Comparison of microalgal biomass profiles as novel functional ingredient for food products
Highlights
► Chemical composition and TGA response of microalgae species for food industry ► Carotenogenesis related to main differences in microalgal physicochemical profile ► Green C. vulgaris and S. maxima present high protein and low fat contents. ► Carotenoid-rich C. vulgaris and H. pluvialis show high fat and thermal resistance. ► D. vlkianum and I. galbana show high protein/fat contents with PUFAω3 (EPA + DHA).
Introduction
Microalgae can use solar energy efficiently to transform wastewater, surplus CO2 and possibly some additional nutrients into a green biomass rich in lipids, sugars, proteins, carbohydrates and other valuable organic compounds. These microorganisms convert inorganic substances such as carbon, nitrogen, phosphorus, sulfur, iron and trace elements into organic matter such as green, blue-green, red, brown and other color biomass.
Microalgae are a potentially great source of natural compounds, which could be used as functional ingredients [1]. There is a large number of available microalgae species, and knowledge of the chemical composition is mandatory as a first step in a screening methodology, since it will help to target valuable compounds, pigments, antioxidants, polyunsaturated fatty acids (PUFAs), etc., in the studied microalga.
As with any higher plant, the chemical composition of algae is not an intrinsic constant factor but varies over a wide range. Environmental factors, such as temperature, salinity, illumination, pH-value, mineral content, CO2 supply, population density, growth phase and physiological status, can greatly modify chemical composition [2]. Most of the environmental parameters vary according to season, and the changes in ecological conditions can stimulate or inhibit the biosynthesis of several nutrients. Hence the growing conditions could be optimized to maximize the production for the biomolecules of interest. Because algae must adapt rapidly to the new environmental conditions in order to survive, they produce a great variety of secondary (biologically active) metabolites, with structures which cannot be found in other organisms [1].
The addition of microalgal biomass to food products is an interesting tool for providing nutritional supplementation with biologically active compounds (e.g., antioxidants, PUFA-ω3), besides coloring purposes. Accordingly, the selection of microalgae species with balanced nutritional profiles is fundamental for successful novel foods development. A detailed physicochemical characterization of the microalgae is an essential stage that will allow determining which algae are best suited for different applications and purposes.
In recent years, some research has been carried out by our team regarding the development of a range of novel attractive healthy foods, prepared from microalgae biomass, rich in carotenoids and polyunsaturated fatty acids with important health properties due to antioxidant and anti-inflammatory effects [1]. At the same time toxicological studies involving all the microalgae to be incorporated are being conducted [3]. Traditional foods, such as mayonnaises/salad dressings [4], puddings/gelled desserts [5], biscuits/cookies [6] and pasta [7], were supplemented with biomass from different microalgae, to add coloring and functional attributes, making the products more sensorially attractive and with possible health benefits.
Microalgae are recognized as an excellent source of natural colorings and it is expected that they will surpass synthetics as well as other natural sources due to their sustainability of production and renewable nature [8]. The European Commission has been committed to enquire the toxicity and replace the 46 authorized food colors [9], since some of them have recently been considered responsible for allergenic and intolerance reactions, namely increased hyperactivity in children [10]. Green algae typically present primary carotenoids (e.g., β-carotene, lutein, violaxanthin), which are distributed within the chloroplasts of green algae (thylakoid membranes), along with chlorophylls. A carotenogenesis process can be induced in response to nutrient starvation or other stressed conditions, i.e., environmental conditions (e.g., light, salinity and nutrients) that result in a metabolic imbalance which requires biochemical and metabolic adjustments before a new steady state of growth can be established [11]. Carotenogenic microalgae present secondary carotenoids, such as canthaxanthin and astaxanthin, accumulated in lipid globules, mainly outside the chloroplast plastids [12] accompanied by a decrease in the chlorophyll content of the cells.
The application of microalgal biotechnology for other purposes, such as biofuel production has been estimated to currently cost 15 to 20 times more than the permissible cost of oil rich cell mass required as raw material for fuel [13]. In fact, while microalgae-derived biodiesel, to be competitive, must be sold at less than 1€/L, microalgal biomass is sold at 36–50€/kg for human and animal nutrition, and fine chemistry compounds reach values of: 215–2150€/kg β-carotene, 43€/g DHA, 7€/mg astaxanthin, 11–50€/mg phycobiliproteins [14]. Therefore, the use of microalgae as a source of functional foods is a priority area in algal technology, to promote a cost effective microalgae production system with environmental and health-related beneficial effects.
The aim of the present work is to characterize the proximate composition, fatty acids profile, pigments profile, mineral content and thermal properties (DSC—Differental Scanning Calorimetry and TGA—Thermogravimetric analysis) of the five microalgae strains that were used in the above mentioned food products: Spirulina (Arthrospira) maxima, Chlorella vulgaris (green and carotenogenic), Haematococcus pluvialis (carotenogenic), Diacronema vlkianum and Isochrysis galbana.
S. (Arthrospira) maxima is a filamentous Cyanobacterium largely used as feed and food supplement. This alga grows profusely in certain alkaline lakes in Mexico and Africa, forming massive blooms, and has been used as a staple food by local populations since ancient times [15]. Since the late 1970s, it has been extensively produced around the world (Hawaii, California, China, Taiwan, Japan) using open raceway ponds [16]. A total production of 3000 tons/year [14] is estimated, being broadly used in food and feed supplements, due of its high protein content and its excellent nutritive value, such as high γ-linolenic acid (GLA; 18:3ω6) and vitamin B12 level [17]. This alga is the main source of phycocyanin, used as a natural food, cosmetic coloring, and as a biochemical tracer in immunoassays, among other uses [18].
C. vulgaris and H. pluvialis are green algae (Chlorophyceae), which are able, under certain culture conditions (light stress, nutrient depletion and high salinity), to accumulate high concentrations of carotenoids in order to protect against oxidation [19], [20].
Chlorella has been used as an alternative medicine in the Far East since ancient times and it is known as a traditional food in the Orient. The commercial production of Chlorella as a novel health food commodity started in Japan in the 1960s and nowadays, Chlorella is widely produced and marketed as a health food supplement in many countries, including China, Japan, Europe and the US, with an estimated total production around 2000 ton/year [14].
H. pluvialis has been identified as the organism that can accumulate the highest level of astaxanthin in nature (1.5–3.0% dry weight), which is currently the prime natural source of astaxanthin for commercial exploitation [21]. During the 1990s in the USA and India, several plants began large-scale production of H. pluvialis, particularly as pigmentation source in farmed salmon, trout and poultry industries, as well as for nutraceutical and pharmacological applications [22].
D. vlkianum and I. galbana (Haptophyceae) are widespread marine microalgae. I. galbana is widely used as feed species for commercial rearing of many aquatic animals, particularly larval and juvenile molluscs, crustacean and fish species [23] due to high PUFA-ω3 accumulation [24], [25]. D. vlkianum has been less studied, but higher growth rates and low mortality for the Pacific oyster Crassostrea gigas larvae have been reported [26]. These microalgae are also potentially promising for the food industry as a valuable source of Long Chain PUFA's, mainly eicosapentaenoic acid (EPA, 20:5ω3) and docosahexaenoic acid (DHA, 22:6ω3), in alternative to fish oils, supplying also sterols (mainly sitosterol), tocopherols, coloring pigments and other nutraceuticals [24], [25].
The present study intended to provide compiled biochemical information useful for choosing the microalgae best suited to specific food applications (rich in protein, PUFA, pigments, etc.). It is intended to compare well-known microalgae, approved for human consumption and/or for animal nutrition. In fact, although microalgae are consumed since ancient times, most of them are considered as unconventional food items and have to undergo a series of toxicological tests to prove their harmlessness. Hence, it is important to use microalgae that have already surpassed these tests for food industry applications. This is the case of Spirulina and Chlorella, while Astaxanthin-rich extracts derived from H. pluvialis have been approved for several companies [27]. The successful authorization of these microalgal based foods and food ingredients broaden perspectives for a wider inclusion of these valuable microorganisms in the human diet.
Section snippets
Microalgae production
S. maxima (Setchell & Gardner, LB 2342) was obtained from the University of Texas Culture Collection (Austin, USA) while I. galbana and D. vlkianum were obtained from Mary Parke collection (Plymouth Laboratory, UK). C. vulgaris (INETI 58) and H. pluvialis (INETI 33) were isolated in LNEG Campus (Lisbon, Portugal). These microalgae were produced in the Bioenergy Unit, LNEG and in IPIMAR/L-INRB (both in Lisbon, Portugal).
Microalgae were cultivated through inoculation of axenic microalgal
Proximate composition
The major differences in biochemical composition of the six microalgae studied were related to the induction of carotenogenesis process in C. vulgaris (orange) and H. pluvialis. Nevertheless, each microalga presented a typical biomass nutrient profile, allowing the selection of desired physicochemical characteristics for specific food technology applications.
Results obtained from the biochemical characterization of microalgal biomass are collected in Table 1. Freeze dried microalgal biomass
Acknowledgments
This work is part of the research projects PTDC/AGR-ALI/65926/2006 and PTDC/AAC-AMB/100354/2008 sponsored by the Portuguese Foundation for the Science and Technology (“Fundação para a Ciência e a Tecnologia”—FCT). A.P. Batista acknowledges the PhD research grant from FCT (SFRH/21388/BD/2005). The authors also thank the Editor and Reviewers comments and suggestion which contributed to the overall quality of this paper, as well as English proofreading by Charles Sangnoir.
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