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Prasiolin, a New UV-Sunscreen Compound in the Terrestrial Green Macroalga Prasiola Calophylla (Carmichael Ex Greville) Kützing

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Prasiolin, a New UV-Sunscreen Compound in the Terrestrial Green Macroalga Prasiola Calophylla (Carmichael Ex Greville) Kützing Planta (2016) 243:161–169 DOI 10.1007/s00425-015-2396-z ORIGINAL ARTICLE Prasiolin, a new UV-sunscreen compound in the terrestrial green macroalga Prasiola calophylla (Carmichael ex Greville) Ku¨tzing (Trebouxiophyceae, Chlorophyta) 1 2 1 3 Anja Hartmann • Andreas Holzinger • Markus Ganzera • Ulf Karsten Received: 22 June 2015 / Accepted: 26 August 2015 / Published online: 10 September 2015 Ó The Author(s) 2015. This article is published with open access at Springerlink.com Abstract one- and two-dimensional 1H and 13C-NMR spectroscopy. Main conclusion We introduced a novel combination As trivial name for this novel MAA we suggest ‘prasiolin’. of chromatographic techniques for the purification and The ecologically essential function of prasiolin for UVR- analysis of a new UV-sunscreen mycosporine-like amino protection in terrestrial algae of the Trebouxiophyceae is acid (MAA) in the terrestrial green alga Prasiola calo- discussed. phylla. Keywords MAA (mycosporine-like amino acid) Prasiola calophylla (Carmichael ex Greville) Ku¨tzing isolation Á MAA purification Á Structural elucidation Á UV (Trebouxiophyceae, Chlorophyta) is a typical member of acclimation terrestrial algal communities in temperate Europe, where it regularly experiences various stress conditions including Abbreviations strong diurnal and seasonal fluctuations in ultraviolet HPTLC High performance thin layer chromatography radiation (UVR). As a photoprotective mechanism Prasi- MAA Mycosporine-like amino acid ola species and other related Trebouxiophycean taxa syn- UVR Ultraviolet radiation thesize a mycosporine-like amino acid (MAA) as natural sunscreen whose chemical structure was unknown so far. In the present study a new methodological approach is described for the isolation, purification and structural elu- Introduction cidation of this novel sunscreen in P. calophylla. The new compound exhibits an absorption maximum at 324 nm (in The green algal genus Prasiola (Trebouxiophyceae, the short ultraviolet-A), a molecular weight of 333 and a Chlorophyta) has a cosmopolitan biogeographic distribution molecular extinction coefficient of 12.393 M-1 cm-1, and from temperate to polar coastal and terrestrial environments could be identified as N-[5,6 hydroxy-5(hydroxymethyl)-2- in both the Northern and Southern Hemispheres (Rindi methoxy-3-oxo-1-cycohexen-1-yl] glutamic acid using 2007). The ecology of its members is very diverse since few species grow under aquatic conditions in freshwater systems or in the supralittoral zone of rocky marine coasts, while & Ulf Karsten most others represent a general and ubiquitous component of [email protected] various terrestrial ecosystems (Friedmann 1969; Rindi and Guiry 2004; Rodriguez et al. 2007). Some Prasiola species, 1 Institute of Pharmacy, Pharmacognosy, University of Innsbruck, Innrain 80-82/IV, 6020 Innsbruck, Austria such as P. crispa ssp. antarctica, show even a symbiotic lifestyle with Ascomycota resulting in the lichen Mastodia 2 Institute of Botany, Functional Plant Biology, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria tessellata (Perez-Ortega et al. 2010). Compared to aquatic 3 environments, terrestrial Prasiola are exposed to harsher Institute of Biological Sciences, Applied Ecology and abiotic conditions, such as strong gradients in water potential Phycology, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany between the terrestrial habitat (e.g. soil or rock surface) and 123 162 Planta (2016) 243:161–169 the atmosphere, resulting in regular desiccation (Hunt and During a study on the occurrence and function of MAAs Denny 2008; Holzinger and Karsten 2013). In addition, in Antarctic macroalgae Hoyer et al. (2001) reported in P. terrestrial algae experience strong diurnal and seasonal crispa ssp. antarctica a high concentration of a single fluctuations in insolation including UVR. unique, but chemically unknown UV-absorbing substance In many regions of the world UVR is enhanced due to with an absorption maximum at 324 nm. Gro¨niger and anthropogenically caused stratospheric ozone loss, which is Ha¨der (2002) confirmed the occurrence of this putative particularly strong during spring in Antarctica (‘ozone ‘‘324 nm-MAA’’ in the closely related P. stipitata from the hole’) (e.g. Whitehead et al. 2000), and UVR additionally supralittoral zone of the rocky island Helgoland (North increases with altitude as documented for the Alps (Blu- Sea). Since species of the thalloid Prasiola are phyloge- menthaler et al. 1996; Karsten 2008). The altitudinal effect netically related to other terrestrial green algae with a is depending on the wavelengths, i.e. ultraviolet-B radia- vegetative coccoid or pseudo-filamentous morphology tion (UV-B, 280–315 nm) is proportionally much stronger (Friedl and O’Kelly 2002), a screening on the occurrence enhanced with increasing elevation than ultraviolet-A of the 324 nm-MAA in these members of the Trebouxio- radiation (UV-A, 315–400 nm) (Blumenthaler et al. 1996). phyceae was undertaken (Karsten et al. 2005). Using high Both UV-A and UV-B represent a major stress factor for pressure liquid chromatography (HPLC) the data again many phototrophic organisms in terrestrial ecosystems confirmed the presence of the same molecule in the tested (Karsten 2008). Terrestrial algae face a photobiological Trebouxiophyceae, and preliminary UVR-exposure exper- dilemma, since solar radiation is essential for photosyn- iments indicated a strong accumulation of this compound thesis, and at the same time the UVR portion of the (Karsten et al. 2005). Based on these results the effect of spectrum can negatively affect many physiological pro- controlled UV-A and UV-B on photosynthetic perfor- cesses, mainly due to direct absorption by key biomole- mance, growth and the capability to synthesize this puta- cules. UV-B, for example, is strongly absorbed by DNA/ tive 324 nm-MAA was investigated in various other than in RNA and proteins causing conformational changes or even Karsten et al. (2005) screened terrestrial Trebouxiophycean photo damage that can subsequently disturb vital metabolic green algae forming biofilms on building facades or functions such as transcription, DNA replication and growing on soil (Karsten et al. 2007). The identical UV- translation (Buma et al. 1997). In the Antarctic terrestrial absorbing compound was assigned by HPLC in Sti- P. crispa ssp. antarctica DNA damage has been docu- chococcus sp. and Chlorella luteo-viridis based on mented after exposure to a combination of natural and matching UV-spectra and retention times. Furthermore, artificially enhanced UV-B (Lud et al. 2001). UVR-exposure experiments resulted in its strong and dose- However, if terrestrial algae are regularly confronted depending biosynthesis and accumulation, thus supporting with UVR in their habitat they rely on a number of dif- the function as an UV sunscreen. More importantly, the ferent physiological or biochemical mechanisms to miti- increase in MAA concentration in Stichococcus sp. and C. gate or even avoid biologically harmful UVR effects to luteo-viridis was reflected in a reduced UV-sensitivity of guarantee long-term survival (Karsten 2008). These growth and photosynthesis, which well explains the con- include avoidance, numerous protective mechanisms and/ spicuous ecological success of many Trebouxiophycean or repair of essential biomolecules (for details see Karsten green algae in the environmentally harsh terrestrial habitat. 2008 and references therein). Since the chemical structure of the putative 324 nm- A key protective mechanism in many terrestrial algae is the MAA in Prasiola and related Trebouxiophycean genera is biosynthesis and accumulation of UV-absorbing sunscreens, still not known, we developed a methodological approach such as mycosporine-like amino acids (MAAs) as docu- to isolate, purify and elucidate the structure of this sun- mented for various members of the Trebouxiophyceae (Kar- screen compound. Prasiola calophylla was used as a model sten et al. 2005, 2007) and Streptophyta (Kitzing et al. 2014; system because it is an abundant component of terrestrial Kitzing and Karsten 2015). MAAs are low-molecular-weight algal communities in rather rainy and temperate regions of compounds with maximum absorption bands between 310 Europe (Rindi and Guiry 2004). and 360 nm in the UV range (Cockell and Knowland 1999). Chemically MAAs represent a suite of closely related, colourless, water-soluble, polar and at cellular pH uncharged Materials and methods or zwitterionic amino acid derivatives that consist of aminocyclohexenone or aminocyclohexenimine rings (Kar- Biological material sten 2008 and references therein). So far, different MAAs have been identified in terrestrial cyanobacteria, green algae Prasiola calophylla (Carmichael ex Greville) Ku¨tzing and fungi (Garcia-Pichel and Castenholz 1993;Gorbushina (Trebouxiophyceae, Chlorophyta) was collected from a et al. 2003; Karsten et al. 2007). concrete basement of a metal fence at the Botanical 123 Planta (2016) 243:161–169 163 Fig. 1 Habitat and morphology of the terrestrial green alga Prasiola thallus showing the cell morphology and arrangement of the cells in calophylla. a Concrete wall with well-developed population of individual rows (arrow). Bars 10 cm (a), 100 lm(b), 50 lm(c) and Prasiola calophylla (arrow); b overview of ribbon-like curved fronds 20 lm(d) (arrow); c individual thallus piece, *160 lm broad; d details of Garden, University of Innsbruck (47°160200N, 11°2303400O, MAA isolation 611
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