Ulva lactuca: History Edit
Subjects: Plant Sciences

Ulva lactuca is a macroalgae and belongs to the phylum Chlorophyta, described by Linnaeus in the Baltic Sea in the seventeenth century [1]. It is able to grow attached, sessile or free floating. The capacity to reproduce involving two methods, one being sexual and the other being from fragmentation of the thallus, is rarely observed in macroalgae [2], but this provides a capacity for it to rapidly proliferate by covering the water surface, decreasing the biodiversity even for other algae species [3]. Ulva lactuca is a polymorphic species with morphologies dependent on the degree of water salinity [4] or symbiosis with bacteria [1].

Macroalgae (or seaweeds) contain high amounts of carbohydrates (up to 60%), medium/high amounts of proteins (10–47%) and low amounts of lipids (1–3%) with a variable content of mineral ash (7–38%) [5]. With decreasing available land and fresh-water resources, the oceans have become attractive alternatives for the production of valuable biomass, comparable to terrestrial crops. Macroalgae cultivated under controlled and sustainable cultivation systems are probably the future method for supplying biomass to meet market development needs [6].
The high carbohydrate fraction includes a large variety of easily-soluble polysaccharides, such as laminarin, alginate, mannitol or fucoidan in brown types; starch, mannans and sulphated galactans in red types and Ulvan in green types [7]. Alginate, one of the main structural polymers of brown seaweeds, provides both stability and flexibility for the specimens exposed to flowing water, and is one of the industrially-relevant carbohydrate compounds found in seaweed biomass, as are other hydrocolloids, such as agar and carrageenans, which are commonly used as thickeners, gelling agents or emulsifiers. Various other non-carbohydrate products obtained from seaweeds include protein, lipids, phenols and terpenoids, and minerals such as iodine, potash and phosphorus—useful for human and animal nutrition [8]. The harvesting of macroalgae—a valuable raw material for food—before they beach could well be developed into an effective solution [9]. The interest of macroalgae in human nutrition is due to their high mineral concentrations (such as calcium, magnesium and potassium) and glutamic acid, which makes them also useful as taste enhancers. Algae could help to address one of the biggest challenges currently faced by the food industry, which is the ever growing human population. Algae are also a source of active principles largely unexplored for pharmaceutical products [7]. The gelling properties of polysaccharides are well known, and the therapeutic applications are in development [10,11]. Algal polysaccharides, pigments, proteins, amino acids and phenolic compounds are potential functional food ingredients for health maintenance and the prevention of chronic diseases, with increasing potential uses in pharmaceutical industries [12].
Ulva lactuca polymorphism dependent upon the environment led to the proposal that different species may exist, such as Ulva armoricana, rigida, prolifera, pertusa, fasciata or rotundata [1,2,3,4]. However, genetic analysis revealed that the different phenotypes observed were not based on genetic variations that would justify the existence of different species other than Ulva lactuca [13]. Taxonomy is challenging for the genus Ulva, which belongs to the phylum of Chlorophyta, constituting four traditional classes (UlvophyceaeTrebouxiophyceaeChlorophyceae and Chlorodendrophyceae) that evolved from unicellular marine planktonic prasinophyte algae in the Neoproterozoic [1]. Trebouxiophyceae and Chlorophyceae are found mainly in fresh water while Ulvophyceaecolonize mainly shallow marine environments, similar to the Australian Collerpa that has colonized the Mediterranean Sea since 20 years ago. Linnaeus was the first to observe that Ulva lactuca could have different phenotypes with a tubular or a sheet-like tail, but taxonomists in the nineteenth century proposed that the tubular green algae were a distinct genus called Enteromorpha. However, molecular approaches demonstrated that Linnaeus was correct—Ulva and Enteromorpha are not distinct genera [13]. Different Ulva species are still described in the literature [14], but it turns out that reproduction is possible between these different “species”, which therefore should be described as Ulva lactuca variants or clades.
Ulva blooms damage marine ecosystems and impair local tourism [9]. Ulva principally invades beaches, and its biodegradation can produce acidic vapors that have induced the death of animals and possibly humans since a horse was reported dead in 2009 on the Brittany coasts (located at the west of France) due to Ulva biodegradation [2]. The first Ulva bloom to be described was in Belfast (in the north of Ireland) at the end of the nineteenth century [15]. Ulva blooms were well-studied in the Laguna of Venice from 1930, with an unexplained decrease observed after 1990 [16,17]. Since 1980, Ulva blooms have been observed worldwide, from Galicia [18] to Tokyo Bay [19], including the American [20] and Australian continents [14]. However the largest events in the world to date have been the green tides observed in the Yellow Sea for ten consecutive years from 2007 and covering 10% of the Yellow Sea [21]. In Europe, Brittany’s north coasts have the biggest Ulva blooms [3]. While there is no doubt that Ulva blooms are due to human activities, it is generally farmers who are accused of being fully responsible for Ulvablooms because of their use of fertilizers [2,3]. However, for the green tides of Belfast and Venice, a correlation was established with human waste, due to an increase of workers [15] or tourists [17]. Furthermore, abundant sources of nitrogen and phosphorus are important for Ulva blooms, but phosphorus does not come from agricultural activity [2] and it is difficult to determine what part of nitrogen is due to fertilizers or human waste.
Preliminary experiments suggest that in the Mediterranean seas there is a virus that might provide a natural and ecological way to control Ulva blooms. Ulva blooms occur in the Mediterranean seas but disappear rapidly, and an enzyme activity related to giant viruses was observed in the bay of Marseille on denatured Ulva tissues (manuscript in preparation). Viruses are well known to participate in the control of microalgae blooms, but this is not demonstrated for macroalgae. Virus controls of microalgae blooms were recently observed in USA, with the two macroalgae Aureococcus anophagefferens inducing harmful bloom algae on the east coast [22] or Tetraselmis in Hawaii [23]. In these two cases, it was because of viruses that have been recently discovered and have been called giant viruses. Giant viruses were first discovered in amoebae [24]. While most viruses known over the past century have a size < 200 nm, such as 160 nm for HIV or 20 nm for the smallest virus (Parvoviridae infecting pigs), giant viruses have a size of up to 1 µm. Since then, giant viruses have been discovered all across the world, infecting many species, particularly marine species [25].
Ulva contains commercially valuable components susceptible of being exploited for cosmetic, pharmaceutical, chemical, food and energy applications [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26] and this review provides a background on products that might be obtained from Ulva, as well as the processing technologies used to date.

2. Potential Riches of Ulva

The integral valorization could represent a more sustainable approach—contributing to biorefinery processes—to valorize different constituents of Ulva offering alternatives to global environmental concerns. Two aspects favor this utilization, valuable products found in Ulva and its high productivity [7].

2.1. Ulva Bioactive Compounds

Ulva protein hydrolysates show antioxidant [27], angiotensin-converting enzyme (ACE)-inhibitory activity [28] and immunomodulatory effects [29]. Ulva has starch (1–4%) as a reserve polysaccharide. Furthermore, Ulva has water-soluble and insoluble cellulose (38–52%) corresponding to structural polysaccharides with a major component called Ulvan. Ulvans are sulphated heteropolysaccharides that contribute to the strength of the cell wall and give flexibility to Ulva, preventing Ulva desiccation for tides. Ulvan is up to 30% Ulva dry weight and contains mainly sulfonic acids, sulphated l-rhamnose, xylose and glucose. This polysaccharide and its oligosaccharides have anti-viral, anti-tumour, anti-coagulant, anti-lipidique, hepato protective, immuno-stimulating, anti-depressant and anti-anxiolytic activities [26,30], and are increasingly requested for pharmaceutical and food applications. In addition, Ulvans are thermos reversible gels, with industrial applications in the chemical, pharmaceutical, biomedical and agricultural areas [26,27,28,29,30]. The commercial application of these gels is not yet as developed as other algal hydrocolloids [31]. However, interesting recent applications were reported with a composite material made of zinc oxide and calcium carbonate capped with Ulva polysaccharides for burn treatments [32]. Ulva carbohydrates can also be a carbon source for microbial production of biomaterials and building blocks to produce a range of chemicals and intermediates, such as organic acids, alcohols and biomaterials, but this market is still emerging [31].
Ulva has a unique fatty acid profile characterized by high levels of alpha linolenic acid (18:3ω-3) and stearidonic acid (18:4ω-3), the latter being an efficient precursor of eicosapentaenoic acid synthesis able to increase its human tissue levels [12,32]. In addition, Ulva contains phenolic, chlorophyll and carotenoids, which can be regarded as active free-radical scavengers [32]. The balanced content of Na and K (a ratio near to 1) is nutritionally beneficial [12]. A double-blinded versus placebo clinical trial showed that an Ulva water-soluble extract rich in oligo-elements (up to 50% and proteins of 10–20%) had a beneficial effect on depression [30].

2.2. Ulva for Food

Ulva can be a source of essential amino acids—some of them, such as histidine, are found in levels comparable to those found in legumes and eggs [12]. Traditional food uses the whole Ulva, which is also spread on agricultural land or composted, but these solutions rapidly reach their limits and have little added value. To eat Ulvafrom green tide is safe, and it is a valuable nutriment based on its high content of proteins and Fe, a good unsaturated lipid acid with a low-fat ratio and also has the presence of essential amino acids [21]. It is important, however, to verify that the concentrations of heavy metals, pesticides and polycyclic aromatic hydrocarbon is under regulation limits. Ulva from green tide could be used for a phytoremediation process of coastal water contaminated with bisphenol A [33]. The removal efficiency was positively influenced by light, nutrients and temperature, and salinity had no effect. This endocrine disruptor is rapidly and efficiently removed (more than 90%) by fresh Ulva,whereas less than 5% could be removed from dead algal biomass.
Ulva can be used to feed fish or mollusks such as abalone and reinforce immunity [34]. Ulva is now used in integrated multi-trophic aquaculture systems as a partial replacement or supplement for the diet of juvenile Litopenaeus vannamei [35]. Harvested Ulva contains a large amount of proteins (up to 30%) with a similar amino acid profile regarding commercial diet, but lower lipid levels (1.9%) and no docosahexaenoic acid. The replacement of up to 25% of the commercial diet with fresh Ulva does not impact shrimp production and juvenile shrimps fed with Ulva have a better growth rate, a higher carotenoid content and a lower lipid content, found in examining shrimp carcasses [36].
Agricultural utilization of Ulva extracts was reported to enhance the vegetative growth in bean plants under drought stress, limiting the lipid peroxidation, increasing the phenolic content and probably contributing to the enhancement of the antioxidant enzymatic activity [37]. Ulva aqueous extracts enhance the vegetative growth under drought stress conditions and antioxidant potential for Salvia officinalis [38].
The utilization of a single fraction from Ulva biomass has been explored and this alternative is recommended when the biomass is destined to a high value added application. Acidic Ulva extracts were used to replace synthetic antioxidants and to protect different cosmetic products from oxidation [39]. Ulva aqueous extracts were used for the synthesis of gold and silver nanoparticles, with excellent biocompatibility on healthy cells and were highly cytotoxic against colorectal cancer cell lines HT-29 and Caco-2 [40]. A new food-grade protein extraction protocol was proposed from Ulva and showed high digestibility in simulated gastro-intestinal tests with a high antioxidant activity [27].
Ulvan, proteins and amino acids offer key opportunities to deliver multiple products and energy through a biorefinery process [41,42]. In a study to explore the use of offshore grown macroalgae as a sustainable feedstock for biorefineries, it was estimated that the annual productivity for Ulva (838 g C/m2 year) was higher than the global average (290 g C/m2·year) estimated for terrestrial biomass in the Middle East [43]. Similarly, it was found that Ulvacan offer the best performance for a future biorefinery (15 g dry weight/m2 d and 56 t/ha year) [44].

2.3. Production of Biofuels

The valorization of Ulva biomass for the production of biofuels is attracting attention regarding three aspects: bioremediation for the ecosystem, a renewable energy source and economic savings [45]. Ulva can be an attractive source for biofuels, since its production does not require arable land and fertilizers. Ulva can grow in saline and waste water and has a higher ability in sequestering atmospheric CO2 than terrestrial energy crops [46]. In addition, the growth rate and productivity are high compared to those of land crops, and they can withstand harsh conditions to survive under stressful conditions. The most studied biofuels are biodiesel, bioethanol and biogas. Ulva could be an alternative to conventional oil crops because they contain oil, suitable for esterification/transesterification reactions for the biodiesel production [47]. For biodiesel production, hexane is one of the most suited, but other organic solvents or their mixtures have been proven suitable for oil extraction from Ulva biomass [48].
After harvest, Ulva biomass requires pre-treatment and/or saccharification and fermentation to be converted in bioethanol. Carbohydrates contain hexose sugars, which are suitable materials for fermentation in producing ethanol. The hydrolysis of these polysaccharides results in monosaccharides, such as glucose, mannose and galactose. These carbohydrates are easily fermentable compounds in anaerobic digestion, and their extraction makes possible a rapid degradation. The quantities of cellulose and lignin, normally abundant in terrestrial biomass, are generally lower in Ulva and in the macro algal genera because of the different structural requirements in aquatic environments [49].
The production of the third-generation bioethanol from marine macroalgae depends mainly on the development of an eco-friendly and eco-feasible pre-treatment (i.e., hydrolysis), a highly effective saccharification step, and, finally, an efficient bioethanol fermentation step. Ulva has cellulose as a main structural component. Different hydrolysis processes are suitable to maximize the extraction of fermentable sugars, such as thermochemical hydrolysis with diluted acids (HCl and H2SO4) and a base (NaOH), and hydrothermal hydrolysis followed by saccharification with different fungal strains, preferentially adapted to the medium [50,51]. Also chemical-free treatments are beneficial. Efficient solubilization (over 90% of sugars) can be achieved by hot-water treatment, and further hydrolysis using cellulases and bioconversion is favored by the lack of enzyme and microbial inhibitors. In addition, nutrient supplementation is not required. Hot-water treatment of Ulva, followed by hydrolysis with cellulases, makes possible the production of fermentation media that can be easily converted into acetone, butanol and ethanol by a microorganism such as Clostridium sp. [52].
Pre-treatment (physical, chemical, enzymatic) of macroalgae has considerable influence on the technical, economic and environmental sustainability of biogas production. Different pre-treatments of Ulva for biogas production were compared, and the reducing sugar yields demonstrate that enzymatic pre-treatment was superior to acid catalysis, thermos alkaline and ultra-sonication [53]. Ulva wastes collected from coastal areas can produce up to 166 L CH4/kg volatile solids, whereas from food wastes and sewage sludge produce 350–380 L CH4/kg volatile solids [54]. Higher biogas yields from Ulva biorefinery facilities yielded up to 271 mL CH4/kg volatile solids (VS) in the range of methane production from cattle manure and crop land-based energies [41]. Enhanced bio methane production was observed in pretreated biomass and also in co-digestion processes [55].
A new promising alternative is the production of hydrogen from Ulva through dark or anaerobic fermentative technology [56,57]. The type of pre-treatment is important on the process performance, which can be improved with combinations of more than one pre-treatment and by the use of mixed anaerobic cultures [57].

3. Processes and Strategies to Extract Component from Ulva

Attempts to valorize Ulva collected on beaches leads to different problems, such as contamination with sands and pollutants from different origins. Industrial processes to produce artificially Ulva were developed to offer a production that is economically feasible and to attain a rational utilization of biomass following a biorefinery approach [58] since the sequential extraction of value-added products in a biorefinery is more efficient and viable [59]. The content of biologically active substances from natural origins depends on the site of the material collection, season and environmental conditions [60]. The medium nutrient content influences the fatty acid content; the ω-6/ω-3 fatty acids ratio and also the chlorophyll, carotenoid and phenolic contents, and therefore the antioxidant and anti-inflammatory properties [32]. Also, the extraction technology and operational conditions have a marked influence on the yields and on the properties of the target compounds.
In order to selectively separate the target components from natural materials, a solvent extraction stage is required. The solvent extraction process is a mass transfer unit operation from a solid material with a solvent, which shows preferential affinity for the target solutes. Different variables are important in the final yield: particle size, solvent type, solvent to solid ratio and temperature. These operational conditions require individual or combined optimization in order to maximize yields, the extraction rate and the purity and properties of the products.
 

3.1. Conventional Processes

Solvents can be different, depending on the polarity and location of Ulva components. An aqueous solvent is suitable for polysaccharides, which is the most abundant fraction. Oil and pigment fractions require less polar solvents. Ulvan is usually extracted with a high yield from hot water and pressurized conditions [61]. Ulvans are thermally stable until approximately 180 °C and present a high correlation between sulphate contents, their reducing power and their scavenging activity [62]. Water extraction of sulphated ulvan gives a product with a high antimicrobial activity against Enterobacter cloace and Escherichia coli [63]. A simple acidic method for extraction of Ulvan, with relatively low content of protein and high sulphate, is frequently used [30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64]. The properties and bioactivities of polysaccharides can be modulated by the extraction conditions; where rhamnose, glucuronic acid and glucose are the major monosaccharides obtained at 90 °C with 0.01 M HCl. Glucose is the major monomer at 150 °C with 0.1 M HCl, and the sulphate content is also influenced by temperature and acid concentration. These parameters have an effect on functional properties, such as oil holding capacity, foaming capacity, stability, antioxidant activity and pancreatic lipase inhibition activity, which are modified [65].
Ulvan extraction is better with a coagulation–sedimentation process to shorten the filtration time of the residual biomass after the extraction step, although this chemical treatment reduced the yield due to coprecipitation [66]. The extraction of proteins and glycoproteins from Ulva is more efficient with lysis solutions containing surfactants than with buffer or deionized water alone. The proteins further hydrolyzed with protease confirmed the availability and the lack of cytotoxicity in Vero cells [60]. The selection of the solvent system for oil extraction is an important factor for fuel production. Simultaneous distillation and extraction to prepare volatile compounds (aldehydes, ketones, carboxylic acids, alcohols and hydrocarbons) show antimicrobial activities and inhibition of tyrosine kinase [67].
An important group of bioactive compounds are phenols, although their content in green algae is lower than in brown types. They are usually extracted with organic solvents, the type of solvent being important on the extract yields and properties. Conventional solvent extraction with methanol or ethanol is used for the extraction of phenols and ethyl acetate [37,68,69,70,71]. Higher yields of pigment and phenolic were obtained using 95% ethanol, and carotenoids using acetone [32]. However, Ulva extracts show lower phenolic content and antioxidant properties compared with other natural materials or synthetic antioxidants [68].

3.2. Biorefineries

Ulva blooms represent a non-competitive green source for production of biofuels and other commodity materials. Abundant recent studies have confirmed the potential of Ulva for biorefinery. A general scheme following this strategy is shown in Figure 1. The major challenges for seaweed biorefineries are in relation with the production of high value products, the lower use of chemicals and waste disposal. The integrated biorefinery philosophy can solve different problems associated with the algal biomass conversion to bioenergy [46,72]. A marine biorefinery could be a solution to intensify Ulva production to obtain bioethanol [73]. The content of monosaccharides released by acid hydrolysis from different seaweeds was compared, revealing that Ulva has the highest economic potential [74].
 
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Figure 1. Simplified scheme of a biorefinery process according to final utilizations [83]. Different washing steps were proposed to remove salts. After evaporation of the washing water, the protein content increased by 11–24% and the energy content by 20–50%. The adequate selection of the operating procedures (temperature, filtration and chemical treatment) determined the chemical composition of extracts.
 
Macro algal proteins and oligo- and polysaccharides are potential raw materials for the new generation of health ingredients having both techno- and bio-functional applications. Their extraction is usually placed in initial steps and the latter steps are usually those leading to biofuels [75]. The interest to extract valuable components present in the biomass in initial steps (phenolic and protein fractions) is to improve the economy of ethanol production and favor industrial implementation [76]. The utilization of the protein fractions would represent an opportunity for developing countries, which permanently face a protein shortage. The extraction processes should provide high protein yields, preserving the quality (amino acid profile and digestibility) and avoiding the presence of antinutritional compounds. Moreover, the extraction process should find its optimal placement in the whole bioethanol production chain.
Different washing steps have been proposed to remove salts for food applications [77]. After the evaporation of the washing water, the remaining solid biomass has a higher protein content from 11 to 24% and energy content from 20 to 50%. Regarding Ulva phenotypes, the content in salts goes from 29% to 36% with Na/K ratios from 1.1 to 2.2 and a maximum at 19% ulvan.
Mixing enzymatic and chemical extractions is proposed to maximize the extraction of high molecular ulvan fractions with gelling properties [78]. The adequate selection of the operating procedures (temperature and acid concentration) determines the chemical composition of ulvan and also the rheological and textural properties. Ulvainsoluble dietary fiber shows high values in water holding capacity and oil holding capacity—comparable to other commercial fibers—which is suitable for the formulation of low caloric foods and in the stabilization of foods rich in fat and emulsion.
The feasibility was tested using Ulva residues remaining after the extraction of polysaccharides as an energetic source after a pre-treatment with hydrogen peroxide to enhance the efficiency of enzymatic hydrolysis and bioethanol yields [21]. The production of methane could be possible from the solid wastes of Ulva after sap extraction, Ulvan extraction and protein extraction, or after the sequential extraction of all these components. The highest methane yield of 408 L CH4/kg VS was observed in sap and Ulvan-removed residue, suggesting that the high protein and sulphate content are major inhibitors in anaerobic digestion [59].
An interesting valorization is obtained from leftovers due to the Ulva polysaccharide extraction process using hot water and enzymes [79]. This material was added to potato chip dough at a level of 2.5%. The water activity of chips with this Ulva extract was significantly less than other control chips without Ulva. The addition of Ulva leftovers increased the protein, ash and dietary fiber contents of baked potato chips. However, sensory scores showed that green algal addition produced an unacceptable color and strong seaweed flavor. The solid residue after the extraction of Ulva polysaccharides was also used to promote growth and to enhance non-specific immune and disease resistance enhancement against Vibrio parahaemolyticus in white shrimp Litopenaeus vannamei [80]. The animal mortality in the group fed with Ulva leftovers was lower compared with the control; the survival in the group fed with the polysaccharides extracted with cold water was 80%. In the group feed with the polysaccharides extracted with hot water, it was 65%, and in the control group, it was 40%.
An original biorefinery approach is proposed to isolate sugars from Ulva [81]. The sugars in the biomass are solubilized by hot water treatment followed by enzymatic hydrolysis and centrifugation, resulting in a sugar-rich hydrolysate, and a protein-enriched extracted fraction, which could be advantageously used in animal feed compared to intact seaweeds. The content in essential amino acids and digestibility suggest a promising use in diets for monogastric animals. Reduction of the high content in minerals and trace elements may be required to allow a high inclusion level of Ulva products in animal diets. The hydrolysate is used successfully for the production of acetone, butanol, ethanol and 1,2-propanediol [82].
A multistep integrated process for the extraction of different products from Ulva provides opportunities to develop novel products and commercial applications [83]. The protein content is 11% in dry weight and protein digestibility is 86%, indicating its suitability for use in food supplements. The cellulose extraction is the final step in this integrated approach and is the least affected by the up-stream treatments compared to other components. A similar strategy using Ulva leftovers after enzymatic saccharification proposes a use for aquaculture food [84]. During saccharification, the relative ash and carbohydrate content is reduced, but total nitrogen, total carbon and lipid content increase, making possible the survival and growth of bivalve spat and commercially valuable sea urchins over the course of three-week preliminary trials. Finally, another biorefinery approach integrates the hydrothermal liquefaction for biomass conversion to produce fuels (bio-oil and gas), aqueous fertilizers and remediation agents for domestic and marine culture effluents [85]. This technology is now used to transform macroalgae into aqueous phase products. Ulva offers the highest bio-oil yields. Hydrothermal liquefaction is effective for Ulva conversion, giving the highest bio-crude yields up to 29.9% and containing up to 60% of the total biomass energy content.
 

Reference

  1. Wichard, ; Charrier, B.; Mineur, F.; Bothwell, J.H.; Clerck, O.D.; Coates, J.C. The green seaweed Ulva: A model system to study morphogenesis. Front. Plant Sci. 2015, 6, 72–82.
  2. Chevassus-au-Louis, ; Andral, B.; Femenias, A.; Buvier, M. Bilan des Connaissances scientifiques sur Les Causes de Prolifération de Macroalgues Vertes; Rapport Pour Le Gouvernement Français 2012. Report No.: CGEDD 007942-01 et CGAAER 11128; Conseil général de l'environnement et du développement durable: Paris, France, 2012. (In French)
  3. Pillard, S. Mise au Point sur Les Algues Vertes: Risques Environnementaux et Valorisations en 2016; Sciences Pharmaceutiques 2016, Dumas-01393938; Universite de Picardie Jules Verne: Amiens, France, 2016. (in French)
  4. Rybak, Species of Ulva (Ulvophyceae, Chlorophyta) as indicators of salinity. Ecol. Indic. 2018, 85, 253–261.
  5. Kraan, Pigments and minor compounds in algae. In Functional Ingredients from Algae for Foods and Nutraceuticals; Domínguez, H., Ed.; Woodhead Publishing: Cambridge, UK, 2013; pp. 205–251.
  6. Robin, ; Sack, M.; Israel, A.; Frey, W.; Müller, G.; Golberg, A. Deashing macroalgae biomass by pulsed electric field treatment. Bioresour. Technol. 2018, 255, 131–139.
  7. Pérez, J.; Falqué, E.; Domínguez, H. Antimicrobial action of compounds from marine seaweed. Mar. Drugs 2016, 14, 52–59.
  8. Neto, T.; Marçal, C.; Queirós, A.S.; Abreu, H.; Silva, A.M.S.; Cardoso, S.M. Screening of Ulva rigida, Gracilaria sp.; Fucus vesiculosus and Saccharina latissima as functional ingredients. Int. J. Mol. Sci. 2018, 19, 10–18.
  9. Smetacek, ; Zingone, A. Green and golden seaweed tides on the rise. Nature 2013, 504, 84–88.
  10. Popa, G.; Reis, R.L.; Gomes, M.E. Seaweed polysaccharide-based hydrogels used for the regeneration of articular cartilage. Crit. Rev. Biotechnol 2014, 3, 410–424.
  11. Morelli, ; Betti, M.; Puppi, D.; Chiellini, F. Design, preparation and characterization of Ulvan based thermosensitive hydrogels. Carbohydr. Polym. 2016, 136, 1108–1117.
  12. Lordan, ; Ross, R.P.; Stanton, C. Marine bioactives as functional food ingredients: Potential to reduce the incidence of chronic diseases. Mar. Drugs 2011, 9, 1056–1100.
  13. Hayden, S.; Blomster, J.; Maggs, C.A.; Silva, P.C.; Stanhope, M.J.; Waaland, J.R. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur. J. Phycol. 2003, 38, 277–294.
  14. Kirkendale, ; Saunders, G.W.; Winberg, P. A Molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J. Phycol. 2012, 49, 69–81.
  15. Letts, A.; Richards, E.H. Report on green seaweeds and especially Ulva latissima in relation to the pollution of the waters in which they occur. In Royal Commission on Sewage Disposal; 7th Report; HMSO: London, UK, 1911; Appendix III, Section II.
  16. Schiffner, ; Vatova, A. The Algae of the Lagoon: Chlorophyceae, Phaeophyceae, Rhodophyceae, Myxophyceae; Minio, M., ed.; The Lagoon of Venice: Venezia, Italy, 1938; Volume 3, p. 250. (In Italian).
  17. Curiel, ; Rismondo, A.; Bellemo, G.; Marzocchi, M. Macroalgal biomass and species variations in the lagoon of Venice (Northern Adriatic Sea, Italy): 1981–1998. Sci. Mar. 2004, 68, 57–67.
  18. Villares, R.; Puente, X.; Carballeira, A. Nitrogen and phosphorus in Ulva in the Galician Rias Bajas (northwest Spain): Seasonal fluctuations and influence on growth. Bol. Inst. Esp. Oceanogr. 1999, 15, 337–341.
  19. Yabe, ; Ishii, Y.; Amano, Y.; Koga, T.; Hayashi, S.; Nohara, S.; Tatsumoto, H. Green tide formed by free-floating Ulva spp. at Yatsu tidal flat, Japan. Limnology 2009, 10, 239–245.
  20. Charlier, H. Morand, P.; Finkl, C.W. How Brittany and Florida coasts cope with green tides. Int. J. Environ. Stud. 2008, 65, 191–208.
  21. Li, -Y.; Yang, F.; Jin, L.; Wang, Q.; Yin, J.; He, P.; Chen, Y. Safety and quality of the green tide algal species Ulva prolifera for option of human consumption: A nutrition and contamination study. Chemosphere 2018, 210, 1021–1028.
  22. Moniruzzaman, ; Gann, E.R.; Wilhelm, S.W. Infection by a giant virus (AaV) induces widespread physiological reprogramming in Aureococcus anophagefferens CCMP1984, a Harmful Bloom Algae. Front. Microbiol. 2018, 9, 752–758.
  23. Schvarcz, R.; Steward, G.F. A giant virus infecting green algae encodes key fermentation genes. Virology 2018, 518, 423–433.
  24. La Scola, ; Audic, S.; Robert, C.; Jungang, L.; de Lamballerie, X.; Drancourt, M.; Birtles, R.; Claverie, J.M.; Raoult, D. A giant virus in amoebae. Science 2003, 299, 2033–2038.
  25. Abergel, ; Legendre, M.; Claverie, J.M. The rapidly expanding universe of giantviruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. FEMS Microbiol. Rev. 2015, 39, 779–796.
  26. Cardoso, M.; Carvalho, L.G.; Silva, P.J.; Rodrigues, M.S.; Pereira, O.R.; Pereira, L. Bioproducts from seaweeds: A review with special focus on the Iberian Peninsula. Curr. Org. Chem. 2014, 18, 896–917.
  27. Kazir, ; Abuhassira, Y.; Robin, A.; Nahor, O.; Luo, J.; Israel, A.; Golberg, A.; Livney, Y.D. Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp.; for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates. Food Hydrocoll. 2019, 87, 194–203.
  28. Paiva, ; Lima, E.; Neto, A.I.; Baptista, J. Isolation and characterization of angiotensin I-converting enzyme (ACE) inhibitory peptides from Ulva rigida C. Agardh protein hydrolysate. J. Funct. Foods 2016, 26, 65–76.
  29. Cian, E.; Hernández-Chirlaque, C.; Gámez-Belmonte, R.; Drago, S.R.; Sánchez de Medina, F.; Martínez-Augustin, O. Green alga Ulva sp. hydrolysates and their peptide fractions regulate cytokine production in splenic macrophages and lymphocytes involving the TLR4-NFκB/MAPK pathways. Mar. Drugs 2018, 16, 235–241.
  30. Sari-Chmayssem, ; Taha, S.; Mawlawi, H.; Guégan, J.-P.; Jeftić, J.; Benvegnu, T. Extracted Ulvans from green algae Ulva linza of Lebanese origin and amphiphilic derivatives: Evaluation of their physico-chemical and rheological properties. J. Appl. Phycol. 2018, 3, 1–16.
  31. Violle, ; Rozan, P.; Demais, H.; Nyvall Collen, P.; Bisson, J.-F. Evaluation of the antidepressant- and anxiolytic-like effects of a hydrophilic extract from the green seaweed Ulva sp. in rats. Nutr. Neurosci. 2018, 21, 248–256.
  32. Cesário, T.; da Fonseca, M.M.R.; Marques, M.M.; de Almeida, M.C.M.D. Marine algal carbohydrates as carbon sources for the production of biochemicals and biomaterials. Biotechnol. Adv. 2018, 36, 798–817.
  33. Dumbrava, ; Berger, D.; Matei, C.; Radu, M.D.; Gheorghe, E. Characterization and applications of a new composite material obtained by green synthesis, through deposition of zinc oxide onto calcium carbonate precipitated in green seaweeds extract. Ceram. Int. 2018, 44, 4931–4936.
  34. McCauley, I.; Winberg, P.C.; Meyer, B.J.; Skropeta, D. Effects of nutrients and processing on the nutritionally important metabolites of Ulva sp. (Chlorophyta). Algal Res. 2018, 35, 586–594.
  35. Zhang, ; Lu, J.; Wu, J.; Luo, Y. Phycoremediation of coastal waters contaminated with bisphenol A by green tidal algae Ulva prolifera. Sci. Total Environ. 2019, 661, 55–62.
  36. Fleurence, ; Le Coeur, C.; Mabeau, S.; Maurice, M.; Landrein, A. Comparison of different extractive procedures for proteins from the edible seaweeds Ulva rigida and Ulva rotundata. J. Appl. Phycol. 1995, 7, 577–582.
  37. Laramore, ; Baptiste, R.; Wills, P.S.; Hanisak, M.D. Utilization of IMTA-produced Ulva lactuca to supplement or partially replace pelleted diets in shrimp (Litopenaeus vannamei) reared in a clear water production system. J. Appl. Phycol. 2018, 2, 3603–3610.
  38. Cruz-Suárez, E.; León, A.; Peña-Rodríguez, A.; Rodríguez-Peña, G.; Moll, B.; Ricque-Marie, D. Shrimp/Ulva co-culture: A sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 2010, 301, 64–68.
  39. Mansori, ; Chernane, H.; Latique, S.; Benaliat, A.; Hsissou, D.; El Kaoua, M. Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.). J. Appl. Phycol. 2015, 27, 1689–1698.
  40. Mansori, ; Chernane, H.; Latique, S.; Benaliat, A.; Hsissou, D.; El Kaoua, M. Effect of seaweed extract (Ulva rigida) on the water deficit tolerance of Salvia officinalis L. J. Appl. Phycol. 2016, 28, 1363–1370.
  41. Balboa, M.; Soto, M.L.; Nogueira, D.R.; González-López, N.; Conde, E.; Moure, A.; Vinardell, M.P.; Mitjans, M.; Domínguez, H. Potential of antioxidant extracts produced by aqueous processing of renewable resources for the formulation of cosmetics. Ind. Crop Prod. 2014, 58, 104–110.
  42. González-Ballesteros, ; Rodríguez-Argüelles, M.C.; Prado-López, S.; Lastra, M.; Grimaldi, M.; Cavazza, A.; Nasi, L.; Salviati, G.; Bigi, F. Macroalgae to nanoparticles: Study of Ulva lactuca L. role in biosynthesis of gold and silver nanoparticles and of their cytotoxicity on colon cancer cell lines. Mater. Sci. Eng. C 2019, 97, 498–509.
  43. Bruhn, ; Dahl, J.; Nielsen, H.B.; Nikolaisen, L.; Rasmussen, M.B.; Markager, S.; Olesen, B.; Arias, C.; Jensen, P.D. Bioenergy potential of Ulva lactuca: Biomass yield, methane production and combustion. Bioresour. Technol. 2011, 102, 2595–2604.
  44. Mata, ; Magnusson, M.; Paul, N.A.; de Nys, R. The intensive land-based production of the green seaweeds Derbesia tenuissima and Ulva ohnoi: Biomass and bioproducts. J. Appl. Phycol. 2016, 28, 365–375.
  45. Chemodanov, ; Jinjikhashvily, G.; Habiby, O.; Liberzon, A.; Israel, A.; Yakhini, Z.; Golberg, A. Net primary productivity, biofuel production and CO2 emissions reduction potential of Ulva sp. (Chlorophyta) biomass in a coastal area of the Eastern Mediterranean. Energy Convers. Manag. 2018, 166, 772–779.
  46. Raikova, ; Le, C.D.; Beacham, T.A.; Jenkins, R.W.; Allen, M.J.; Chuck, C.J. Towards a marine biorefinery through the hydrothermal liquefaction of macroalgae native to the United Kingdom. Biomass Bioenergy 2017, 107, 244–253.
  47. Soliman, M.; Younis, S.A.; El-Gendy, N.S.; Mostafa, S.S.M.; El-Temtamy, S.A.; Hashim, A.I. Batch bioethanol production via the biological and chemical saccharification of some Egyptian marine macroalgae. J. Appl. Microbiol. 2018, 125, 422–440.
  48. Saqib, ; Tabbssum, M.R.; Rashid, U.; Ibrahim, M.; Gill, S.S.; Mehmood, M.A. Marine macroalgae Ulva: A potential feed-stock for bioethanol and biogas production. Asian J. Agric. Biol. 2013, 3, 155–163.
  49. Suganya, ; Renganathan, S. Optimization and kinetic studies on algal oil extraction from marine macroalgae Ulva lactuca. Bioresour. Technol. 2012, 107, 319–326.
  50. Tabassum, R.; Xia, A.; Murphy, J.D. Potential of seaweed as a feedstock for renewable gaseous fuel production in Ireland. Renew. Sustain. Energy Rev. 2017, 68, 136–146.
  51. Jiang, ; Ingle, K.N.; Golberg, A. Macroalgae (seaweed) for liquid transportation biofuel production: What is next? Algal Res. 2016, 14, 48–57.
  52. El Harchi, ; Fakihi Kachkach, F.Z.; El Mtili, N. Optimization of thermal acid hydrolysis for bioethanol production from Ulva rigida with yeast Pachysolen tannophilus. S. Afr. J. Bot. 2018, 115, 161–169.
  53. Van der Wal, ; Sperber, B.L.; Houweling-Tan, B.; Bakker, R.R.; Brandenburg, W.; López-Contreras, A.M. Production of acetone, butanol, and ethanol from biomass of the green seaweed Ulva lactuca. Bioresour. Technol. 2013, 128, 431–437.
  54. Karray, ; Hamza, M.; Sayadi, S. Evaluation of ultrasonic, acid, thermo-alkaline and enzymatic pre-treatment on anaerobic digestion of Ulva rigida for biogas production. Bioresour. Technol. 2015, 187, 205–213.
  55. Koçer, T.; Özçimen, D. Investigation of the biogas production potential from algal wastes. Waste Manag. Res. 2018, 36, 1100–1105.
  56. Ganesh Saratale, ; Kumar, G.;Banu, R.; Xia, A.; Periyasamy, S.; Dattatraya Saratale, G. A critical review on anaerobic digestion of microalgae and macroalgae and co-digestion of biomass for enhanced methane generation. Bioresour. Technol. 2018, 262, 319–332.
  57. Park, -I.; Lee, J.; Sim, S.J.; Lee, J.-H. Production of hydrogen from marine macro-algae biomass using anaerobic sewage sludge microflora. Biotechnol. Bioprocess Eng. 2009, 14, 307–315.
  58. Wijffels, H.; Barbosa, M.J.; Eppink, M.H.M. Microalgae for the production of bulk chemicals and biofuels. Biofuels Bioprod. Biorefin. 2010, 4, 287–295.
  59. Mhatre, ; Gore, S.; Mhatre, A.; Trivedi, N.; Sharma, M.; Pandit, R.; Anil, A.; Lali, A. Effect of multiple product extractions on bio-methane potential of marine macrophytic green alga Ulva lactuca. Renew. Energy 2018, 132, 742–751.
  60. Wijesekara, ; Lang, M.; Marty, C.; Gemin, M.-P.; Boulho, R.; Douzenel, P.; Wickramasinghe, I.; Bedoux, G.; Bourgougnon, N. Different extraction procedures and analysis of protein from Ulva sp. in Brittany. J. Appl. Phycol. 2017, 29, 2503–2511.
  61. Yaich, ; Amira, A.B.; Abbes, F.; Bouaziz, M.; Besbes, S.; Richel, A.; Blecker, C.; Attia, H.; Garna, H. Effect of extraction procedures on structural, thermal and antioxidant properties of Ulvan from Ulva lactuca collected in Monastir coast. Int. J. Biol. Macromol. 2017, 105, 1430–1439.
  62. Tran, T.V.; Truong, H.B.; Tran, N.H.V.; Quach, T.M.T.; Nguyen, T.N.; Bui, M.L.; Yuguchi, Y.; Thanh, T.T.T. Structure, conformation in aqueous solution and antimicrobial activity of Ulvan extracted from green seaweed Ulva reticulata. Nat. Prod. Res. 2018, 32, 2291–2296.
  63. Hernández-Garibay, ; Zertuche-González, J.A.; Pacheco-Ruíz, I. Isolation and chemical characterization of algal polysaccharides from the green seaweed Ulva clathrata (Roth) C. Agardh. J. Appl. Phycol. 2011, 23, 537–542.
  64. Yuan, ; Xu, X.; Jing, C.; Zou, P.; Zhang, C.; Li, Y. Microwave assisted hydrothermal extraction of polysaccharides from Ulva prolifera: Functional properties and bioactivities. Carbohydr. Polym. 2018, 181, 902–910.
  65. Kanno, ; Fujita, Y.; Honda, S.; Takahashi, S.; Kato, S. Urethane foam of sulfated polysaccharide Ulvan derived from green-tide-forming chlorophyta: Synthesis and application in the removal of heavy metal ions from aqueous solutions. Polym. J. 2014, 46, 813–818.
  66. Kajiwara, ; Matsui, K.; Akakabe, Y.; Murakawa, T.; Arai, C. Antimicrobial browning-inhibitory effect of flavor compounds in seaweeds. J. Appl. Phycol. 2006, 18, 413–422.
  67. De Lima, L.; Pires-Cavalcante, K.M.S.; de Alencar, D.B.; Viana, F.A.; Sampaio, A.H.; Saker-Sampaio, S. In vitro evaluation of antioxidant activity of methanolic extracts obtained from seaweeds endemic to the coast of Ceará, Brazil. Acta Sci. Technol. 2016, 38, 247–255.
  68. Kellogg, ; Lila, M.A. Chemical and in vitro assessment of Alaskan coastal vegetation antioxidant capacity. J. Agric. Food Chem. 2013, 61, 11025–11032.
  69. Raja, ; Hemaiswarya, S.; Arunkumar, K.; Carvalho, I.S. Antioxidant activity and lipid profile of three seaweeds of Faro, Portugal. Rev. Bras. Bot. 2016, 39, 9–17.
  70. Cho, ; Kang, I.-J.; Won, M.-H.; Lee, H.-S.; You, S. The antioxidant properties of ethanol extracts and their solvent-partitioned fractions from various green seaweeds. J. Med. Food 2010, 13, 1232–1239.
  71. Goh, S.; Lee, K.T. A visionary and conceptual macroalgae-based third-generation bioethanol (TGB) biorefinery in Sabah, Malaysia as an underlay for renewable and sustainable development. Renew. Sustain. Energy Rev. 2010, 14, 842–848.
  72. Golberg, ; Vitkin, E.; Linshiz, G.; Khan, S.A.; Hillson, N.J.; Yakhini, Z.; Yarmush, M.L. Proposed design of distributed macroalgal biorefineries: Thermodynamics, bioconversion technology, and sustainability implications for developing economies. Biofuels Bioprod. Biorefin. 2014, 8, 67–82.
  73. Robin, ; Chavel, P.; Chemodanov, A.; Israel, A.; Golberg, A. Diversity of monosaccharides in marine macroalgae from the Eastern Mediterranean Sea. Algal Res. 2017, 28, 118–127.
  74. Pezoa-Conte, ; Leyton, A.; Baccini, A.; Ravanal, M.C.; Mäki-Arvela, P.; Grénman, H.; Xu, C.; Willför, S.; Lienqueo, M.E.; Mikkola, J.-P. Aqueous extraction of the sulfated polysaccharide Ulvan from the green alga Ulva rigida-Kinetics and modeling. Bioenergy Res. 2017, 10, 915–928.
  75. Chiesa, ; Gnansounou, E. Protein extraction from biomass in a bioethanol refinery—Possible dietary applications: Use as animal feed and potential extension to human consumption. Bioresour. Technol. 2011, 102, 427–436.
  76. Ge, ; Ni, Q.; Chen, Z.; Li, J.; Zhao, F. Effects of short period feeding polysaccharides from marine macroalga, Ulva prolifera on growth and resistance of Litopenaeus vannamei against Vibrio parahaemolyticus infection. J. Appl. Phycol. 2018, 10, 1663–1669.
  77. Bikker, ; van Krimpen, M.M.; van Wikselaar, P.; Houweling-Tan, B.; Scaccia, N.; van Hal, J.W.; Huijgen, W.J.J.; Cone, J.W.; López-Contreras, A.M. Biorefinery of the green seaweed Ulva lactuca to produce animal feed, chemicals and biofuels. J. Appl. Phycol. 2016, 28, 3511–3525.
  78. Gajaria, K.; Suthar, P.; Baghel, R.S.; Balar, N.B.;Sharnagat, P.; Mantri, V.A.; Reddy, C.R.K. Integration of protein extraction with a stream of byproducts from marine macroalgae: A model forms the basis for marine bioeconomy. Bioresour. Technol. 2017, 243, 867–873.
  79. Magnusson, ; Carl, C.; Mata, L.; de Nys, R.; Paul, N.A. Seaweed salt from Ulva: A novel first step in a cascading biorefinery model. Algal Res. 2016, 16, 308–316.
  80. Schiener, ; Atack, T.; Wareing, R.A.; Kelly, M.S.; Hughes, A.D. The by-products from marine biofuels as a feed source for the aquaculture industry: A novel example of the biorefinery approach. Biomass Convers. Biorefin. 2016, 6, 281–287.
  81. Raikova, ; Olsson, J.; Mayers, J.J.; Nylund, G.M.; Albers, E.; Chuck, C.J. Effect of geographical location on the variation in products formed from the hydrothermal liquefaction of Ulva intestinalis. Energy Fuels 2018, 10, 1021–1028.
  82. Díaz-Reinoso, ; González-Muñoz, M.J.; Domínguez, H. Introduction. In Water Extraction of Bioactive Compounds; Domínguez, H., González-Muñoz, M.J., Eds.; Elsevier: Kidlington, UK, 2017.
  83. Harrysson, ; Hayes, M.; Eimer, F.; Carlsson, N.-G.; Toth, G.B.; Undeland, I. Production of protein extracts from Swedish red, green, and brown seaweeds, Porphyra umbilicalis Kützing, Ulva lactuca Linnaeus, and Saccharina latissima (Linnaeus) J. V. Lamouroux using three different methods. J. Appl. Phycol. 2018, 10, 1–16.
  84. Boisvert, ; Beaulieu, L.; Bonnet, C.; Pelletier, E. Assessment of the antioxidant and antibacterial activities of three species of edible seaweeds. J. Food Biochem. 2015, 39, 377–387.
  85. Singh, ; Bhaskar, T.; Balagurumurthy, B. Effect of solvent on the hydrothermal liquefaction of macroalgae Ulva fasciata. Process Saf. Environ. Prot. 2015, 93, 154–160.