Ecology and biochemical composition of a newly reported non-indigenous red alga, Grateloupia gibbesii, in the Mediterranean Sea, with reference to edible red seaweeds

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Abstract

Data on the chemical composition of 40 edible red algal species was compared to Grateloupia gibbesii, a recently reported non-indigenous red alga in the Mediterranean Sea. There has been no information on the seasonality or the chemical composition of G. gibbesii from its areas of distribution. The species was reported in a single location in the Mediterranean Sea, a eutrophic embayment in Egypt. Grateloupia gibbesii existed in spring from late March to early June. The short life span of G. gibbesii affected its biochemical constituents. Crude lipids and total carbohydrate contents represented 12 % and 70% of its dry mass; resp. Five grams of dry G. gibbesii could provide 8.6% and 91% of the recommended dietary intake of lipids and carbohydrates. In contrast, protein and ash contents were low in comparison to other red seaweeds. The analysis of mineral content showed that Ca, Fe and Zn concentrations were high, while Cd and total As, might be at a toxic level. In Egypt, exploitation of seaweeds is still emerging; accordingly, more studies are needed to assess the application of seaweeds as a healthy and renewable alternative in the nutraceutical, cosmetics, and well-being industries.

Introduction

Like all plants, seaweeds produce primary metabolites, which are essential to their growth, survival, and proliferation (Salehi et al., 2019). These compounds are mainly lipids, proteins, and carbohydrates. In addition, seaweeds accumulate minerals that are essential to their life and contribute to their nutritional and pharmacological value. Marine algae are an excellent source of bioactive compounds, including high-quality proteins with essential amino acids, vitamins, dietary fibers, fatty acids, and phenolic compounds. Most of these compounds are suitable as natural antioxidants, which are essential to human health and the food industry since in most countries there are limitations in using synthetic supplements and antioxidant compounds due to their side effects (Pandey and Rizvi, 2009).

The compounds produced by seaweeds differ in terms of chemical structure and quantities depending on the taxonomic position of seaweeds and the geographical and environmental distributions of the same species. Therefore, seaweeds have improved pharmaceutical and food industry products with diverse novel compounds (Gamal, 2011). In addition, seaweeds are consumed directly as food all over the world. At least 221 species of seaweeds (32 Chlorophyta, 64 Phaeophyta, and 125 Rhodophyta) have been used in food industry and 101 species for phycocolloid production (Zemke-White and Ohno, 1999).

Determination of the biochemical composition of seaweeds is the first step in assessing their nutritional value (Darcy-Vrillon, 1993). In view of the recent increasing demand for seaweed products, both as food and as an ingredient, the aim of this research was mainly to determine the total phenolic content, antioxidants activity, ash, crude protein, total lipids, carbohydrates, minerals, and physicochemical properties of the foliose red alga, Grateloupia gibbesii Harvey, which was recently reported as an introduced seaweed in the Mediterranean Sea by Rodríguez-Prieto et al. (2021). The nutritional value of G. gibbesii has never been reported, therefore, the evaluation of its chemical content is an essential step to determine the feasibility of its cultivation for exploiting this species as a sea vegetable or ingredient. Moreover, the assessment of trace elements and heavy metals content was of special importance to determine its potential health risk.

Section snippets

Seaweed sampling

Grateloupia gibbesii specimens were collected from the Eastern Harbor, Alexandria, Egypt (31°12’ 18.90 N 29°53’ 7.35 E) in May 2019. The samples were transported to the laboratory in an icebox. Epiphytes and sediment particles were removed by washing thoroughly using tap water and distilled water. A portion of the fresh samples was dried in the shade for 5 days at a constant temperature of 25  °C. The dried seaweed was powdered using a mechanical blender and stored in a freezer (−20  °C) for later

Results and discussion

Water quality of G. gibbesii habitat in Alexandria.

Grateloupia gibbesii, originally described from South Carolina, and potentially distributed in the western Atlantic Ocean was reported for the first time in the Mediterranean Coast of Egypt (Rodríguez-Prieto et al., 2021). The distribution of G. gibbesii has been observed for three years (2018, 2019, and 2020) along the Mediterranean coast of Egypt from Port-Said to Matrouh, during these years it was observed only in Alexandria. It exists in

CRediT authorship contribution statement

Soha Shabaka: Conceptualization, Resources, Investigation, Writing - original draft. Madelyn Moawad: Resources, Methodology, Revising, Investigation.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References (139)

  • KhaledA. et al.

    Distribution of heavy metals in seaweeds collected along Marsa-Matrouh beaches, Egyptian Mediterranean Sea

    Egypt. J. Aquat. Res.

    (2014)
  • KumariP. et al.

    Comparative evaluation and selection of a method for lipid and fatty acid extraction from macroalgae

    Anal. Biotechnol.

    (2011)
  • LiY.X. et al.

    Phlorotannins as bioactive agents from brown algae

    Process. Biochem.

    (2011)
  • LowryO.H. et al.

    Protein measurement with the folin phenol reagent

    J. Biol. Chem.

    (1951)
  • MabeauS. et al.

    Seaweed in food products: Biochemical and nutritional aspects

    Trends Food Sci. Technol.

    (1993)
  • MakkarH.P. et al.

    Seaweeds for livestock diets: A review

    Feed Sci. Technol.

    (2016)
  • Marinho-SorianoE. et al.

    Seasonal variation in the chemical composition of two tropical seaweeds

    Bioresour. Technol.

    (2006)
  • MarshamS. et al.

    Comparison of nutritive chemistry of a range of temperate seaweeds

    Food Chem.

    (2007)
  • MedeirosR.J. et al.

    Determination of inorganic trace elements in edible marine fish from Rio de Janeiro State, Brazil

    Food Control

    (2012)
  • MiyashitaK. et al.

    Chemical and nutritional characteristics of brown seaweed lipids: A review

    J. Funct. Foods

    (2013)
  • MoubayedN.M.S. et al.

    Antimicrobial, antioxidant properties and chemical composition of seaweeds collected from Saudi Arabia (Red Sea and Arabian Gulf)

    Saudi J. Biol. Sci.

    (2017)
  • PaivaL. et al.

    Health-promoting ingredients from four selected Azorean macroalgae

    Food Res. Int.

    (2016)
  • PhaneufD. et al.

    Evaluation of the contamination of marine algae (seaweed) from the St. Lawrence River and likely to be consumed by humans

    Environ. Res.

    (1999)
  • PrietoP. et al.

    Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E

    Anal. Biochem.

    (1999)
  • PrimpasI. et al.

    Principal component analysis: development of a multivariate index for assessing eutrophication according to the European water framework directive

    Ecol. Indic.

    (2010)
  • RainbowP.S.

    Trace metal bioaccumulation: Models, metabolic availability and toxicity

    Environ. Int.

    (2007)
  • AdmassuH. et al.

    Bioactive peptides derived from seaweed protein and their health benefits: Antihypertensive, antioxidant, and antidiabetic properties

    J. Food Sci.

    (2018)
  • AOAC

    Official Methods of Analyses

    (1990)
  • APHA

    Standard Methods for the Examination of Water and Wastewater

    (1989)
  • AriveP.L.C. et al.

    In vitro antioxidant activity of selected seaweeds in the Philippines

    Int. J. Theor. Appl. Sci.

    (2017)
  • AroyehunA.Q. et al.

    Effects of seasonal variability on the physicochemical, biochemical, and nutritional composition of western peninsular Malaysia Gracilaria manilaensis

    Molecules

    (2019)
  • AthukoralaY. et al.

    Potential antioxidant activity of marine red alga Grateloupia filicina extracts

    J. Food Lipids

    (2003)
  • AwadN.E.

    Bioactive brominated diterpenes from the marine red alga Jania rubens (L.) Lmx

    Phytother. Res.

    (2004)
  • BarbarinoE. et al.

    An evaluation of methods for extraction and quantification of protein from marine macro- and microalgae

    J. Appl. Phycol.

    (2005)
  • BetoJ.A.

    The role of calcium in human aging

    Clin. Nutr. Res.

    (2015)
  • BlackW.A.

    Seasonal variation in chemical composition of some of the littoral seaweeds common to scotland. Part II. Fucus serratus, Fucus Vesiculosus, Fucus spiralis, and pelvetia canaliculata

    J. Soc. Chem. Ind.

    (1949)
  • CabritaM.T. et al.

    Halogenated compounds from marine algae

    Mar. Drugs

    (2010)
  • CardosoS.M. et al.

    Seaweeds as preventive agents for cardiovascular diseases: From nutrients to functional foods

    Mar. Drugs

    (2015)
  • CarretoJ.I. et al.

    Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects

    Mar. Drugs

    (2011)
  • CarrittD.E. et al.

    Comparison and evaluation of currently employed modifications of the Winkler method for determining dissolved oxygen in sea water. A NASCO report

    J. Mar. Res.

    (1966)
  • CatarinoM.D. et al.

    Phycochemical constituents and biological activities of Fucus spp

    Mar. Drugs

    (2018)
  • ChakrabortyK. et al.

    Antioxidant activities and phenolic contents of three red seaweeds (Division: Rhodophyta) harvested from the Gulf of Mannar of Peninsular India

    J. Food Sci. Technol.

    (2015)
  • ChandrasekharaR.A. et al.

    Improvement of yield and quality of agar from Gracilaria edulis (Gmelin.) silva

    Res. Utiln.

    (2003)
  • ChenQ. et al.

    Distribution of metals and metalloids in dried seaweeds and health risk to population in southeastern China

    Sci. Rep.

    (2018)
  • CherryP. et al.

    Risks and benefits of consuming edible seaweeds

    Nutr. Rev.

    (2019)
  • CianR.E. et al.

    Chemical composition, nutritional and antioxidant properties of the red edible seaweed porphyra columbina

    Int. J. Food Sci. Nutr.

    (2014)
  • CofradesS. et al.

    Nutritional and antioxidant properties of different brown and red spanish edible seaweeds

    Food Sci. Technol. Int.

    (2010)
  • CoteG.I. et al.

    Production and properties of native agars from Gracilaria tikvahiae and other red algae

    Bot. Mar.

    (1986)
  • CraigieJ.S.

    Cell walls

  • CraigieJ.S. et al.

    Interspecific and nutritionally determined variations in the composition of agar from Gracilaria sp

    Bot. Mar.

    (1984)
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