMed
Manley, S.L., Goodwin, K., and North, W.J. (1992). Laboratory production of bromoform, methylene bromide, and methyl-iodide by macroalgae and distribution in nearshore Southern California waters. Limnol. Oceanogr. 37: 1652–1659, https://doi.org/10.4319/lo.1992.37.8.1652.Search in Google Scholar
Murua, P., Goecke, F., Westermeier, R., Van West, P., Küpper, F.C., and Neuhauser, S. (2017). Maullinia braseltonii sp. nov. (Rhizaria, Phytomyxea, Phagomyxida): a cyst-forming parasite of the bull kelp Durvillaea spp. (Stramenopila, Phaeophyceae, Fucales). Protist 168: 468–480, https://doi.org/10.1016/j.protis.2017.07.001.Search in Google Scholar PubMed PubMed Central
O’dowd, C., Mcfiggans, G., Creasey, D.J., Pirjola, L., Hoell, C., Smith, M.H., Allan, B.J., Plane, J.M.C., Heard, D.E., Lee, J.D., et al.. (1999). On the photochemical production of new particles in the coastal boundary layer. Geophys. Res. Lett. 26: 1707–1710, https://doi.org/10.1029/1999gl900335.Search in Google Scholar
O’dowd, C.D., Jimenez, J.L., Bahreini, R., Flagan, R.C., Seinfeld, J.H., Hämeri, K., Pirjola, L., Kulmala, M., Jennings, S.G., and Hoffmann, T. (2002). Marine aerosol formation from biogenic iodine emissions. Nature 417: 632–636, https://doi.org/10.1038/nature00775.Search in Google Scholar PubMed
Palmer, C.J., Anders, T.L., Carpenter, L.J., Küpper, F.C., and Mcfiggans, G.B. (2005). Iodine and halocarbon response of Laminaria digitata to oxidative stress and links to atmospheric new particle production. Environ. Chem. 2: 282–290, https://doi.org/10.1071/en05078.Search in Google Scholar
Petursdottir, A.H., Fletcher, K., Gunnlaugsdottir, H., Krupp, E., Küpper, F.C., and Feldmann, J. (2016). Environmental effects on arsenosugars and arsenolipids in Ectocarpus (Phaeophyta). Environ. Chem. 13: 21–33, https://doi.org/10.1071/en14229.Search in Google Scholar
Ronan, J.M., Stengel, D.B., Raab, A., Feldmann, J., O’hea, L., Bralatei, E., and Mcgovern, E. (2017). High proportions of inorganic arsenic in Laminaria digitata but not in Ascophyllum nodosum samples from Ireland. Chemosphere 186: 17–23, https://doi.org/10.1016/j.chemosphere.2017.07.076.Search in Google Scholar PubMed
Saenko, G.N., Kravtsova, Y.Y., Ivanenko, V.V., and Sheludko, S.I. (1978). Concentration of iodine and bromine by plants in the seas of Japan and Okhotsk. Mar. Biol. 47: 243–250, https://doi.org/10.1007/bf00541002.Search in Google Scholar
Saiz-Lopez, A., Plane, J.M.C., Mcfiggans, G., Williams, P.I., Ball, S.M., Bitter, M., Jones, R.L., Hongwei, C., and Hoffmann, T. (2006). Modelling molecular iodine emissions in a coastal marine environment: the link to new particle formation. Atmos. Chem. Phys. 6: 883–895, https://doi.org/10.5194/acp-6-883-2006.Search in Google Scholar
Silberfeld, T., Leigh, J.W., Verbruggen, H., Cruaud, C., De Reviers, B., and Rousseau, F. (2010). A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”. Mol. Phylogenet. Evol. 56: 659–674, https://doi.org/10.1016/j.ympev.2010.04.020.Search in Google Scholar PubMed
Smith, K.E., Aubin, M., Burrows, M.T., Filbee-Dexter, K., Hobday, A.J., Holbrook, N.J., King, N.G., Moore, P.J., Sen Gupta, A., Thomsen, M., et al.. (2024). Global impacts of marine heatwaves on coastal foundation species. Nat. Commun. 15, https://doi.org/10.1038/s41467-024-49307-9.Search in Google Scholar PubMed PubMed Central
Tala, F., Edding, M., and Vasquez, J. (2004). Aspects of the reproductive phenology of Lessonia trabeculata (Laminariales : Phaeophyceae) from three populations in northern Chile. N. Z. J. Mar. Freshwater Res. 38: 255–266, https://doi.org/10.1080/00288330.2004.9517235.Search in Google Scholar
Teagle, H., Hawkins, S.J., Moore, P.J., and Smale, D.A. (2017). The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J. Exp. Mar. Biol. Ecol. 492: 81–98, https://doi.org/10.1016/j.jembe.2017.01.017.Search in Google Scholar
Teas, J., Pino, S., Critchley, A., and Braverman, L.E. (2004). Variability of iodine content in common commercially available edible seaweeds. Thyroid 14: 836–841, https://doi.org/10.1089/thy.2004.14.836.Search in Google Scholar PubMed
Truesdale, V.W. (2008). The biogeochemical effect of seaweeds upon close-to natural concentrations of dissolved iodate and iodide in seawater. Preliminary study with Laminaria digitata and Fucus serratus. Estuarine, Coastal Shelf Sci. 78: 155–165, https://doi.org/10.1016/j.ecss.2007.11.022.Search in Google Scholar
Tymon, T.M., Miller, E.P., Gonzales, J.L., Raab, A., Küpper, F.C., and Carrano, C.J. (2017). Some aspects of the iodine metabolism of the giant kelp Macrocystis pyrifera (Phaeophyceae). J. Inorg. Biochem. 177: 82–88, https://doi.org/10.1016/j.jinorgbio.2017.09.003.Search in Google Scholar PubMed
Villouta, E. and Santelices, B. (1986). Lessonia trabeculata sp. nov. (Laminariales, Phaeophyta), a new kelp from Chile. Phycologia 25: 81–86, https://doi.org/10.2216/i0031-8884-25-1-81.1.Search in Google Scholar
Wernberg, T., Bennett, S., Babcock, R.C., De Bettignies, T., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C.J., Hovey, R.K., et al.. (2016). Climate-driven regime shift of a temperate marine ecosystem. Science 353: 169–172, https://doi.org/10.1126/science.aad8745.Search in Google Scholar PubMed
Supplementary Material
This article contains supplementary material (https://doi.org/10.1515/bot-2025-0055).
© 2025 Walter de Gruyter GmbH, Berlin/Boston
