Minerals and trace elements content and concentration in marine algae
vary depending on species morphology and physiology; as well as growing
environmental conditions. Despite this variability, accumulation of magnesium,
and especially iron, seems to be common in Chlorophyta; while Rhodophyta and
Heterokontophyta show higher affinity to manganese. The red agarophyte Alsidium
triquetrum was used to analyze the
relationship between metal concentration, environmental conditions and growth
rate. Specimens grown in situ showed a large variability of Fe,
Mn, Mg, and Al, in thallus tissue concentrations. Further, a compelling relationship between the growth rate and
the thallus concentration of Mg and Mn, Zn, and Al was detecte. Manganese, unlike the other trace elements
analyzed showed a positive linear relationship between growth rate and tissue
content during the period of greatest vegetative growth.
References
[1]
Davis, T.A., Volesky, B. and Mucci, A. (2003) A Review of the Biochemistry of Heavy Metal Biosorption by Brown Algae. Water Research, 37, 4311-4333.
https://doi.org/10.1016/S0043-1354(03)00293-8
[2]
Cabrita, A. R.J., Maia, M.R.G., Oliveira, H.M., Sousa-Pinto, I., Almeida, A.A., Pinto, E. and Fonseca, A.J.M. (2016) Tracing Seaweeds as Mineral Sources for Farm-Animals. Journal of Applied Phycology, 28, 3135-3150.
https://doi.org/10.1007/s10811-016-0839-y
[3]
Ruperez, P. (2002) Mineral Content of Edible Marine Seaweeds. Food Chemistry, 79, 23-26. https://doi.org/10.1016/S0308-8146(02)00171-1
[4]
Dhaneesh, K.V., Gopi, M., Noushad, K.M., Ganeshamurthy, R., Kumar, T.T.A. and Balasubramanian, T. (2012) Determination of Metal Levels in Thirteen Fish Species from Lakshadweep Sea. Bulletin of Environmental Contamination and Toxicology, 88, 69-73. https://doi.org/10.1007/s00128-011-0459-9
[5]
Circuncisão, A.R., Catarino, M.D., Cardoso, S.M. and Silva, A.M.S. (2018) Minerals from Macroalgae Origin: Health Benefits and Risks for Consumers. Marine Drugs, 16, Article No. 400. https://doi.org/10.3390/md16110400
[6]
Gressler, V., Yokoya, N.S., Fujii, M.T., Colepicolo, P., Filho, J.M., Torres, R.P. and Pinto, E. (2010) Lipid, Fatty Acid, Protein, Amino Acid and Ash Contents in Four Brazilian Red Algae Species. Food Chemistry, 120, 585-590.
https://doi.org/10.1016/j.foodchem.2009.10.028
[7]
Marinho, G.S., Holdt, S.L. and Angelidaki, I. (2015) Seasonal Variations in the Amino Acid Profile and Protein Nutritional Value of Saccharina latissima Cultivated in a Commercial IMTA System. Journal of Applied Phycology, 27, 1991-2000.
https://doi.org/10.1007/s10811-015-0546-0
[8]
Tala, F. and Chow, F. (2014) Ecophysiological Characteristics of Porphyra spp. (Bangiophyceae, Rhodophyta): Seasonal and Latitudinal Variations in Northern-Central Chile. Journal of Applied Phycology, 26, 2159-2171.
https://doi.org/10.1007/s10811-014-0249-y
[9]
Zhou, A.Y., Robertson, J., Hamid, N., Ma, Q. and Lu, J. (2015) Changes in Total Nitrogen and Amino Acid Composition of New Zealand Undaria pinnatifida with Growth, Location and Plant Parts. Food Chemistry, 186, 319-325.
https://doi.org/10.1016/j.foodchem.2014.06.016
[10]
Edding, M., Fonck, E., Acuña, R. and Tala, F. (2008) Cultivation of Chondrus canaliculatus (C. Agardh) Greville (Gigartinales, Rhodophyta) in Controlled Environments. Aquaculture, 16, 283-295. https://doi.org/10.1007/s10499-007-9142-x
[11]
Abreu, M.H., Pereira, R., Yarish, C., Buschmann, A.H. and Sousa-Pinto, I. (2011) IMTA with Gracilaria vermiculophylla: Productivity and Nutrient Removal Performance of the Seaweed in a Land-Based Pilot Scale System. Aquaculture, 312, 77-87. https://doi.org/10.1016/j.aquaculture.2010.12.036
[12]
Redmond, S., Green, L., Yarish, C., Kim, J. and Neefus, C. (2014) New England Seaweed Culture Handbook—Nursery Systems. Connecticut Sea Grant CTSG-14-01, 92 p.
[13]
Jayasinghe, G.D.T.M., Kamal Jinadasa, B.K.K.K. and Manoj Chinthaka, S.D. (2018) Nutritional Composition and Heavy Metal Content of Five Tropical Seaweeds. Open Science Journal of Analytical Chemistry, 3, 17-22.
[14]
Rodríguez-Martínez, R.E., Roy, P.D., Torrescano-Valle, N., Cabanillas-Terán, N., Carrillo-Domínguez, S., Collado-Vides, L., García-Sánchez M. and van Tussenbroek, B.I. (2020) Element Concentrations in Pelagic Sargassum along the Mexican Caribbean Coast in 2018-2019. PeerJ, 8, e8667. https://doi.org/10.7717/peerj.8667
[15]
Mallea, A.J.A., Cabrera, R. and Díaz-Larrea, J. (2020) Biotecnología de agarófitas del género Alsidium C. Agardh: Requerimientos para el cultivo. Editorial Académica Española, London, 137 p.
[16]
Cabrera, R., Areces, A., Díaz-Larrea, J., Núñez-García, L.G. and Cruz-Aviña, J. (2021) Influence of the Macronutrients N, P and K on the Agarophyte Alsidium triquetrum (S. G. Gmelin) Trevisan, during Experimental Culture. American Journal of Plant Sciences, 12, 573-585. https://doi.org/10.4236/ajps.2021.124038
[17]
Areces, A.J. and Araujo, M. (1996) Influencia de la salinidad y la temperatura sobre el crecimiento de Bryothamnion triquetrum (Gmelin) Howe (Rhodophyta: Rhodomelaceae). Revista Biología Tropical, 44, 449-454.
[18]
Areces, A.J. and Soberats, L.R. (1992) Optimización del cultivo in situ de Bryothamnion triquetrum (Gmelin) Howe mediante evaluación de diversos sistemas de sujeción. Ciencias Biológicas, 18, 65-76. https://doi.org/10.7773/cm.v18i2.892
[19]
Areces, A.J., Cabrera, R. and Díaz-Larrea, J. (2022) Guía ilustrada para el cultivo in situ de Alsidium triquetrum. Brazilian Journals Editora, Sao José dos Pinhais, 24 p.
https://doi.org/10.35587/brj.ed.0001359
[20]
Jackson, M.I. (1970) Determinaciones del fósforo en los suelos. In: Análisis Químico de los Suelos, Revolucionaria, La Habana, 213-216.
[21]
Kjeldahl, J. (1883) Neue Methode zur Bestimmung des Stickstoffs in organischen Körpern. Zeitschrift für Analytische Chemie, 22, 366-382.
https://doi.org/10.1007/BF01338151
[22]
Chapman, H.D and Pratt, P.F. (1962) Methods of Analysis for Soils, Plants and Waters. 93, 68. https://doi.org/10.1097/00010694-196201000-00015
[23]
Yong, Y.S., Yong, W.T.L. and Anton, A. (2013) Analysis of Formulae for Determination of Seaweed Growth Rate. Journal of Applied Phycology, 25, 1831-1834.
https://doi.org/10.1007/s10811-013-0022-7
[24]
Sokal, R.R. and Rohlf, F.J. (1981) Biometry. 2nd Edition, W.H. Freeman, New York.
[25]
Siegel, S. (1972) Diseño experimental no-paramétrico aplicado a las ciencias de la conducta. Revolucionaria, La Habana, 346 p.
STATSOFT, Inc. (2004) STATISTICA (Data Analysis Software System), Version 7.
http://www.statsoft.com
[28]
Morel, F.M.M., Hudson, R.J.M. and Price, N. M. (1991) Limitation of Productivity by Trace Metals in the Sea. Limnology and Oceanography, 36, 1742-1755.
https://doi.org/10.4319/lo.1991.36.8.1742
[29]
Bilal, M., Rasheed, T., Sosa-Hernández, J.E., Raza, A., Nabeel, F. and Iqbal, H.M.N. (2018) Biosorption: An Interplay between Marine Algae and Potentially Toxic Elements—A Review. Marine Drugs, 16, Article No. 65.
https://doi.org/10.3390/md16020065
[30]
Bruland, K.W., Donat, J.R. and Hutchins, D.A. (1991) Interactive Influences of Bioactive Trace Metals on Biological Production in Oceanic Waters. Limnology and Oceanography, 36, 1555-1577. https://doi.org/10.4319/lo.1991.36.8.1555
[31]
Black, W.A.P. and Mitchell, R.L. (1952) Trace Elements in the Common Brown Algae and in Sea Water. Journal of the Marine Biological Association of the United Kingdom, 30, 575-584. https://doi.org/10.1017/S0025315400012984
[32]
Costa, G.B., Simioni, C., Ramlov, F., Maraschin, M., Chow, F., Bouzon, Z.L. and Schmidt, é.C. (2017) Effects of Manganese on the Physiology and Ultrastructure of Sargassum cymosum. Environmental and Experimental Botany, 133, 24-34.
https://doi.org/10.1016/j.envexpbot.2016.09.007
[33]
Yeats, P.A. and Strain, P.M. (1990) The Oxidation of Manganese in Seawater: Rate Constants Based on Field Data. Estuarine Coastal and Shelf Science, 31, 11-24.
https://doi.org/10.1016/0272-7714(90)90025-M
[34]
Kowalski, N., Dellwig, O., Beck, M., Grunwald, M., Badewien, T., Brumsack, H.-J., van Beusekom, J.E.E. and Böttcher, M.E. (2012) A Comparative Study of Manganese Dynamics in the Water Column and Sediments of Intertidal Systems of the North Sea. Estuarine Coastal and Shelf Science, 100, 3-17.
https://doi.org/10.1016/j.ecss.2011.03.011
[35]
Rai, L.C., Gaurx, J.P. and Kumar, H.D. (1981) Phycology and Heavy-Metal Pollution. Biological Review, 5, 99-151.
https://doi.org/10.1111/j.1469-185X.1981.tb00345.x
[36]
Millaleo, R., Reyes-Díaz, M., Ivanov, A.G., Mora, M.L. and Alberdi, M. (2010) Manganese as Essential and Toxic Element for Plants: Transport, Accumulation and Resistance Mechanisms. Journal of Soil Science and Plant Nutrition, 10, 476-494.
https://doi.org/10.4067/S0718-95162010000200008
[37]
Bachmann, R.W. and Odum, E.P. (1960) Uptake of Zinc 65 and Primary Productivity in Marine Benthic Algae. Limnology and Oceanography, 5, 349-355.
https://doi.org/10.4319/lo.1960.5.4.0349
[38]
Rice, D.L. and Lapoint, B.E. (1981) Experimental Outdoor Studies with Ulva fasciata Delille. II. Trace Metal Chemistry. Journal of Experimental Marine Biology and Ecology, 54, 1-11. https://doi.org/10.1016/0022-0981(81)90098-8
[39]
Cabrera, R., Díaz-Larrea, J., Cano, M. and Areces, A.J. (2019) Abundance and Components of the Ulva fasciata Delile 1813 Northern Coast of Havana City, Cuba. Merit Research Journal of Microbiology and Biological Sciences, 7, 56-72.
[40]
Thompson, M.W. (2022) Regulation of Zinc-Dependent Enzymes by Metal Carrier proteins. BioMetals, 35, 187-213. https://doi.org/10.1007/s10534-022-00373-w
[41]
Sawidis, T. and Voulgaropoulus, A.N. (1986) Seasonal Bioaccumulation of Iron, Cobalt and Copper in Marine Algae from Thermaikos Gulf of the Northern Aegean Sea, Greece. Marine Environmental Research, 19, 39-47.
https://doi.org/10.1016/0141-1136(86)90038-3
[42]
Rönnberg, O., Adjers, K., Ruokolahti, C. and Bondestan, M. (1990) Fucus vesiculosus as an Indicator of Heavy Metal Availability in a Fish Farm Recipient in the Northern Baltic Sea. Marine Pollution Bulletin, 21, 388-392.
https://doi.org/10.1016/0025-326X(90)90648-R
[43]
Aerts, R. and Chapin III, F.S. (2000) The Mineral Nutrition of Wild Plants Revisited: A Re-Evaluation of Processes and Patterns. Advances in Ecological Research, 30, 1-67. https://doi.org/10.1016/S0065-2504(08)60016-1
[44]
Reef, R., Pandolfi, J.M. and Lovelock, C. E. (2012) The Effect of Nutrient Enrichment on the Growth, Nucleic Acid Concentrations, and Elemental Stoichiometry of Coral Reef Macroalgae. Ecology and Evolution, 2, 1985-1995.
https://doi.org/10.1002/ece3.330
[45]
Ganesan, M., Kannan, R., Rajendran, K., Govindasamy, C., Sampathkumar, P. and Kannan, L. (1991) Trace Metals Distribution in Seaweeds of the Gulf of Mannar, Bay of Bengal. Marine Pollution Bulletin, 22, 205-207.
https://doi.org/10.1016/0025-326X(91)90472-5
[46]
Kureishy, T.W. (1991) Heavy Metals in Algae around the Coast of Qatar. Marine Pollution Bulletin, 22, 414-416. https://doi.org/10.1016/0025-326X(91)90347-U
[47]
Ramírez, M., Areces, A.J. and González, H. (1988) Concentración de metales pesados en macroalgas del litoral rocoso. área no contaminada. Ciencias Biológicas, 19/20, 88-95.
[48]
Alberts, J.J., Price, M.T. and Kania, M. (1990) Metal Concentrations in Tissues of Spartina alterniflora (Loisel.) and Sediments of Georgia Salt Marshes. Estuarine, Coastal and Shelf Science, 30, 47-58. https://doi.org/10.1016/0272-7714(90)90076-4
[49]
D’Souza, T.J. and Mistry, K.B. (1979) Uptake and Distribution of Gamma-Emitting Activation Products 59Fe, 58Co, 54Mn and 65Zn in Plants. Environmental and Experimental Botany, 19, 193-200. https://doi.org/10.1016/0098-8472(79)90048-0
[50]
D’Armas, H., Jaramillo, C., D’Armas, M., Echavarría, A. and Valverde, P. (2019) Proximate Composition of Several Green, Brown and Red Seaweeds from the Coast of Ecuador. Revista de Biología Tropical, 67, 61-68.
https://doi.org/10.15517/rbt.v67i1.33380
[51]
Cabrera, R., Areces, A.J., Díaz-Larrea, J., Sahu, S.K., Cruz-Aviña, J.R. and Nuñez García, L.G. (2022). Population Dynamics of Colonizing Fauna and Its Effect on Growth Rates of the Farmed Red Alga Alsidium triquetrum (S.G. Gmelin) Trevisan. Natural Science, 14, 42-55. https://doi.org/10.4236/ns.2022.142005
[52]
Milner, M.J., Seamon, J., Craft, E. and Kochian, L.V. (2013) Transport Properties of Members of the ZIP Family in Plants and Their Role in Zn and Mn Homeostasis. Journal of Experimental Botany, 64, 369-381. https://doi.org/10.1093/jxb/ers315
[53]
Rebhun, S. and Ben-Amotz, A. (1988) Antagonistic Effect of Manganese to Cadmium Toxicity in the Alga Dunaliella salina. Marine Ecology-Progress Series, 42, 97-104. https://doi.org/10.3354/meps042097
[54]
Souza, P.O., Ferreira, L.R., Pires, N.R.X., Filho, P.J.S., Duarte, F.A., Pereira, C.M.P. and Mesko, M.F. (2012) Algae of Economic Importance That Accumulate Cadmium and Lead: A Review. Brazilian Journal of Pharmacognosy, 22, 825-837.
https://doi.org/10.1590/S0102-695X2012005000076
[55]
Harrison, G.I. and Morel, F.M.M. (1986) Response of the Marine Diatom Thalassiosiran weissfloogii to Iron Stress. Limnology and Oceanography, 5, 349-355.
https://doi.org/10.4319/lo.1986.31.5.0989
[56]
Viljoen, J.J., Weir, I., Fietz, S., Cloete, R., Loock, J., Philibert, R. and Roychoudhury, A.N. (2019). Links between the Phytoplankton Community Composition and Trace Metal Distribution in Summer Surface Waters of the Atlantic Southern Ocean. Frontier Marine Science, 6, 295. https://doi.org/10.3389/fmars.2019.00295
[57]
Kazumi, J., Zorkin, N. and Lewis, A.G. (1987) The Effect of Manganese-Copper Interactions on Growth of a Diatom in Water From a Manganese-Rich British Columbia Fjord. Estuarine, Coastal and Shelf Science, 25, 337-346.
https://doi.org/10.1016/0272-7714(87)90076-X
[58]
Alejandro, S., Höller, S., Meier, B. and Peiter, E. (2020) Manganese in Plants: From Acquisition to Subcellular Allocation. Frontier in Plant Science, 11, Article 300.
https://doi.org/10.3389/fpls.2020.00300
[59]
Broadley, M., Brown, P., Cakmak, I., Rengel, Z. and Zhao, F. (2012) Function of Nutrients: Micronutrients. In: Marschner, P., Ed., Marschner’s Mineral Nutrition of Higher Plants, 3rd Edition, San Diego, USA, 191-249.
https://doi.org/10.1016/B978-0-12-384905-2.00007-8
[60]
Deboer, J.A. (1981) The Marine Plant Resources and Their Aquaculture Potential in Bahamas. A Report to the Fisheries Training and Development Project (BHA/78/001), 49 p.
[61]
Rice, D.L. (1984) A Simple Mass Transport Model for Metal Uptake by Marine Macroalgae Growing at Different Rates. Journal of Experimental Marine Biology and Ecology, 82, 175-182. https://doi.org/10.1016/0022-0981(84)90102-3
[62]
Zingde, M.D., Singbal, S.Y.S., Moroses, C.F. and Reddy, C.V.G. (1976) Arsenic, Copper, Zinc and Manganese in Marine Flora and Fauna of Coastal Estuarine Waters Aroud Goa. Indian Journal of Geo-Marine Sciences, 5, 212-217.
[63]
Catsiki, V. A., Papathanassiou, E. and Bei, F. (1991) Heavy Metal Levels in Characteristic Benthic Flora and Fauna in the Central Aegean Sea. Marine Pollution Bulletin, 22, 566-569. https://doi.org/10.1016/0025-326X(91)90898-3
[64]
Stengel, D.B., McGrath, H. and Morrison, L.J. (2005) Tissue Cu, Fe and Mn Concentrations in Different-Aged and Different Functional Thallus Regions of Three Brown Algae from Western Ireland. Estuarine, Coastal and Shelf Science, 65, 687-696. https://doi.org/10.1016/j.ecss.2005.07.003
