Hydrothermal extraction and thorough characterization of carrageenans and proteins from Gigartina pistillata

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Food Hydrocolloids 157 (2024) 110390

Available online 6 July 2024

nc-nd/4.0/).

Hydrothermal extraction and thorough characterization of carrageenans

and proteins from Gigartina pistillata

Milena ´

Alvarez-Vi˜

nas

, Fernanda Zamboni

, Guido Domingo

, Candida Vannini

, María

Dolores Torres

, Maurice N. Collins

, Herminia Domínguez

CINBIO, Department of Chemical Engineering, University of Vigo (Campus Ourense), Edicio Polit´

ecnico, As Lagoas, 32004, Ourense, Spain

Stokes Laboratories, School of Engineering, Bernal Institute, University of Limerick, Limerick, V94 T9PX, Ireland

Health Research Institute and AMBER University of Limerick, Limerick, V94 T9PX, Ireland

Department of Biotechnology and Life Sciences, University of Insubria, Via J. Hdunant 3, 21100, Varese, Italy

ARTICLE INFO

Keywords:

Hydrothermal treatment

Carrageenan

Hydrogels

Cytotoxicity

Peptides

Proteins

ABSTRACT

Carrageenan, an interesting biopolymer from red seaweed, possesses a myriad of applications in food, nutra-

ceutical, or pharmaceutical industries. Although its conventional extraction used to be performed with alkaline

solvents, water extraction under subcritical conditions is an alternative eco-friendly technique that has gained

popularity in recent years. This work evaluates the recovery and characterization of carrageenan and proteins

from Gigartina pistillata. The highest number of proteins was identied at the lowest processing tempeartures.

Extracted carrageenan exhibits molecular weights greater than 500 kDa and good rheological behaviour, with

interest for food applications and for the formulation of hydrogels when mixed with KCl. The carrageenans and

carrageenan hydrogels presented interesting properties such as good thermal stability until 170 ◦C (TGA-DTG)

and show characteristic bands of kappa/iota carrageenans in FTIR studies. Greater cell viability than 70% were

achieved on NIH/3T3 broblast at carrageenan concentrations of 0.05 and 0.025%, whereas carrageenan

extracted at 160 ◦C (concentration of 0.025%) displays a lower inammatory action than other samples. In this

sense, in this work the eco-friendlier extracted carrageenan was thoroughly characterized and its potentiality to

be used in the biomedical eld was evaluated.

1. Introduction

The awareness of the need for natural molecules with biological

potential of sustainable origin has increased rapidly due to the growing

concerns around climate change, population growth and unsustainable

practices in general. Among different sources, seaweeds are considered

an interesting option due to: being ubiquitous, presenting a high

photosynthetic efcacy, not competing for arable land, little water

consumption, great potential for obtaining high-added value products,

among others … (Rodríguez-Jasso et al., 2013; Ruiz et al., 2013).

Additionally, marine algae present diverse applications, including

environmental indicators of water quality, vegetable biostimulants, food

or even as source of proteins, ber, minerals, polysaccharides, and other

compounds of interest for the food, cosmetic or pharmaceutical in-

dustries. All this converts seaweed in a multifaceted resource (Mateo-

s-Aparicio et al., 2018).

Red seaweeds are also known as Rhodophyta, which is considered

the oldest phylum and has the most diversity of species. They comprise

great amounts of pigments (chlorophyll a and d, carotenoids, phycoer-

ythrin, phyllocyanin and allophycocyanin), proteins and poly-

saccharides, highlighting the carrageenan and agar (Carpena et al.,

2021). Carrageenan has been widely studied due to its potential as

anticoagulant, antithrombotic, antiviral, antitumor, antimicrobial,

antioxidant, biological properties both in vitro and in vivo (Carpena

et al., 2021).

Gigartina pistillata is an edible underexplored carrageenophyte which

produces a heterogeneous type of sulfated carrageenans, which as in

other Gigartina species, are determined by the life cycle phase (Mateo-

s-Aparicio et al., 2018), presenting either kappa/iota carrageenan

(gametophyte phase) or lambda carrageenan (tetrasporophytic phase)

(Cotas et al., 2020). The carrageenans obtained vary depending on the

species used, normally producing complex hybrids rather than pure

carrageenans. The structure of carrageenan type is dened by the

presence of 3,6-anhydro-D-galactose, the number and position of sulfate

* Corresponding author.

E-mail address: matorres@uvigo.es (M.D. Torres).

Contents lists available at ScienceDirect

Food Hydrocolloids

journal homepage: www.elsevier.com/locate/foodhyd

https://doi.org/10.1016/j.foodhyd.2024.110390

Received 21 March 2024; Received in revised form 12 June 2024; Accepted 5 July 2024

Food Hydrocolloids 157 (2024) 110390

groups, and the conformation of the pyranosidic ring (G´

omez-Ord´

o˜

nez

& Rup´

erez, 2011). For instance, kappa carrageenan is usually obtained

from Kappaphycus alvarezii (commercially known as “cottonii”), iota

carrageenan from Euchema denticulatum, and lambda carrageenan from

different species of Gigartina and Chondrus (Pereira & van de Velde,

2011). Depending on the type of carrageenan the chemical composition

and, hence, their rheological properties can differ. Kappa and iota

carrageenan contain 3,6-anhydro-galactose units, being kappa carra-

geenan able to form hard, strong, and brittle gels, while iota carrageenan

forms soft and weak gels. Lambda carrageenan does not have the ability

to form gels (it only contains galactose residues), and it is used as a

thickening agent (Pereira & van de Velde, 2011). Considering all the

above, and although the controversial around the use of carrageenan, it

has become a promising biopolymer to be used in the food, pharma-

ceutical and biomedical industries via the manufacture of exible edible

lms and coatings (Sedayu et al., 2019), as thickening/gelling agent (Zia

et al., 2017), or as drug delivery system (Li et al., 2014) amongst others.

Although conventional methods for extracting carrageenan can be

effective, they are based on the use of alkali mixtures such as KOH

(Raquzzaman et al., 2016) or NaOH (Al-Alawi et al., 2011; Azevedo et

la., 2013) which has environmental consequences. In contrast, the

employment of subcritical water is an interesting alternative, green

technology. High temperatures enable the recovery of water-soluble

compounds due to the self-ionization of water (Cheng et al., 2021).

The carrageenan obtainment by water extraction methods is still an

under explored strategy; however, Gereniu et al. (2018) studied the use

of subcritical water in combination with ionic liquids to recover carra-

geenan from Solomon Islands red seaweed, while Bahari et al. (2021)

evaluated the temperature (22–90 ◦C) and extraction time (2–8 h).

The current work aims to study the potential of the red seaweed

Gigartina pistillata as a source of proteins and carrageenan. For that

reason, it was processed by an environmentally friendly process such as

subcritical water, and the carrageenan was subsequently precipitated

with ethanol. The biopolymer was thoroughly characterized to deter-

mine its physiochemical properties and further analyzed via an ELISA

test to determine their inuence on the immune response and were

subsequently utilized to produce hydrogels which were further charac-

terized in terms of physiochemical properties and cell viability studies.

Fig. 1. Flow diagram of the experimental and analytical stages in the present study.

Table 1

Characterization of the raw material Gigartina pistillata, expressed in dry basis,

except moisture.

Component Content

Moisture (%, d.b.) 8.75 ±0.20

Ash (%, d.b.) 19.87 ±0.03

AIR (%, d.b.) –

Proteins (%, d.b.) 12.89 ±0.07

Carbon (%, d.b.) 29.45 ±0.27

Hydrogen (%,d.b.) 4.59 ±0.08

Sulfates (%, d.b.) 11.73 ±0.01

Extractives (%, d.b.) 4.51 ±0.03

Carbohydrates (%, d.b.) Glucose in polymeric units 7.69 ±0.31

Galactose in polymeric units 40.30 ±0.53

Minerals (mg/kg) Calcium (Ca

) 4578

Potassium (K

) 1458

Magnesium (Mg2+) 5659

Sodium (Na

) 20,299

Phosphorous (P3+) 1458

Zinc (Zn

) 94.50

Iodine (I

−

) –

Heavy metals (mg/kg) Arsenic (As

) 11.20

Cadmium (Cd

) 0.40

Copper (Cu

) 3.90

Mercury (Hg

) <20

Iron (Fe

) 85.40

Lead (Pb

) 0.50

Data are given as mean ±standard deviation, except for minerals and heavy

metals where standard deviations were <2% in all cases and were independently

studied.

M. ´

Alvarez-Vi˜

nas et al.

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