The Marine Macroalgae of the Genus Ulva: Chemistry, Biological Activities and Potential Applications

The genus Ulva (Phylum Chlorophyta, Class Ulvophyceae, Order Ulvales, Family Ulvaceae) was first identified by Linnaeus in 1753 [1]. Since then many taxonomists and phycologists have been involved in the identification of Ulva species [2] which are notoriously difficult to classify due to the morphological plasticity expressed by many members as well as the few reliable characters available for differentiating taxa [2,3]. Its morphology resembles bright green sheets [4], heavily influenced by environmental conditions, age of the thallus, and life style, making difficult the delineation of species by morphological features alone [2]. There is an important relationship between morphological features of Ulva and salinity and nutrient concentrations in these freshwater habitats; however, the most essential physical factor positively correlated with mats development was water depth [3,5].


Introduction
The genus Ulva (Phylum Chlorophyta, Class Ulvophyceae, Order Ulvales, Family Ulvaceae) was first identified by Linnaeus in 1753 [1]. Since then many taxonomists and phycologists have been involved in the identification of Ulva species [2] which are notoriously difficult to classify due to the morphological plasticity expressed by many members as well as the few reliable characters available for differentiating taxa [2,3]. Its morphology resembles bright green sheets [4], heavily influenced by environmental conditions, age of the thallus, and life style, making difficult the delineation of species by morphological features alone [2]. There is an important relationship between morphological features of Ulva and salinity and nutrient concentrations in these freshwater habitats; however, the most essential physical factor positively correlated with mats development was water depth [3,5].
At present, there are 562 species names in the Algaebase and 99 of which have been flagged as currently accepted taxonomically [6]. These organisms have a potential for rapid and proliferous growth [3] with a ubiquitous distribution with species living in a wide range of habitats and environments [2,3,5,7]. Although Ulva species are primarily marine taxa found in saline and salty waters, they can also proliferate in freshwater habitats [6].

Secondary Metabolites
Although the members of the phylum Chlorophyta are abundant and relatively easy to collect, their chemistry continues to be underrepresented [8]. Among all macroalgae, the green algae with less than 300 known compounds are the least producers of natural compounds when compared to the red (Rhodophyta) and brown algae (Phaeophyta) [9,10]. Anyhow, a wide range of compounds, predominantly terpenes, polyphenols and steroids, have been reported in various marine green algae [11,12]. The chemical composition of these macroalgae was found to vary depending on geographical distribution and seasons and the principal environmental factors affecting the composition being water temperature, salinity, light, nutrients and minerals availability [5].
Roussis et al. have investigated the production and release of volatile metabolites from U. rigida during light and darkness, under natural conditions and after the biological death of the plant [22]. Using GC and GC-MS methods to analyze the chemical constituents released from live U. rigida to the atmosphere, they have found that oxygenated metabolites, mainly aldehydes and alcohols, were the major components and aliphatic and aromatic hydrocarbons were present in significant amounts; however vestigial quantities of the halogenated and sulfated compounds were also detected. In order to determine the chemical load of the volatile compounds that would be liberated in the atmosphere at the end of the biological cycle, the volatile oil obtained from steam distillation of U. rigida was analyzed by GC-MS. The results showed that dimethyl sulfide, acetaldehyde and dichloromethane were the major compounds. Furthermore, dichloromethane was found to be a major metabolite during the light period [22].
Another class of secondary metabolites of green algae is sterols. Sterols from green algae have been reported to be non-toxic and capable of reducing blood cholesterol level and were found to be able to reduce the tendency to form a greasy liver and excessive fat deposition in the heart [60].
Finally, it is worth mentioning green algae as an important source of Polyunsaturated Fatty Acids (PUFAs). Due to nutritional values and beneficial effects of PUFAs, many researchers have investigated the suitability of using macroalgae as novel dietary sources of PUFAs. Pereira et al. have detected higher percentages (16%) of α-Linolenic Acid (ALA), in comparison to Linoleic Acid (LA), in Ulva sp., collected at the Algarve coast, Portugal [61]. Moreover, PUFAs can be considered also as having an important ecological role. Alamsjah et al. have found that Hexadeca-4, 7, 10, 13-Tetraenoic Acid (HDTA), Octadeca-6,9,12,15-Tetraenoic Acid (ODTA), and α-Linolenic Acid, isolated from the methanol extract of U. fasciata by bioassay-guided fractionation, exhibited a potent algicidal activity against the red-tide phytoplankton Heterosigma akashiwo (with LC 50 1.35 µg/ml, 0.83 µg/ml and 1.13 µg/ml, respectively) and this result demonstrated the potential of these PUFAs for practical harmful algal bloom control [62].

Use of Ulva spp. as Food
Although algae are known to contain a multitude of bioactive compounds, the interest in these organisms is also due to their nutritional proprieties [30,31,63]. Edible marine algae, sometimes referred as seaweeds, have attracted a special interest as good sources of nutrients [26] since they are an excellent source of vitamins, carbohydrates, dietary fiber and minerals [14,31,64,65] that could be potentially exploited as functional ingredient for both human and animal health [23,25]. Interestingly, many types of seaweeds used as traditional food in many cultures are known not only to cure various diseases but also to maintain health and were found to have immunomodulating and antitumor activities [36].  The green algae belonging to the genus Ulva are a group of edible algae that are widely distributed along the coasts of the world's oceans [7,63], and they have an interesting chemical composition that makes their commercial exploitation attractive to produce functional or health promoting food [7,66]. The macroalgae of the order Ulvales are already used in Asia as a food condiment and as a nutritional supplement in Japan, China and other Southeast Asian countries as well as in North and South America and Oceania. For instance, they are consumed as part of the traditional Hawaiian cuisine [67], in Japan, they are included in a variety of dishes such as salads, soups, cookies, meals and condiments as well as a mixed product with other green seaweeds [7,68]. Interestingly, the interest in these algae as a novelty food is expanding in the West [7], and especially in France where they were authorized for human consumption as vegetables [69].
In the recent years, ulvan has been investigated in order to develop functional foods [26] since they cannot be digested in the human gastrointestinal tract [45,47,67,70] and therefore may be regarded as a good source of dietary fiber and a potential source of prebiotics [67]. It is interesting to note that only few species of Ulva have been studied for their application in food industry. These include U. lactuca, U. pertusa, U. compressa and U. clathrata. These macroalgae exhibited a broad spectrum of nutritional composition which makes them excellent candidates for a healthy food for human nutrition [68]. With high levels of protein (between 10 and 25% of dry mass), dietary fiber, low total lipid contents, and relatively high levels of essential amino acids, they constitute a good alternative source of amino acids and of some essential polyunsaturated fatty acids such as Oleic, Linoleic and Linolenic Acids, vitamins and minerals, especially iron [38,59,68,71]. While U. lactuca is used in salads, cookies and soups [62,68], U. pertusa, which is frequently consumed under the name of "aonori" in Japan, has a high level of protein (between 20 and 26% dry product) [63], and abundant with vitamins, trace elements and dietary fibers but with low calorie [55]. The dried U. compressa is used in cooking, particularly with eggs. It is also used as an ingredient in the preparation of high fiber snack "Pakoda", a common Indian product made from chickpea flour. The crude protein levels of this alga are found to be ranging from 21 to 32% [63]. On the other hand, as U. clathrata is a good source of soluble dietary fiber, high-quality polyunsaturated fatty acids, carotenoids and some minerals, it can be a valuable source of protein and may be efficiently used as an ingredient in human and animal foods [7].