Startseite Lebenswissenschaften Trace element concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Trace element concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes

  • Hanan Al-Adilah

    Hanan Al-Adilah (right) is a research associate at Kuwait Institute for Scientific Research. She has a BSc in plant biology from Kuwait University (2011). She obtained her Master’s degree from Kuwait University with distinction, in the field of marine phytoplankton diversity in 2015. She is currently in the 4th year of her PhD in algal diversity and biochemistry at the University of Aberdeen aiming at exploring the halogen metabolism of seaweeds of the Arabian Gulf.

    , Dhia Al-Bader

    Dhia Al-Bader is an associate professor in the Botany Program, Department of Biological Sciences, Kuwait University. Research in her lab includes environmental algal biodiversity, algal phylogeny and taxonomy, and stress tolerance of seagrasses and algae.

    , Mohammed Elkotb , Ioanna Kosma

    Ioanna Kosma holds a B.Sc. in marine sciences and a M.Sc. in “Integrated Coastal Management” from the University of the Aegean (UA), Department of Marine Sciences. Her research background focuses on marine biodiversity and ecology in combination with scientific diving, and she also has experience in marine immunology. She has extensive field work experience, and she has participated in scientific excursions in Cyprus, Kuwait, and Greece. From 2019 she has been working as a research associate at UA (Department of Marine Sciences) and particularly in the Marine Remote Sensing group, participating in various work packages and deliverables.

    , Puja Kumari

    Puja Kumari is a Marie Curie (MSCA-IF) postdoctoral research fellow in the School of Biological Sciences, University of Aberdeen. She obtained her PhD in biotechnology through a joint program of MK Bhavnagar University and CSIR-CSMCRI, India. She is the former recipient of ARO (Israel), BIDR-Blaustein (Israel) and JSPS (Japan) postdoctoral fellowships. Her research pursuit included algal stress physiology, lipidomics, metabolomics, chemotaxonomy and algal bioprospection leading to a patent for integrated process for obtaining value-added products from seaweeds without any in situ chemical reactions. Currently, she is working on elucidating the role of halogen metabolism in brown algal pathologies.

    ORCID logo
    und Frithjof Christian Küpper

    Frithjof Christian Küpper (left) has held the chair in marine biodiversity at the University of Aberdeen since 2011, after eight years at the Scottish Association for Marine Science (Oban) as a lecturer and reader, studying the biodiversity and biochemistry of marine plants/algae. He conducted graduate studies at Roscoff and Konstanz for a joint French–German PhD. His research found that iodide serves as an inorganic antioxidant in kelp, the first described from a living system, impacting atmospheric and marine chemistry. A certified scientific diver, Frithjof has worked in the Mediterranean, South Atlantic (Ascension, Falkland Islands), Antarctica, the Arctic and the Arabian Gulf.

    EMAIL logo
Veröffentlicht/Copyright: 20. Juli 2021

Abstract

Even though seaweeds have been considered a nutrient-rich dietary source of minerals in other parts of the world, there is little knowledge about trace element accumulation in seaweeds of the Arabian Gulf. The Arabian Gulf is of particular interest due to being an extreme environment, as it features some of the highest temperatures and salinities observed in any marine waters in the world. This study determined the minerals contents using inductively-coupled plasma-mass spectrometry (ICP-MS) in 10 of the most common seaweeds of this region (Iyengaria stellata, Padina boergesenii, Chondria sp., Feldmannia indica, Codium papillatum, Sargassum aquifolium, Ulva chaugulii, Ulva tepida and Ulva sp.) supported by morphological and molecular (DNA barcode)-based identification. The finding of U. chaugulii reported here is a new record for Kuwait. Most of the seaweeds were rich in essential minerals including Ca, Mg, Na, K, Fe and Zn and their contents were higher than those of other mineral-rich foods. Principal component analysis revealed species-specific distributions of minerals in seaweeds. U. tepida and I. stellata were found to be exceptionally rich in most of the macro- and trace elements along with low As and Se, and thus can be utilized for food and feed applications.


Corresponding author: Frithjof Christian Küpper, School of Biological Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, AberdeenAB24 3UU, Scotland, UK; and Department of Chemistry, Marine Biodiscovery Centre, University of Aberdeen, AberdeenAB24 3UE, Scotland, UK, E-mail:

Award Identifier / Grant number: NE/D521522/1

Award Identifier / Grant number: NE/J023094/1

Funding source: Scottish Government

Award Identifier / Grant number: HR09011

About the authors

Hanan Al-Adilah

Hanan Al-Adilah (right) is a research associate at Kuwait Institute for Scientific Research. She has a BSc in plant biology from Kuwait University (2011). She obtained her Master’s degree from Kuwait University with distinction, in the field of marine phytoplankton diversity in 2015. She is currently in the 4th year of her PhD in algal diversity and biochemistry at the University of Aberdeen aiming at exploring the halogen metabolism of seaweeds of the Arabian Gulf.

Dhia Al-Bader

Dhia Al-Bader is an associate professor in the Botany Program, Department of Biological Sciences, Kuwait University. Research in her lab includes environmental algal biodiversity, algal phylogeny and taxonomy, and stress tolerance of seagrasses and algae.

Ioanna Kosma

Ioanna Kosma holds a B.Sc. in marine sciences and a M.Sc. in “Integrated Coastal Management” from the University of the Aegean (UA), Department of Marine Sciences. Her research background focuses on marine biodiversity and ecology in combination with scientific diving, and she also has experience in marine immunology. She has extensive field work experience, and she has participated in scientific excursions in Cyprus, Kuwait, and Greece. From 2019 she has been working as a research associate at UA (Department of Marine Sciences) and particularly in the Marine Remote Sensing group, participating in various work packages and deliverables.

Puja Kumari

Puja Kumari is a Marie Curie (MSCA-IF) postdoctoral research fellow in the School of Biological Sciences, University of Aberdeen. She obtained her PhD in biotechnology through a joint program of MK Bhavnagar University and CSIR-CSMCRI, India. She is the former recipient of ARO (Israel), BIDR-Blaustein (Israel) and JSPS (Japan) postdoctoral fellowships. Her research pursuit included algal stress physiology, lipidomics, metabolomics, chemotaxonomy and algal bioprospection leading to a patent for integrated process for obtaining value-added products from seaweeds without any in situ chemical reactions. Currently, she is working on elucidating the role of halogen metabolism in brown algal pathologies.

Frithjof Christian Küpper

Frithjof Christian Küpper (left) has held the chair in marine biodiversity at the University of Aberdeen since 2011, after eight years at the Scottish Association for Marine Science (Oban) as a lecturer and reader, studying the biodiversity and biochemistry of marine plants/algae. He conducted graduate studies at Roscoff and Konstanz for a joint French–German PhD. His research found that iodide serves as an inorganic antioxidant in kelp, the first described from a living system, impacting atmospheric and marine chemistry. A certified scientific diver, Frithjof has worked in the Mediterranean, South Atlantic (Ascension, Falkland Islands), Antarctica, the Arctic and the Arabian Gulf.

Acknowledgments

The authors acknowledge Kuwait University Research Administration Sector Project Units (RSPU) facilities No. GS 01/02 for sequencing. Special thanks to Department of Marine Sciences and National Unit for Environmental Research and services (SRUL01/13) for using their facilities and labs.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: We are grateful to the Kuwait Institute for Scientific Research (KISR) for PhD funding for Hanan Al-Adilah. We would equally like to thank the UK Natural Environment Research Council for their support to FCK (program Oceans 2025 – WP 4.5 and grants NE/D521522/1 and NE/J023094/1). This work also received support from the Marine Alliance for Science and Technology for Scotland pooling initiative. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Abbaspour, N., Hurrell, R., and Kelishadi, R. (2014). Review on iron and its importance for human health. J. Res. Med. Sci. 19: 164–174.Suche in Google Scholar

Al-Adilah, H., Peters, A.F., Al-Bader, D., Raab, A., Akhdhar, A., Feldmann, J., and Küpper, F.C. (2020). Iodine and fluorine concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes. Bot. Mar. 63: 509–519, https://doi.org/10.1515/bot-2020-0049.Suche in Google Scholar

Al-Yamani, F., Polikarpov, I., Al-Ghunaim, A., and Mikhaylova, T. (2014). Field guide of marine macroalgae (Chlorophyta, Rhodophyta, Phaeophyceae) of Kuwait. Kuwait: Kuwait Institute for Scientific Research.Suche in Google Scholar

Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402, https://doi.org/10.1093/nar/25.17.3389.Suche in Google Scholar PubMed PubMed Central

Bartolo, A., Zammit, G., Peters, A.F., and Küpper, F.C. (2020). DNA barcoding of macroalgae in the Mediterranean Sea. Bot. Mar. 63: 253–272, https://doi.org/10.1515/bot-2019-0041.Suche in Google Scholar

Cabrita, A.R., Maia, M.R., Oliveira, H.M., Sousa-Pinto, I., Almeida, A.A., Pinto, E., and Fonseca, A.J. (2016). Tracing seaweeds as mineral sources for farm-animals. J. Appl. Phycol. 28: 3135–3150, https://doi.org/10.1007/s10811-016-0839-y.Suche in Google Scholar

Camaschella, C. (2015). Iron-deficiency anemia. N. Engl. J. Med. 372: 1832–1843.10.1056/NEJMra1401038Suche in Google Scholar PubMed

Cardoso, S.M., Carvalho, L.G., Silva, P.J., Rodrigues, M.S., Pereira, O.R., and Pereira, L. (2014). Bioproducts from seaweeds: a review with special focus on the Iberian peninsula. Curr. Org. Chem. 18: 896–917, https://doi.org/10.2174/138527281807140515154116.Suche in Google Scholar

Circuncisão, A.R., Catarino, M.D., Cardoso, S.M., and Silva, A. (2018). Minerals from macroalgae origin: health benefits and risks for consumers. Mar. Drugs 16: 400, https://doi.org/10.3390/md16110400.Suche in Google Scholar PubMed PubMed Central

Dawagreh, A.K., Hailat, M., Khasawneh, H., Khasawneh, E., Sundaramurthy, S., and Titinchi, S. (2019). Study of the presence of metal elements in sea water in the State of Kuwait. Ecol. Environ. Conserv. 25: S70–S74.Suche in Google Scholar

Dawczynski, C., Schäfer, U., Leiterer, M., and Jahreis, G. (2007). Nutritional and toxicological importance of macro, trace, and ultra-trace elements in algae food products. J. Agric. Food Chem. 55: 10470–10475, https://doi.org/10.1021/jf0721500.Suche in Google Scholar PubMed

Dawes, C.J. (1998). Marine botany, 2nd ed. New York, USA: John Wiley & Sons.Suche in Google Scholar

De La Rocha, S.R., Sánchez-Muniz, F., Gómez-Juaristi, M., and Marín, M.L. (2009). Trace elements determination in edible seaweeds by an optimized and validated ICP-MS method. J. Food Compos. Anal. 22: 330–336, https://doi.org/10.1016/j.jfca.2008.10.021.Suche in Google Scholar

Famà, P., Wysor, B., Kooistra, W., and Zuccarello, G.C. (2002). Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J. Phycol. 38: 1040–1050, https://doi.org/10.1046/j.1529-8817.2002.t01-1-01237.x.Suche in Google Scholar

Geiszinger, A., Goessler, W., Pedersen, S.N., and Francesconi, K.A. (2001). Arsenic biotransformation by the brown macroalga Fucus serratus. Environ. Toxicol. Chem. 20: 2255–2262, https://doi.org/10.1897/1551-5028(2001)020<2255:abbtbm>2.0.co;2.10.1897/1551-5028(2001)020<2255:ABBTBM>2.0.CO;2Suche in Google Scholar

Holdt, S.L. and Kraan, S. (2011). Bioactive compounds in seaweed: functional food applications and legislation. J. Appl. Phycol. 23: 543–597, https://doi.org/10.1007/s10811-010-9632-5.Suche in Google Scholar

Ichikawa, S., Kamoshida, M., Hanaoka, K., Hamano, M., Maitani, T., and Kaise, T. (2006). Decrease of arsenic in edible brown algae Hijikia fusiforme by the cooking process. Appl. Organomet. Chem. 20: 585–590.10.1002/aoc.1102Suche in Google Scholar

Ichikawa, S., Nozawa, S., Hanaoka, K., and Kaise, T. (2010). Ingestion and excretion of arsenic compounds present in edible brown algae, Hijikia fusiforme, by mice. Food Chem. Toxicol. 48: 465–469.10.1016/j.fct.2009.09.037Suche in Google Scholar

John, D.M. and Al-Thani, R.F. (2014). Benthic marine algae of the Arabian Gulf: a critical review and analysis of distribution and diversity patterns. Nova Hedwigia 98: 341–392, https://doi.org/10.1127/0029-5035/2014/0156.Suche in Google Scholar

Kazi, M.A., Kavale, M.G., and Singh, V.V. (2016). Morphological and molecular characterization of Ulva chaugulii sp. nov., U. lactuca and U. ohnoi (Ulvophyceae, Chlorophyta) from India. Phycologia 55: 45–54, https://doi.org/10.2216/15-11.1.Suche in Google Scholar

Kuda, T. and Ikemori, T. (2009). Minerals, polysaccharides and antioxidant properties of aqueous solutions obtained from macroalgal beach-casts in the Noto Peninsula, Ishikawa, Japan. Food Chem. 112: 575–581, https://doi.org/10.1016/j.foodchem.2008.06.008.Suche 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.Suche in Google Scholar

Küpper, F.C., Feiters, M.C., Olofsson, B., Kaiho, T., Yanagida, S., Zimmermann, M.B., Carpenter, L.J., Luther, G.W.III, 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.Suche in Google Scholar

Küpper, H., Setlik, I., Spiller, M., Küpper, F.C., and Prasil, O. (2002). Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J. Phycol. 38: 429–441, https://doi.org/10.1046/j.1529-8817.2002.t01-1-01148.x.Suche in Google Scholar

Macartain, P., Gill, C.I., Brooks, M., Campbell, R., and Rowland, I.R. (2007). Nutritional value of edible seaweeds. Nutr. Rev. 65: 535–543, https://doi.org/10.1301/nr.2007.dec.535-543.Suche in Google Scholar

Mann, J. and Truswell, S. (2017). Essentials of human nutrition. Oxford University Press, Oxford.Suche in Google Scholar

Marinho-Soriano, E., Fonseca, P., Carneiro, M., and Moreira, W. (2006). Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour. Technol. 97: 2402–2406, https://doi.org/10.1016/j.biortech.2005.10.014.Suche in Google Scholar

Moreda-Pineiro, A., Pena-Vázquez, E., and Bermejo-Barrera, P. (2011). Significance of the presence of trace and ultratrace elements in seaweeds. In: Kim, S. K. (Ed.). Handbook of marine macroalgae. John Wiley & Sons, Hoboken NJ, USA, pp. 116–170.10.1002/9781119977087.ch6Suche in Google Scholar

Munoz, I.L. and Diaz, N.F. (2020). Minerals in edible seaweed: health benefits and food safety issues. Crit. Rev. Food Sci. Nutr. 18: 1–16.Suche in Google Scholar

Nabti, E., Jha, B., and Hartmann, A. (2017). Impact of seaweeds on agricultural crop production as biofertilizer. Int. J. Environ. Sci. Technol. 14: 1119–1134.10.1007/s13762-016-1202-1Suche in Google Scholar

Perelló, G., Martí-Cid, R., Llobet, J.M., and Domingo, J.L. (2008). Effects of various cooking processes on the concentrations of arsenic, cadmium, mercury, and lead in foods. J. Agric. Food Chem. 56: 11262–11269.10.1021/jf802411qSuche in Google Scholar

Perez, V. and Chang, E.T. (2014). Sodium-to-potassium ratio and blood pressure, hypertension, and related factors. Adv. Nutr. 5: 712–741.10.3945/an.114.006783Suche 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: 21–33.10.1071/EN14229Suche in Google Scholar

Pirian, K., Piri, K., Sohrabipour, J., Jahromi, S.T., and Blomster, J. (2006). Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran. Bot. Mar. 59: 47–158.10.1515/bot-2016-0009Suche in Google Scholar

Price, A.R.G., Vincent, L.P.A., Venkatachalam, A.J., Bolton, J.J., and Basson, P.W. (2006). Concordance between different measures of biodiversity in Indian Ocean macroalgae. Mar. Ecol. Prog. Ser. 319: 85–91.10.3354/meps319085Suche in Google Scholar

Rupérez, P. (2002). Mineral content of edible marine seaweeds. Food Chem. 79: 23–26.10.1016/S0308-8146(02)00171-1Suche in Google Scholar

Sanchez-Rodriguez, I., Huerta-Dia, M.A., Choumiline, E., Holguin-Quinones, O., and Zertuche-Gonzalez, J.A. (2001). Elemental concentrations in different species of seaweeds from Loreto Bay, Baja California Sur, Mexico: implication for the geochemical control of metals in algal tissue. Environ. Pollut. 114: 145–160.10.1016/S0269-7491(00)00223-2Suche in Google Scholar

Sheppard, C., Al-Husiani, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, F., Dutrieux, E., Dulvy, N.K., Durvasula, S.R.V., et al.. (2010). The Gulf: a young sea in decline. Mar. Pollut. Bull. 60: 13–38.10.1016/j.marpolbul.2009.10.017Suche in Google Scholar

Silva, P.C., Basson, P.W., and Moe, R.L. (1996). Catalogue of the benthic marine algae of the Indian Ocean, Vol. 79. University of California Publications in Botany, Oakland CA, USA, pp. 1–1259.Suche in Google Scholar

Smith, J., Summers, G., and Wong, R. (2010). Nutrient and heavy metal content of edible seaweeds in New Zealand. N. Z. J. Crop Hortic. Sci. 38: 19–28.10.1080/01140671003619290Suche in Google Scholar

Soares, C., Švarc-Gajić, J., Oliva-Teles, M.T., Pinto, E., Nastić, N., Savić, S., Almeida, A., and Delerue-Matos, C. (2020). Mineral composition of subcritical water extracts of Saccorhiza polyschides, a brown seaweed used as fertilizer in the north of Portugal. J. Mar. Sci. Eng. 8: 244.10.3390/jmse8040244Suche in Google Scholar

Sudharsan, S., Seedevi, P., Ramasamy, P., Subhapradha, N., Vairamani, S., and Shanmugam, A. (2012). Heavy metal accumulation in seaweeds and sea grasses along southeast coast of India. J. Chem. Pharmaceut. Res. 4: 4240–4244.Suche in Google Scholar

Tokalıoğlu, Ş. (2012). Determination of trace elements in commonly consumed medicinal herbs by ICP-MS and multivariate analysis. Food Chem. 134: 2504–2508.10.1016/j.foodchem.2012.04.093Suche in Google Scholar

USDA. (2019). Food composition databases show nutrients list, Available at: https://fdc.nal.usda.gov/ndb/nutrients (Accessed 10 May 2021).Suche in Google Scholar

Van Netten, C., Cann, S.H., Morley, D., and Van Netten, J. (2000). Elemental and radioactive analysis of commercially available seaweed. Sci. Total Environ. 255: 169–175.10.1016/S0048-9697(00)00467-8Suche in Google Scholar

Vasuki, S., Kokilam, G., and Babitha, D. (2020). Mineral composition of some selected brown seaweeds from Mandapam region of Gulf of Mannar, Tamil Nadu. Indian. J. Geo-Mar. Sci. 49: 63–66.Suche in Google Scholar

Wells, M.L., Potin, P., Craigie, J.S., Raven, J.A., Merchant, S.S., Helliwell, K.E., Smith, A.G., Camire, M.E., and Brawley, S.H. (2017). Algae as nutritional and functional food sources: revisiting our understanding. J. Appl. Phycol. 29: 949–982.10.1007/s10811-016-0974-5Suche in Google Scholar

Westby, T. (2018). Investigation of the mineral profile of Fucus serratus Linneaus aqueous extracts and examination of the routes of uptake of minerals both in vivo and in vitro. Sligo: Institute of Technology.Suche in Google Scholar

Wilson, S. (2002). Nutritional value of detritus and algae in blenny territories on the Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 271: 155–169.10.1016/S0022-0981(02)00035-7Suche in Google Scholar

Yoganandham, S.T., Raguraman, V., Muniswamy, G., Sathyamoorthy, G., Renuka, R.R., Chidambaram, J., Rajendran, T., Chandrasekaran, K., and Ravindranath, R.R.S. (2019). Mineral and trace metal concentrations in seaweeds by microwave-assisted digestion method followed by quadrupole inductively coupled plasma mass spectrometry. Biol. Trace Elem. Res. 187: 579–585.10.1007/s12011-018-1397-8Suche in Google Scholar PubMed

Received: 2021-03-19
Accepted: 2021-06-09
Published Online: 2021-07-20
Published in Print: 2021-08-26

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 15.1.2026 von https://www.degruyterbrill.com/document/doi/10.1515/bot-2021-0027/html
Button zum nach oben scrollen