Exploring Ulva australis Areschoug for possible biotechnological applications: In vitro antioxidant and enzymatic inhibitory properties, and fatty acids contents
Introduction
Ulva australis Areschoug (Ulvales, Chlorophyta) is a green macroalgae from the Ulvaceae family and is widely distributed along the coasts of the Yellow Sea and the Bo Sea of China [1]. This species, previously known as Ulva pertusa Kjellman, is often misidentified as U. rigida [2] due to its cryptic morphology [3].
Ulva australis is edible and traditionally consumed in the Mediterranean area and in Korea [4], and has an interesting nutritional profile in terms of minerals, vitamins, and noncaloric dietary fibers [1]. This species has also a long history of use in Chinese traditional medicine, for example, in the form of decoctions for the treatment of hyperlipidemia, sunstroke, and urinary diseases [1]. Ulva australis exhibits algicidal effects [5,6] and contains bioactive metabolites, such as sulphated polysaccharides (ulvans) with diverse biological activities, including antioxidant, antihyperlipidemic, immuno-modulatory and anti-viral [[7], [8], [9], [10]]. Other bioactive components were also identified in U. australis, as for example asarone, phytol derivatives, uracil, guanosine, stearic acid, vanillin, several sterols and 3-hydroxy-4,7-megastigmadien-9-one [1,[11], [12], [13]].
Ulva australis tolerates a wide range of salinity, temperature and water quality, and grows rapidly in nutrient rich habitats [3]. These characteristics have rendered it the classification of invasive species [14] whose presence has been recorded in the North Adriatic Sea and in the Venice Lagoon (Italy) [3]. Invasive species are inflicting serious impacts on the ecosystem processes that are fundamental to human well-being leading to social and economic damages [15]. Particularly, lagoons are subject to accidental and voluntary introductions of new species with a broad range of possible negative effects, from cell to community level [16]. Invasive species compete with the native ones leading to their displacement and promote biodiversity loss, thus impoverishing local genetic variability [17]. Although it is recognized that invasive seaweeds are serious threats to the ecosystem's equilibrium, few attempts to control their spread have proven to be efficient [17]. Hand removal of invasive seaweeds is extremely expensive and time-consuming and the use of toxic chemicals to remove them can harshly affect all surrounding species [18]. Therefore, harvesting these seaweeds for commercial purposes can be an efficient cost-effective alternative to control, or at least mitigate, their damaging effects [17,19]. The economic exploitation of alien invasive species could control their spread and satisfy different human needs. The concept of “eradication by utilization” [20] has already been applied, for example, to different plant species, such as Typha australis Schum. and Thonn. and Nypha fruticans in many countries such as Nigeria, India and Sudan [21], and could be a strategy to be applied in the North Adriatic Sea and in the Venice Lagoon for the management of U. australis, moving from inefficient control methods to a socio-economic utilization.
Algae are economically valuable resources and have been suggested as potential sources of bioactive compounds (e.g. sulphated polysaccharides and sterols) to be used as food, fodder, fertilizers, and medicines [22]. The seaweed industry is estimated to have an annual value of US$6 billion, the largest share (US$5 billion) corresponding to human food products [23]. The remaining US$1 billion is largely based on seaweed extracts, such as hydrocolloids for use in animal feeds, fertilizers and bioactive compounds [23]. Seaweed derived compounds, such as phenolics, polyunsaturated fatty acids, polysaccharides, pigments and proteins, have recently gained an increasing commercial interest due to their interesting bioactive potential [17].
An integral biomass valorisation could represent a viable approach for the sustainable use of U. australis, offering alternatives to global environmental concerns. In this sense, two aspects favour the use of biomass from this species: the presence of commercially valuable components and its high productivity [19]. In this context, and aiming to increase knowledge on the possible biotechnological uses of U. australis, this work explored this species as a potential source of bioactive products with multiple applications. For that purpose, biomass was collected in the Chioggia inlet area (Lagoon of Venice, Italy) and evaluated for fatty acids methyl esters profile (FAME) by gas chromatography–mass spectrometry (GC–MS). Infusions, decoctions, tinctures and dichloromethane extracts were then prepared from the dried biomass and its chemical profile was established by spectrophotometric methods, in terms of total contents of phenolics (TPC), flavonoids (TFC) condensed tannins (CTC) and carbohydrates (TCC). Extracts were further evaluated for in vitro antioxidant activity by different radical and metal-based assays, and for inhibition of enzymes related to neurological disorders (acetylcholinesterase: AChE, butyrylcholinesterase: BuChE), skin hyperpigmentation (tyrosinase), obesity (lipase), diabetes (α-glucosidase and α-amylase) and skin ageing (elastase).
Section snippets
Chemicals
The compounds 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), fatty acid methyl ester (FAME) standards (Supelco® 37 Component FAME Mix), AChE (EC.3.1.1.7) from electrical eel, BuChE (EC 3.1.1.8) from horse serum, acetylthiocholine iodide, butyrylthiocholine iodide, lipase (EC 3.1.1.3), elastase (EC 3.4.21.36), tyrosinase (EC 1.14.18.1), glucosidase (EC 3.2.1.20), from Saccharomyces cerevisiae, amylase (EC 3.2.1.1 (from porcine pancreas),
Molecular analysis
To establish the taxonomical status of the seaweed thalli collected from the Chioggia inlet area (Lagoon of Venice) a molecular analysis was performed, using the elongation factor Tu (tufA) gene. The comparison of the tufA gene sequences of collected thalli with other sequences available in GenBank, showed the highest percentage identity (100%) with sequences of Ulva australis Areschoug (syn. Ulva pertusa Kjellmann) from different vouchers collected from Mallacoota (Victoria, Australia)
Discussion
In this work the invasive species U. australis was collected from the Venice Lagoon (Italy) and explored as a potential source of products with biotechnological applications. Aiming that, extracts were prepared from dried biomass and evaluated for in vitro antioxidant properties, inhibitory capability towards enzymes implicated on the onset of relevant human diseases, and for chemical composition in terms of total phenolics, flavonoids, tannins and polysaccharides. Biomass was also appraised
CRediT authorship contribution statement
Riccardo Trentin:Writing - original draft, Investigation, Formal analysis.Luísa Custódio:Writing - original draft, Funding acquisition, Project administration, Supervision, Investigation.Maria João Rodrigues:Writing - review & editing, Investigation.Emanuela Moschin:Writing - review & editing, Investigation.Katia Sciuto:Writing - review & editing, Investigation.José Paulo da Silva:Investigation.Isabella Moro:Writing - original draft, Project administration, Supervision.
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.
Acknowledgments
Work supported by the Foundation for Science and Technology (FCT) and the Portuguese National Budget, through CCMAR/Multi/04326/2019 and GreenVet [ALG-01-0145-FEDER-028876] projects. Maria Joao Rodrigues acknowledge FCT for the PhD grant [SFRH/BD/116604/2016]. Luísa Custódio was supported by the FCT Scientific Employment Stimulus [CEECIND/00425/201].
Statement of informed consent
No conflicts, informed consent, or human or animal rights are applicable to this study.
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