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Mastocarpus Stellatus and Chondrus Crispus Kristina Koch1*, Wilhelm Hagen2, Martin Graeve3 and Kai Bischof1

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Mastocarpus Stellatus and Chondrus Crispus Kristina Koch1*, Wilhelm Hagen2, Martin Graeve3 and Kai Bischof1 Koch et al. Helgol Mar Res (2017) 71:15 DOI 10.1186/s10152-017-0495-x Helgoland Marine Research ORIGINAL ARTICLE Open Access Fatty acid compositions associated with high‑light tolerance in the intertidal rhodophytes Mastocarpus stellatus and Chondrus crispus Kristina Koch1*, Wilhelm Hagen2, Martin Graeve3 and Kai Bischof1 Abstract The rhodophytes Mastocarpus stellatus and Chondrus crispus occupy the lower intertidal zone of rocky shores along North Atlantic coastlines, with C. crispus generally occurring slightly deeper. Consequently, M. stellatus is exposed to more variable environmental conditions, related to a generally higher stress tolerance of this species. In order to extend our understanding of seasonal modulation of stress tolerance, we subjected local populations of M. stellatus and C. crispus from Helgoland, North Sea, to short-term high-light stress experiments over the course of a year (Octo- ber 2011, March, May and August 2012). Biochemical analyses (pigments, antioxidants, total lipids, fatty acid com- positions) allowed to reveal mechanisms behind modulated high-light tolerances. Overall, C. crispus was particularly more susceptible to high-light at higher water temperatures (October 2011 and August 2012). Furthermore, species- specifc diferences in antioxidants, total lipid levels and the shorter-chain/longer-chain fatty acid ratio (C14 C16/ C18 C20) were detected, which may enhance the tolerance to high-light and other abiotic stress factors in+ M. stel- latus+, so that this species is more competitive in the highly variable upper intertidal zone compared to C. crispus. Since the high-light tolerance in C. crispus seemed to be afected by water temperature, interactions between both species may be impacted in the future by rising mean annual sea surface temperature around the island of Helgoland. Keywords: Antioxidants, Chondrus crispus, Helgoland, High-light stress, Fatty acid composition, Macroalgae, Mastocarpus stellatus Introduction economic importance, providing food and habitat to Mastocarpus stellatus ((Stackhouse) Guiry, 1984; Phyl- associated invertebrates [3, 5] and representing a source lophoraceae, Gigartinales, Rhodophyta) and Chondrus of carrageenan, which is used in food, cosmetic and crispus (Stackhouse, 1797; Gigartinaceae, Gigartina- pharmaceutical industries [6]. Additionally, the species les, Rhodophyta) are morphologically similar red mac- are of commercial interest due to their high content of roalgal species, both approximately 10 cm in size with polyunsaturated fatty acids with 20 carbon atoms such as numerous dichotomously branching blades arising from 20:4(n-6) (arachidonic acid) and 20:5(n-3) (eicosapentae- a fattened stipe [1–3]. In the lower intertidal zone of noic acid) [7]. Arachidonic acid has medical signifcance rocky shorelines along North Atlantic coastlines [4], M. as precursor of prostaglandins, whereas eicosapentaenoic stellatus and C. crispus are of signifcant ecological and acid is an essential constituent in the feed of several mari- culture species and this omega-3 fatty acid is suggested to reduce the risk of thrombosis, atherosclerosis and heart *Correspondence: [email protected] disease in humans [8, 9]. 1 Marine Botany, Bremen Marine Ecology ‑ Center for Research As inhabitants of the intertidal zone, M. stellatus and and Education (BreMarE), University of Bremen, Leobener Str. NW2, 28359 Bremen, Germany C. crispus alternate between periods of immersion in sea- Full list of author information is available at the end of the article water and exposure to air, where they experience several © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Koch et al. Helgol Mar Res (2017) 71:15 Page 2 of 16 potentially stressful environmental conditions such as membrane protein complexes, light-induced variations intense photosynthetically active and ultraviolet radiation in the photosynthetic performance might likely be mir- (PAR and UV), high or low temperatures (e.g. changes rored in the thylakoid membrane fatty acid composition of 10 to 20 °C compared to seawater temperature in the [e.g. 23]. Tereby, adjustments of fatty acid profles can Gulf of Maine, USA) [10], desiccation, osmotic stress and facilitate electron and ion transport across/within the thy- nutrient limitation [11]. To prevail in their particularly lakoid membranes [27] and enhance the stabilizing efect challenging, dynamic environment, intertidal macroal- of lipids on the protein complexes during photosynthesis gae have generally developed efective ecophysiological under variable light conditions [28, 29]. acclimation mechanisms [e.g. 11]. Such mechanisms may Te frequency and duration of submersed periods include a high scavenging capacity for reactive oxygen during high tide and emersed periods during low tide species (ROS) [12, 13] and UV-screening substances, e.g. depends on the vertical position of an alga on the shore. mycosporine-like amino acids (MAA), commonly found Species found higher on the coast are generally thought in red algae [14, 15]. Furthermore, the algae have to adjust to be less susceptible to environmental stress than those their thylakoid membrane fuidity to the prevailing envi- inhabiting lower levels [12, 30, 31]. M. stellatus and C. ronmental conditions in order to maintain the integrity crispus occupy diferent levels within the lower inter- of these membranes, and thus, a proper operation of the tidal, with C. crispus generally occurring slightly deeper photosynthetic machinery in a highly variable environ- [4]. Along the south-western coast of the island of Hel- ment. Photosystem II is embedded in the thylakoid mem- goland in the North Sea, for example, the highest part brane, so that the rate of the D1 reaction center protein of the lower intertidal is dominated by an almost mono- repair cycle, especially the re-integration of de-novo syn- specifc zone of M. stellatus, whereas in the deeper part thesized proteins via lateral difusion through the mem- the two macroalgal species co-occur as mixed assem- brane, depends strongly on membrane fuidity [16] and blages [32]. Consequently, M. stellatus is considered as references therein]. Besides this, optimal membrane fuid- being more tolerant with respect to the adverse efects ities under variable environmental conditions are needed of ultraviolet-B radiation [15], freezing [33, 34] and des- in order to stabilize membrane-associated proteins and to iccation [35] than C. crispus. Interestingly, M. stellatus maintain electron transport chains and transmembrane was not recorded on Helgoland before 1983, when the proton gradients [17]. Membrane fuidity is mainly deter- species was accidentally introduced to the island during mined by the chain length of fatty acids and their satura- scientifc feld experiments [3]. Afterwards, M. stellatus tion state. It is generally accepted that at low temperatures, established and massively dispersed over the island, with biological membranes feature higher amounts of shorter- drastic alterations of the native communities [36]. Difer- chain and unsaturated fatty acids with lower melting ences in stress tolerances appear to be advantageous for points, which compensate for low temperature-induced M. stellatus over C. crispus in terms of competition and decreases in membrane fuidity. At high temperatures, colonization of new habitats [15, 33–35]. vice versa, more longer-chain and saturated fatty acids Te object of the present study was to extend our under- with higher melting points are incorporated into biomem- standing of stress tolerance in the local populations of M. branes. Tese fatty acids increase rigidity and, thus, may stellatus and C. crispus from Helgoland. As light exposure prevent membrane leakage at elevated temperatures is a major factor controlling vertical distribution of algae [18]. Some previous studies have already demonstrated on the shore, we selected high-light as abiotic variable in that changes in temperature can lead to modifcations of stress experiments. Our study should be considered as a macroalgal fatty acid profles [e.g. 19–22]. Becker et al. rather general approach, since we refer to the overall light [16] reported, for example, that the Antarctic red alga stress (frequency and duration), which the algae experi- Palmaria decipiens acclimated to diferent tempera- ence during the submersed periods at high tide as well as ture regimes by adjusting the degree of fatty acid satura- during the emersed periods at low tide. More specifcally, tion. In addition, variations in light conditions were also we tackled the question, whether diferences in high-light shown to afect the membrane fatty acid composition of tolerance are species-specifc or rather habitat-specifc, macroalgae, but they did not reveal consistent responses with habitat being defned as vertical position on the [e.g. 23–26]. Since marine macroalgae are poikilother- shore. Further, we checked for the possible ecophysiologi- mic organisms, the sensitivity of membrane fuidity and cal mechanisms behind diferent high-light tolerances. the change in fatty acid composition in response to tem- Besides measurements of pigment concentrations and perature is plausible, but fuctuation
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