Abstract
Marine algae have made a strong contribution to global food security in the future. This study is the first report describing the concentration, pathways, and interactions of halogens in 15 species of marine algae collected from the Eastern Harbor in Alexandria, Egypt, relative to 22 key variables. The relationship between halogen content and chemical and biochemical parameters was studied through multivariate analysis. Among all the tested algae, the iodine content was the lowest (2.53–3.00 μg/g). The range of fluoride and chloride in macroalgae (1.12–1.70 and 0.10–0.46 mg/g) was smaller than that of microalgae (0.10–0.46 and 1.48–3.17 mg/g). The bromide content in macroalgae (0.36–5.45 mg/g) was higher than that in microalgae (0.40–0.76 mg/g). The halogen content in macroalgae was arranged in the order of Br > F > Cl > I. In addition, the biochemical parameters such as carbohydrates, proteins, lipids, and certain heavy metals (Fe, Zn, Cu, Mn, Pb, Ni, Co, Cd, and Cr) were determined. Calories, energy, total antioxidant activity (TAC), K/Na, and ion quotient amounts were estimated. The results showed that the green seaweed species had the highest TAC content. In most of the studied algal species, the calculated ion quotient referred to their likelihood of overcoming high blood pressure. The estimated daily intake (EDI) of algae showed no adverse effects on human health. Most of the research variables are below the acceptable WHO/FAO level. Generally, the calorie content of the selected algae is less than 2 kcal, which makes the algae considered an alternative source of healthy food to reduce obesity.
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References
Abdallah MAM (2008) Chemical composition, mineral content and heavy metals of some marine seaweed from Alexandria coast, Egypt: potential uses. Egypt J Aquat Res 34(2):84–94
Aleem AA (1993) The marine algae of Alexandria. Faculty of Science, University of Alexandria, Egypt, Egypt, p 125
Almela C, Algora S, Benito V, Clemente MJ, Devesa V, Súñer MA, Vélez D, Montoro R (2002) Heavy metal, total arsenic, and inorganic arsenic contents of algae food products. J Agric Food Chem 50:918–923
AOAC (2000) Official Methods of Analysis of the Association of Official Analytical Chemists, 17th edn. AOAC International, Gaithersburg MD
APHA (American Public Health Association) (1999) Standard methods for the examination of water and waste water, 20th edn. APHA (American Public Health Association), Washington DC
ATSDR (2003) (Public health service, Agency for Toxic Substances and Disease Registry), Division of toxicology/toxicology information branch 1600 Clifton Road NE, Mailstop E-29 Atlanta, Georgia 30,333, pp 356
Benton D (2015) Portion size: what we know and what we need to know. Crit Rev Food Sci Nutr 55(7):988–1004
Berbasova T, Nallur S, Sells T, Smith KD, Gordon PB, Tausta SL, Strobel SA, Sokolowski B (2017) Fluoride export (FEX) proteins from fungi, plants and animals are 'single barreled' channels containing one functional and one vestigial ion pore. PLOS ONE 12 (5):e0177096
Bhakar RN, Kumar R, Pabbi S (2013) Total lipids and fatty acid profile of different Spirulina strains as affected by salinity and incubation time. Int J Plant Res 26:148–154
Bhatnagar M, Bhatnagar A (2000) Algal and cyanobacterial responses to fluoride. Fluoride 33(2):55–65
Bilal M, Rasheed T, Sosa-Hernández JE, Raza A, Nabeel F, Iqbal HMN (2018) Biosorption: an interplay between marine algae and potentially toxic elements - A Review. Mar Drugs 16(2):65
Blaine J, Chonchol M, Levi M (2015) Renal control of calcium, phosphate, and magnesium homeostasis. Clin J Am Soc Nephrol 10(7):1257–1272
Bleakley S, Hayes M (2017) Review algal proteins: extraction, application, and challenges concerning production. Foods 6(5):1–34
Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2015) Marine natural products. Nat Prod Rep 32(2):116–211
Bouga M, Combet E (2015) Emergence of seaweed and seaweed-containing foods in the UK: focus on labeling, iodine content, toxicity and nutrition. Foods 4(2):240–253
Bowen HJM (1966) Trace Elements in Biochemisrrv. Academic Press, London, New York
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254
Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, London
Capelli B, Cysewski GR (2010) Potential health benefits of Spirulina microalgae. Nutrafoods 9(2):19–26
Chen Q, Pan X-D, Huang B-F, Han J-L (2018) Distribution of metals and metalloids in dried seaweeds and health risk to population in southeastern China. Sci Rep 8(1):3578
Cherry P, O’Hara C, Magee PJ, McSorley EM, Allsopp PJ (2019) Risks and benefits of consuming edible seaweed. Nutr Rev. 77(5):307–329
Cocchi M, Venturi S (2000) Iodide antioxidant function and omega-6 and omega-3 fatty acids: a new hypothesis of biochemical cooperation? Prog Nut 2:15–19
Combet E (2017) Iodine status, thyroid function, and vegetarianism.Vegetarian and plant-based diets in health and disease prevention. Academic Press, London, pp 769–790
Cui Y, Winton MI, Zhang Z-F, Rainey C, Marshall J, De Kernion JB, Eckhert CD (2004) Dietary boron intake and prostate cancer risk. Oncol Rep 11(4):887–892
Deniaud-Bouët E, Kervarec N, Michel G, Tonon T, Kloareg B, Hervé C (2014) Chemical and enzymatic fractionation of cell walls from Fucales: insights into the structure of the extracellular matrix of brown algae. Ann Bot 114(6):1203–1216
Desikachary TV (1959) Cyanophyta, Indian Council of Agriculture Research
Dubois M, Giles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
El-Said GF (2013) Bioaccumulation of key metals and other contaminants by seaweed from the Egyptian Mediterranean Sea coast in relation to human health risk. Hum Ecol Risk Assess 19:1285–1305
El-Said GF, El-Sikaily A (2013) Chemical composition of some seaweed from Mediterranean Sea coast, Egypt. Environ Monit Assess 185(7):6089–6099
Eyster KM (2007) The membrane and lipids as integral participants in signal transduction: lipid signal transduction for the non-lipid biochemist. Adv Physiol Educ 31(1):5–16
Fathy AA (2007) Evaluation of nutritional composition of some attached and drifted marine algae from Alexandria, Egypt. Egypt J Phycol 8(1):131–141
Fordyce FM (2003) Database of the iodine content of food and diets populated with data from published literature. Department for International Development (DfID) KAR Project R7411, Environmental Controls in Iodine Deficiency Disorders, Commissioned Report no. CR/03/84N. Keyworth, Nottingham, British Geological Survey, UK
Frankel EN (1998) Lipid oxidation. The Oily Press, Dundee
Franzaring J, Klumpp A, Fangmeier A (2007) Active biomonitoring of airborne fluoride near an HF producing factory using standardized grass cultures. Atmos Environ 41(23):4828–4840
FSANZs (Food standards Australia and New Zealand) (2008) Voluntary addition of fluoride to packaged water. International assessment report, Application A588. http://www.Foodstandards.gov.au/standardsdevelopment/.
Ganesan AR, Subramani K, Shanmugam M et al (2020) A comparison of nutritional value of underexploited edible seaweeds with recommended dietary allowances. J King Saud Univ Sci 32(1):1206–1211
Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nat 488(7411):329–335
Grasshoff K (1976) Methods of seawater analysis. Verlag Chemie, Weinkeim and New York, p 317
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of Marine Invertebrate Animals. Plenum Press, New York, pp 26–60
Guiry MD, Guiry GM (2018) Algae Base. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org
Gutiérrez-Salmeán G, Fabila-Castillo L, Chamorro-Cevallos G (2015) Nutritional and toxicological aspects of Spirulina (Arthrospira). Nutr Hosp 32(1):34–40
Health Consultation and Land Crab Evaluation, National Oceanographic Atmospheric Administration Data (2006) Isla deVieques Vieques. In: Rico P (ed) Department of Health and Human Services Agency for Toxic Substances and Disease Registry Division of Health Assessment and Consultation, pp 26
Hekman WE, Budd K, Palmer GR, MacArthur JD (1984) Responses of certain fresh water planktonic algae to fluoride. J Phycol 20:243–249
Helbert W (2017) Marine polysaccharide sulfatases. Front Mar Sci 4:1–10
Hemalatha A, Girija K, Parthiban C, Saranya C, Anantharaman P (2013) Antioxidant properties and total phenolic content of a marine diatom, Navicula clavata and green microalgae, Chlorella marina and Dunaliella marina. Adv Appl Sci Res 4(5):151–157
Ismail MM, El-Sheekh M (2017) Enhancement of biochemical and nutritional contents of some cultivated seaweed under laboratory conditions. J Diet Suppl 15(3):318–329
Ismail GA, Ismail MM (2017) Variation in oxidative stress indices of two green seaweed growing under different heavy metal stresses. Environ Monit Assess 189(2):68–80
Ismail MM, Gheda SF, Pereira L (2016) Variation in bioactive compounds in some seaweed from Abo Qir bay, Alexandria, Egypt. Rend Lincei Sci Fis 27(2):269–279
Ismail MM, El Zokm GM, El-Sayed AM (2017) Variation in biochemical constituents and master elements in common seaweed from Alexandria Coast, Egypt, with special reference to their antioxidant activity and potential food uses: prospective equations. Environ Monit Assess 189:648
Ismail MM, Ismail GA, El-Sheekh MM (2020) Potential assessment of some micro- and macroalgal species for bioethanol and biodiesel production. Energy Sources, Part A: Rrecovery, Utilization, and Environmental Effects. 1–17
Jaishankar M, Tseten T, Anbalagan N et al (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72
Jha B, Reddy CRK, Thakur MC, Rao MU (2009) Seaweed of India, the diversity and distribution of seaweed of the Gujarat Coast. Springer, Dordrecht, p 15
Juneja A, Ceballos RM, Murthy GS (2013) Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6(9):4607–4638
Kamunde C, Sappal R, Melegy TM (2019) Brown seaweed (Aqua Arom) supplementation increases food intake and improves growth, antioxidant status and resistance to temperature stress in Atlantic salmon, Salmosalar. PLoS ONE 14(7):219792
Kanaan H, Belous O (2016) Marine algae of the Lebanese coast. Nova science publisher, Inc., New York
Keisham M, Mukherjee S, Bhatla SC (2018) Mechanisms of sodium transport in plants - progresses and challenges. Int J Mol Sci 19:647
Kidgell JT, Magnusson M, de Nys R, Glasson CRK (2019) Ulvan: a systematic review of extraction, composition and function. Algal Res 39:101422
Kumar JI, Kumar RN, Amb MK et al (2010) Variation of biochemical composition of eighteen marine macroalgae collected from Okha coast, Gulf of Kutch, India. Electronic J Environm Agricult Food Chem 9:404–410
Kumar M, Vishal G, Kumari P, Reddy CRK, Jha B (2011) Assessment of nutrient composition and antioxidant potential of Caulerpaceae seaweeds. J Food Compost Anal 24:270–278
Kumar K, Giri A, Vivek P, Kalaiyarasan T, Kumar B (2017) Effects of fluoride on respiration and photosynthesis in plants: an overview. Ann Environ Sci Toxicol 2(1):43–47
Küpper FC, Carrano CJ (2019) Key aspects of the iodine metabolism in brown algae: a brief critical review. Metallomics 11:756–764
Küpper FC, Schweigert N, ArGall E et al (1998) Iodine uptake in laminariales involves extracellular, haloperoxidase mediated oxidation of iodide. Planta. 207(2):163–171
Küpper FC, Leblanc C, Meyer-Klaucke W et al (2014) Different speciation for bromine in brown and red algae, revealed by in vivo x-ray absorption spectroscopic studies. J. Phycol. 50:652–664
La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar Drugs 8:988–1010
Lauritano C, Andersen JH, Hansen E et al (2016) Bioactivity screening of microalgae for antioxidant, anti-Inflammatory, anticancer, anti-diabetes, and antibacterial activities. Front. Mar. Sci. 3(68):1–12
Leung AM, Braverman LE (2014) Consequences of excess iodine. Nat Rev. Endocrinol 10:136–142
Li M, Eastman CJ (2012) The changing epidemiology of iodine deficiency. Nat Rev. Endocrinol 8:434–440
Li Z-Y, Guo S-Y, Li L, Cai M-Y (2007) Effects of electromagnetic field on the batch cultivation of Spirulina platensis in an air-lift photobioreactor. Bioresour Technol 98(3):700–705
Li Y, Ghasemi Naghdi F, Garg S et al (2014) A comparative study: the impact of different lipid extraction methods on current microalgal lipid research. Microb. Cell Fact 13(14):1–9
Lin F-M, Wu H-L, Kou H-S, Lin S-J (2003) Highly sensitive analysis of iodide anion in seaweed as pentafluorophenoxyethyl derivative by capillary gas chromatography. J Agricult Food Chem 51(4):867–870
Lincoln RA, Strupinski K, Walker JM (1991) Bioactive compounds from algae. Life Chem Rep 8:97–183
Liteplo R, Howe P, Malcolm H (2002) Fluorides. Environmental Health criteria. WHO, Geneva, p 227
Manual of Methods of Analysis of Foods (2005) Fruit and vegetable products: Directorate General of Health Services. Ministry of Health and Family Welfare, Government of India, New Delhi, p 57
Maret W (2013) Zinc Biochemistry: from a single zinc enzyme to a key element of life. Adv Nutr 4(1):82–91
Marinho-Soriano E, Fonseca PC, Carneiro MAA, Moreira WSC (2006) Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour Technol. 97(18):2402–2406
Masoud MS, El-Sarraf WM, Harfoush AA, El-Said GF (2006) The effect of fluoride and other ions on algae and fish of coastal water of Mediterranean Sea. Egypt American J Environ Sci 2(2):49–59
Mišurcová L, Machǔ L, Orsavová J (2011) Seaweed minerals as nutraceuticals. Adv Food Nut Res 64:371–390
Miyashita K, Mikami N, Hosokawa M (2013) Chemical and nutritional characteristics of brown seaweed lipids: A review. J Funct Foods 5(4):1507–1517
Mohamed AA (1999) Natural pigments and iodine contents in certain marine macroalgae. Ph.D. Thesis, Department of Chemistry, Faculty of science, Helwan University, Egypt, pp 202
Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev. 27(2–3):239–261
Neumann CS, Fujimori DG, Walsh CT (2008) Halogenation strategies in natural product biosynthesis. Chem Biol 15:99–109
Nielsen FH, Eckhert CD (2020) Boron. Adv Nutr. 111(2):461–462. https://doi.org/10.1093/advances/nmz110
NRC (National Research Council) (1993) Nutrient requirements of fish. National Academy Press, Washington, DC, pp 62–63
Olasehinde TA, Olaniran AO, Okoh AI (2019) Macroalgae as a valuable source of naturally occurring bioactive compounds for the treatment of Alzheimer’s disease. Mar Drugs. 17:1–18
Øverland M, Mydland LT, Skrede A (2018) Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J Sci Food Agricult 99(1):13–24
Prescott GW (1962) Algae of the Western Great Lakes Area, 2nd edn. Wm. C. Brown Co, Dubuque, Iowa, p 977
Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal biochem 269(2):337–341
Rao PVS, Mantri VA (2006) Indian seaweed resources and sustainable utilization: scenario at the dawn of a new century. Curr Sci 91(2):164–174
Ratana-arporn P, Chirapart A (2006) Nutritional evaluation of tropical green seaweed Caulerpa lentillifera and Ulva reticulata. Kasetsart J Nat Sci 40:75–83
Regional Screening Levels (RSLs)-Generic Tables 2019, https://www.epa.gov/risk/regional-screening-levels-rsls-generic-tables
Rogina B, Dubravčić M (1953) Micro-determination of iodides by arresting the catalytic reduction of ceric ions. Anal 78(931):594–599
Saenger P (1972) A rapid spectrophotometric method for the determination of bromine in seawater and in the ash of marine algae. Helgoländer wissen schaftliche Meeresuntersuchungen. 23(1):32–37
Sajid IK, Satam SB (2003) Seaweed mariculture scope and potential in India. Aquacult Asia 8(4):26–29
Salehi B, Sharifi-Rad J, Seca A et al (2019) Current trends on seaweeds: looking at chemical composition, Phytopharmacology, and Cosmetic Applications. Mol. (Basel, Switzerland) 24(22):4182
Sathasivam R, Radhakrishnan R, Hashem A et al (2019) Microalgae metabolites: a rich source for food and medicine. Saudi J Biol Sci 26(4):709–722
SCF (Scientific Committee for Food) (1993) Nutrient and energy intakes for the European Community. Reports of the Scientific Committee for Food (Thirty-first series. European Commission, Luxembourg)
SCF (Scientific Committee on Food, European Commission) (2002) Opinion of the Scientific Committee on Food on the Tolerable Upper Intake Level of Iodine. European Commission, SCF/CS/NUT/UPPLEV/26 Final Report, Brussels
Schuhmacher M, Domingo JL (1996) Concentrations of selected elements in oysters (Crassostrea angulata); from the Spanish Coast. Bull Environ Cont Toxicol 56(1):106–113
Strickland JDH, Parsons TR (1965) A Manual of Seawater Analysis, 2nd edit. Bulletin 125, 203 pp. Fisheries Research Board of Canada, Ottawa, ON, Canada
Taboada C, Millan R, Miguez I (2009) Composition, nutritional aspects and effect on serum parameters of marine algae Ulva rigida. J Sci Food Agricult 90(3):445–449
Vaskonen T (2003) Dietary minerals and modification of cardiovascular risk factors. J Nut Biochem 14(9):492–506
Visser TJ (2018) Regulation of thyroid function, synthesis and function of thyroid hormones. Thy Dis:1–30
Wang C, Yatsuya H, Li YY et al (2016) Prospective study of seaweed consumption and thyroid cancer incidence in women: the Japan Collaborative Cohort Study. Eur J Cancer Prev 25(3):239–245
Welch RM (1981) The biological significance of Ni. J Plant Nutr 3(1-4):345–356
Wells ML, Potin P, Craigie JS et al (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29(2):949–982
Wever R, Van der Horst MA (2013) The role of vanadium haloperoxidases in the formation of volatile brominated compounds and their impact on the environment. Dalton Trans 42:1177
WHO/FAO (2013) World Health Organization (WHO) and Food and Agriculture Organization (FAO), Geneva, Switzerland, Tech. Rep, “Guidelines for the safe use of wastewater and food stuff”. Volume 2 No. 1
Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84(1):14–21
Yang L, Zhang L-M (2008) Chemical structural and chain conformational characterization of some bioactive polysaccharides isolated from natural sources. Carbohydr Polym 76:349–361
Zarrouk C (1966) Contribution a l’etude d’une cyanobacterie: influence de divers facteurs physiques et chimiques sur la croissance et la photosynthese de Spirulina maxima (Setchell et Gardner) Geitler. University of Paris, France
Zbikowski R, Szefer P, Latała A (2006) Distribution and relationships between selected chemical elements in green alga Enteromorpha sp. from the southern Baltic. Environ Poll 143:435–448
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Dr. Gehan M. El-Zokm has measured elements and halogen contents in the tested algae and analysis the data.
Dr. Mona M. Ismail has collected the tested seaweed and identified them, plus purification and cultivation of the microalgae. Also, she has measured all the biochemical composition of the collected algae and has participated in the writing.
Prof. Dr. Ghada M. Farouk has estimated the elements and halogen content in the collected algae and has participated in the writing.
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Highlights
- Chemotaxonomic study of 15 marine algal species was conducted.
- Levels of 26 parameters included four halogens were illustrated.
- Multiple regression analysis was used to give deep insights into pathways and interactions between the studied parameters.
- Calories, energy, TAC, K/Na, ion quotient, EDI, and halogen ratio were estimated.
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El Zokm, G.M., Ismail, M.M. & El-Said, G.F. Halogen content relative to the chemical and biochemical composition of fifteen marine macro and micro algae: nutritional value, energy supply, antioxidant potency, and health risk assessment. Environ Sci Pollut Res 28, 14893–14908 (2021). https://doi.org/10.1007/s11356-020-11596-0
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DOI: https://doi.org/10.1007/s11356-020-11596-0