Journal of Marine Science and Engineering Review Ecological Function of Phenolic Compounds from Mediterranean Fucoid Algae and Seagrasses: An Overview on the Genus Cystoseira sensu lato and Posidonia oceanica (L.) Delile Anna Maria Mannino 1,* and Carla Micheli 2 1 Department of Biological, Chemical and Pharmaceutical Sciences and Technologies, University of Palermo, 90123 Palermo, Italy 2 Department of Energy Technologies, Laboratory of Biomass and Biotechnologies for Energy, ENEA Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Research Centre Casaccia, PO Box 2400, 00123 Rome, Italy; [email protected] * Correspondence: [email protected]; Tel.: +39-091-23891218 Received: 30 November 2019; Accepted: 31 December 2019; Published: 1 January 2020 Abstract: Biodiversity is undergoing rapid and worrying changes, partially driven by anthropogenic activities. Human impacts and climate change (e.g., increasing temperature and ocean acidification), which act at different spatial scales, represent the most serious threats to biodiversity and ecosystem structure and function. In the Mediterranean Sea, complex systems such as fucoid algae and seagrasses, characterized by a high associated biodiversity, are regularly exposed to natural and anthropogenic pressures. These systems, particularly sensitive to a variety of stressors, evolved several physiological and biochemical traits as a response to the different pressures which they are subjected to. For instance, they produce a huge quantity of secondary metabolites such as phenolic compounds, to adapt to different environmental stressors and to defend themselves from biological pressures. These natural products are receiving increasing attention due to their possible applications in a wide range of industrial sectors. In this paper we provide an overview on the ecological role of phenolic compounds from the genus Cystoseira sensu lato and Posidonia oceanica (L.) Delile, also highlighting their potential use as ecological biomarkers. Keywords: phenolic compounds; ecological role; Cystoseira sensu lato; Posidonia oceanica; biomarkers; Mediterranean Sea 1. Introduction Marine algae and seagrasses produce secondary metabolites to adapt and acclimate to environmental stressors, but also to defend themselves from biological pressures such as competitors, pathogens, grazers and epiphytes [1–7]. The production of these metabolites is known to vary with environmental conditions (e.g., light, nutrient, and temperature), but also with geographical distribution and biological status (e.g., life cycle) [8–11]. Among secondary metabolites, phenolic compounds, carbon-based metabolites ranging from simple molecules, such as free and ester-bound phenolic acid, to more complex polymers such as condensed tannins and lignins, are commonly produced by algae and seagrasses for structural, protective and ecological purposes [4–6,12–17]. For instance, algae and plants living in saltworks produce and accumulate polyphenols as defense strategies to cope with these extreme environmental conditions [18]. J. Mar. Sci. Eng. 2020, 8, 19; doi:10.3390/jmse8010019 www.mdpi.com/journal/jmse J. Mar. Sci. Eng. 2020, 8, 19 2 of 19 J. Mar. Sci.In theEng. Mediterranean2019, 7, x FOR PEER Sea, REVIEW which is a true hotspot of biodiversity [19–21], large, brown,2 fucoid of 19 algae of the genus Cystoseira sensu lato (Fucales, Phaeophyceae), according to Orellana et al. [22], seagrassesand seagrasses like Posidonialike Posidonia oceanica oceanica (L.) Delile(L.) Delile (Posidoniaceae, (Posidoniaceae, Alismatales) Alismatales) (Figure (Figure 1), supporting1), supporting high biodiversityhigh biodiversity and providing and providing essential essential ecological ecological goods goodsand services, and services, are valuable, are valuable, productive productive and uniqueand unique habitats habitats [19,21 [,2193,2421,]23. Since,24]. the Since Mediterranean the Mediterranean basin is basin also isone also of onethe ofmain the climate main climate (e.g., increases(e.g., increases of temperatures of temperatures and andCO2) CO change2) change “hot “hot-spots”-spots” [25] [ 25and] and impacted impacted sea, sea, these these valuable valuable communitiescommunities are are significantly significantly threatened threatened by by all all these these pressures pressures which which are are predicted predicted to to increase increase in in the the futurefuture [24,26 [24,26,27,27]].. FigureFigure 1. 1.Cystoseira Cystoseira sensu latu latu community community (A (A),), Posidonia Posidonia oceanica oceanica meadow meadow (B). (B ). FucoidFucoid algae algae and and seagrasses, seagrasses, partic particularlyularly sensitive sensitive to to a a variety variety of of stressors, stressors, evolved evolved several several physiologicalphysiological and and biochemical biochemical traits traits as asresponse response to the to thedifferent different pressures pressures they theyare subjected are subjected.. For instance,For instance, they theyproduce produce a huge a huge quantity quantity of phenolic of phenolic compounds compounds playing playing multiple multiple roles roles [17,28 [17,28–3–333].]. SinceSince these these compounds compounds also also have have several several biological biological properties, properties, they they are are receiving receiving increasing increasing attention attention duedue to to their their applications applications in in a awide wide range range of of pharma pharmaceuticalceutical (e.g. (e.g.,, anticancer, anticancer, antimicrobial, antimicrobial, antifungal antifungal oror anti anti-inflammatory),-inflammatory), medical medical and and industrial industrial sectors sectors [18, [183,344––3636].]. Tannins Tannins are are considered considered to to be be one one of of thethe mostmost broadlybroadly distributed distributed phenolic phenolic compound compound types, andtype amongs, and them, among phlorotannins them, phlorotannins (halogenated (halogenatedor sulphated or oligomers sulphated or oligomers polymers ofor phloroglucinol—1,3,5-trihydroxybenzene,polymers of phloroglucinol - 1,3,5-trihydroxybenzene Figure2A) constitute, Figure 2aA heterogeneous) constitute a heterogeneous group exclusively group present exclusively in brown present algae, suchin brown as fucoid algae algae,, such presenting as fucoid chemical algae, presentingstructures chemical not found structures in terrestrial not found plants in [terrestrial13,37–40]. plants Seagrasses [13,37– such40]. Se asagrassesP. oceanica suchare as alsoP. oceanica rich in arephenolic also rich compounds, in phenolic as compounds, testified by theas testified presence by of the “tannin presence cells” of [“tannin1,2,41–43 cells”]. [1,2,41–43]. SinceSince these systemssystems are are susceptible susceptible to humanto human pressures, pressures, their healththeir statushealth is status currently is consideredcurrently consideredas an indicator as an indicator of the environmental of the environ qualitymental quality of the of coastal the coastal zone. zone. Therefore, Therefore, understanding understanding the themechanisms mechanisms these these valuable valuable communities communities use use to respond to respond to di toff erentdifferent stressors stressors is crucial is crucial to predict to predict their theirresponses responses to future to future climate climate scenarios. scenarios. The aim The of aim this paperof this is paper to provide is to provide an overview an overview on the ecological on the ecologicalfunctions offunctions phenolic of compounds phenolic compounds from the fucoid from algae the fucoid of the genusalgae Cystoseiraof the genus sensu Cystoseira lato and seagrassessensu lato andlike seagrassesP. oceanica, likealso P. evaluating oceanica, also their evaluating potential usetheir as potential ecological use biomarkers. as ecological biomarkers. TheThe search search for for relevant relevant literature, literature, updated updated up up to to summer summer 2019, 2019, was was carried carried out out using using standard standard electronicelectronic databases databases (Google (Google Scholar, Scholar, Web Web of of Science, Science, Scopus Scopus and and Pub Pub Med). Med). The The research research crit criteriaeria werewere based based up uponon the the following following list list of of key keywords:words: “Fucales “Fucales”,”, “f “fucoiducoid algae”, algae”, “Cystoseira “Cystoseira”,”, “seagrasses”, “seagrasses”, ““PosidoniaPosidonia oceanica oceanica”,”, “ “phenol”,phenol”, “ “metabolites”,metabolites”, “tannin “tannin”,”, “ “function”,function”, “role”, “role”, “ecological”, “ecological”, “indicator”, “indicator”, “markers”,“markers”, “ “MediterraneanMediterranean Sea Sea”.”. 2. Genus Cystoseira sensu lato 2. Genus Cystoseira sensu lato In the Mediterranean Sea, fucoid algae are important canopy-forming algae on a rocky substrata In the Mediterranean Sea, fucoid algae are important canopy-forming algae on a rocky substrata from exposed to sheltered conditions and from the intertidal zone to more than 50 m depth [44–48]. from exposed to sheltered conditions and from the intertidal zone to more than 50 m depth [44–48]. Recently, Orellana et al. [22] revised the genus Cystoseira sensu lato and recognized three different genera: Cystoseira sensu stricto, Carpodesmia Greville, gen. emend., Treptacantha Kützing, gen. emend. These communities provide food, habitat and shelter for a large number of marine organisms, and are therefore considered biological “formers” of habitat