Geographic Variation in Biochemical and Physiological Traits of the Red Seaweeds Chondracanthus Chamissoi and Gelidium Lingulatum from the South East Pacific Coast
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Journal of Applied Phycology https://doi.org/10.1007/s10811-018-1532-0 Geographic variation in biochemical and physiological traits of the red seaweeds Chondracanthus chamissoi and Gelidium lingulatum from the south east Pacific coast Karina Véliz1,2,3 & Nancy Chandía 2,3 & Ulf Karsten4 & Carlos Lara 5 & Martin Thiel3,6,7 Received: 16 November 2017 /Revised and accepted: 28 May 2018 # Springer Science+Business Media B.V., part of Springer Nature 2018 Abstract Diverse phenotypic characteristics have evolved in seaweeds to cope with environmental stress, but these traits can vary among populations of the same species especially if these are distributed along environmental gradients. In this study, natural populations of the carrageenophyte Chondracanthus chamissoi and the agarophyte Gelidium lingulatum from a latitudinal gradient along the Chilean coast (between 20° S and 41° S) were compared. We determined physiological and biochemical traits in field and culture samples. Sulfated polysaccharide contents ranged from 15.4 to 52.7% dry weight (DW) in C. chamissoi and from 10.9 to 25.1% DW in G. lingulatum. Carrageenan amounts were higher in gametophytes than tetrasporophytes and were also, depending on life cycle phase, negatively correlated with the geographic variation of temperature, photosynthetically active radiation (PAR), and chlorophyll a (Chl a), whereas agar showed no significant correlation with these variables. The UV-absorbing mycosporine-like amino acids (MAAs) shinorine and palythine in both species ranged from 0.8 to 6.8 mg g−1 DW and these contents were positively correlated to PAR and Chl a levels at the sampling site. In C. chamissoi variation among populations in their photosynthetic characteristics, pigment concentrations, antioxidant capacity, and MAA contents were persistent after acclimation under common-garden conditions, suggesting ecotypic differentiation in this species. Contrary, G. lingulatum seems to have a more generalist strategy because differences after cultivation were observed only in some photosynthetic parameters and phycobiliprotein concentration. This study confirms that intraspecific differences in phenotypic traits along the same geographic area are strongly dependent on species and life cycle phases. Keywords Rhodophyta . Carrageenans . Agar . Mycosporine-like amino acids . Ecotypes . Chile Introduction * Karina Véliz [email protected] The biosynthesis of chemical compounds in benthic sea- weeds, as in other sessile organisms, is an important adaptive 1 Doctorado en Biología y Ecología Aplicada, Universidad Católica strategy to deal with environmental variability. Among those, del Norte, Coquimbo, Chile sulfated cell wall polysaccharides (carrageenans and agar) and 2 Laboratorio de Moléculas Bioactivas, Universidad Católica del UV-absorbing mycosporine-like amino acids (MAAs) are two Norte, Coquimbo, Chile different classes of important compounds biosynthesized by 3 Departamento de Biología Marina, Facultad de Ciencias del Mar, red seaweeds, which are involved in primary and secondary Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile metabolic functions, respectively (Carreto and Carignan 2011; 4 Institute of Biological Sciences, Applied Ecology and Phycology, Ficko-Blean et al. 2015; Lee et al. 2017a). University of Rostock, Albert-Einstein-Strasse 3, 18057 Rostock, Germany Carrageenans and agar mainly perform a structural func- tion as cell wall components. Both polysaccharides are com- 5 Centro de Investigación en Recursos Naturales y Sustentabilidad (CIRENYS), Universidad Bernardo O’Higgins, Av. Viel 1497, posed of a linear backbone of galactose residues linked by Santiago, Chile alternating β-1,3 and α-1,4 glycosidic bonds, being the 4- α 6 Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Av. linked -galactose residues of the D-series in carrageenans Ossandon 877, Coquimbo, Chile and of the L-series in agar. However, this regular structure 7 Millennium Nucleus Ecology and Sustainable Management of becomes complex by the substitution of hydroxyl groups with Oceanic Island (ESMOI), Coquimbo, Chile sulfate, and by the presence of the α-1,4-(3,6)- JApplPhycol anhydrogalactose (3,6-AG) moiety in the galactan chain of carbohydrates and nitrogenous compounds is differently (Lahaye 2001; van de Velde 2008). The chemical variation regulated by nutrient availability (Macler 1986; Bird 1988; in carrageenans and agar determines differences in their gel- Collén et al. 2004), an inverse trend between the contents of like physicochemical properties. Consequently, their addition- sulfated polysaccharides and MAAs could be expected ac- al functions, which include the provision of flexibility against cording to nutrient concentration in the natural habitats of hydrodynamic stress (Carrington et al. 2001), resistance to seaweeds. algal endophyte attack (Bouarab et al. 1999), and cellular ion- The quantity and quality of seaweed compounds can also ic regulation by selective cationic exchange (Mariani et al. vary among populations of the same species depending on 1990), can also be modified. geographical variation of selective factors. Genetic or ecotypic The MAAs are a family of intracellular nitrogenous metab- differentiation, as result of divergent selection, is more prob- olites that function as photoprotective sunscreens (Karsten able in species distributed along environmental gradients and 2008; Bischof and Steinhoff 2012). Different types of with a low genetic connectivity (Sanford and Kelly 2011). MAAs vary in the nitrogen substituent bound to their Although some studies have examined the variation in the cyclohexenone or cyclohexenimine chromophore, which in- production of carrageenans and agar regarding the site of sea- fluences the maximum of UVabsorption in the range of 310 to weed origin (e.g., Hurtado et al. 2011; Pereira and van de 360 nm, as well as their antioxidant capacity (Carreto and Velde 2011; Tasende et al. 2012, 2013), no consistent geo- Carignan 2011). Currently, in marine organisms, there are graphic patterns have been identified to date, maybe due to about 23 MAAs identified, being shinorine, palythine, the restricted spatial scale used which does not include the asterina-330, mycosporine-glycine, palythinol, and entire species geographic range. In the case of MAAs, their porphyra-334 the most commonly reported MAAs from red intraspecific variation has been mainly analyzed considering seaweeds (Karsten et al. 1998a, b). coastal bathymetric gradients, reporting an inverse relation- The biosynthesis of carrageenans, agar, and MAAs is af- ship between MAA contents and depth of seaweed collection fected by several factors acting at different levels. In the first (Karsten and Wiencke 1999; Hoyer et al. 2001, 2002; place, the type of cell wall polysaccharide is determined by Huovinen et al. 2004). phylogenetic relationships among species, as well as by the The coast of Chile (18° S to 56° S) is located along the life cycle phase in the specific case of carrageenans (Craigie South Eastern (SE) Pacific temperate coast. It is characterized 1990;Chopinetal.1999). MAA composition also appears to by a latitudinal gradients of sea surface temperature (SST) be genetically defined according to studies carried out in sea- (Ramos-Rodriguez et al. 2012) and solar radiation (Vernet et weeds (Hoyer et al. 2002; Karsten 2008). Based on the total al. 2009), but also by mesoscale variation (10’sto100’sof MAA amounts and the induction patterns after exposure to km) in oceanographic and atmospheric nearshore conditions different radiation conditions, red algae can be classified in related to coastal upwelling (Hernández et al. 2012; Tapia et three groups: type I—unable to biosynthesize MAAs, type al. 2014). There is little information about the adaptive phys- II—MAAs inducible in variable concentrations, and type iological and biochemical mechanisms of seaweed species III—permanently high MAA contents. While type I typically inhabiting latitudinal gradients along this coast. This contrasts represents deep-water seaweeds, types II and III species grow with the high commercial and social importance of seaweeds from the upper and mid sublittoral zone up to the supra- and in Chile, which is the main producer of red seaweeds in South eulittoral zone (Hoyer et al. 2002). America for the phycocolloid industry (Hayashi et al. 2014). The content and composition of carrageenans and agar are Among the most important commercial species, also determined by the interaction of several environmental Chondracanthus chamissoi isasourceofcarrageenans factors such as light, temperature, nutrient supply, salinity, and (Wang et al. 2012; Véliz et al. 2017), whereas Gelidium water movement. These factors can influence the availability lingulatum produces agar (Matsuhiro and Urzúa 1991). and allocation of necessary resources for carbohydrate biosyn- Since both species have a wide geographic range along the thesis due to their effects on photosynthesis (Macler 1986, SE Pacific coast where their populations are exposed to con- 1988;Bird1988; Fournet et al. 1999; Goulard et al. 2001), trasting environmental conditions, there is a high probability or they can alter the physiological conditions of seaweeds that intraspecific differences in their physiological and/or bio- depending on the species’ tolerance to limitation or disruptive chemical traits could have evolved as response to local habitat stress (Collén et al. 2004; Lee et al. 2017b; Navarro et al. conditions. 2017). In the case of MAAs, it is well