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Photochemical & Photobiological Sciences Photochemical & Photobiological Sciences Accepted Manuscript This is an Accepted Manuscript, which has been through the Royal Society of Chemistry peer review process and has been accepted for publication. Accepted Manuscripts are published online shortly after acceptance, before technical editing, formatting and proof reading. Using this free service, authors can make their results available to the community, in citable form, before we publish the edited article. We will replace this Accepted Manuscript with the edited and formatted Advance Article as soon as it is available. You can find more information about Accepted Manuscripts in the Information for Authors. Please note that technical editing may introduce minor changes to the text and/or graphics, which may alter content. The journal’s standard Terms & Conditions and the Ethical guidelines still apply. In no event shall the Royal Society of Chemistry be held responsible for any errors or omissions in this Accepted Manuscript or any consequences arising from the use of any information it contains. www.rsc.org/pps Page 1 of Journal9 Name Photochemical & Photobiological Sciences Dynamic Article Links ► Cite this: DOI: 10.1039/c0xx00000x www.rsc.org/xxxxxx ARTICLE TYPE On the Photostability of Scytonemin, Analogues Thereof and Their Monomeric Counterparts Andreas Ekebergh,a Peter Sandina and Jerker Mårtensson*a Received (in XXX, XXX) Xth XXXXXXXXX 20XX, Accepted Xth XXXXXXXXX 20XX 5 DOI: 10.1039/b000000x Manuscript As a part of their sun-protective strategy, cyanobacteria produce the natural UV-screener scytonemin. Its accumulation in the extracellular sheaths allows the bacteria to thrive in inhospitable locations highly exposed to solar radiation. Scytonemin is often referred to as photostable and has been reported to be non- fluorescent. Taken together, these properties indicate inherently fast non-radiative relaxation processes. 10 Despite these interesting traits, the photophysics of scytonemin is as yet almost completely unexplored. In this study, we have compared the steady-state photophysics of scytonemin itself and four derivatives thereof. Furthermore, the in vitro photostability of scytonemin was studied in different solvents using a solar simulation system. Scytonemin and the investigated derivatives demonstrated a more rapid Accepted photoinduced decay in comparison with two commercial UV-screening agents. The photostability could 15 be modulated by varying the solvent, with the protic solvent ethanol providing the most stabilizing environment. Scytonemin has often been referred to as an exceptionally Introduction stable or photostable compound.3, 8-10 It is reported to remain largely intact in the sheaths of desiccated bacteria even after The extracellular cyanobacterial pigment scytonemin is believed 11 50 exposure to UVA for two months. The observed Sciences to be essential for the notable survival ability of many strains of photodegradation of scytonemin was shown to be orders of 20 cyanobacteria. Its vital importance to these organisms is magnitude slower in vivo than that of chlorophyll, another accentuated by the fact that despite the structural complexity of essential biological pigment. scytonemin, the compound is found in vast amounts in Scytonemin has also been proposed to provide the cyanobacteria cultures, accounting for up to 5% of the dry 55 cyanobacteria with a high tolerance to desiccation. This ability weight,1, 2 and the pigment has been observed in more than 300 has not only been ascribed to the UV-protection capacity but also 3 25 species of cyanobacteria. Additional support for the importance to the antioxidative properties of scytonemin.12, 13 Measurements of scytonemin has been provided by genomic comparisons, which have shown that scytonemin has a strong but slow radical reveal that the biosynthetic gene cluster of scytonemin is highly scavenging activity, and it has been suggested to be the main conserved between evolutionary diverse strains of 60 hydrophobic antioxidant in the extracellular matrix of cyanobacteria.4, 5 cyanobacteria.12 Therefore, scytonemin is proposed to play 30 The principal role of scytonemin is believed to be as a passive multiple roles in the defence mechanisms activated in response to UV-sunscreen that protects cyanobacteria against harmful UV- environmental stress such as UV radiation and desiccation.13 radiation. The proposed UV-protective role is corroborated by the Scytonemin is characterized by a homodimeric core structure Photobiological demonstration that transcription of the biosynthetic gene cluster 65 that is unique among natural products, and is composed of two and the biosynthesis of scytonemin is induced by UV- & cyclopenta[b]indol-2(1H)-one moieties linked at the 1 and 1’ 2, 4 35 irradiation. In addition, scytonemin is often found in the upper positions. The core is symmetrically appended by 4- layers of microbial mats that thrive in areas exposed to intense hydroxybenzylidene in the 3-position of the fused tricyclic solar irradiation. It is a greenish brown pigment and absorbs light cyclopenta[b]indol-2(1H)-one system. The parent skeleton only weakly in the visible region but shows strong absorption of 70 comprising the eight rings has been given the trivial name UV-light. Thus, scytonemin efficiently shields the cyanobacteria scytoneman by Proteau et al. who in 1993 were the first to 40 from high-energy radiation, while at the same time allows elucidate the chemical structure of the scytonemin pigment.14 penetration of light of the correct wavelengths necessary to The ascertained role as a “natural UV-sunscreen” has sparked support the vital photosynthesis. This UV-defence mechanism the interest of using scytonemin as a UV-absorbing agent has enabled cyanobacteria to occupy diverse ecological niches 75 (UVA)/sunscreen agent in consumer products or as a starting and to adapt to various extreme environments such as soil point for the development of new UVAs.9, 15 This interest has 45 surfaces, rocks, as well as in intertidal zones where the intensity certainly been nurtured by the reported stability of the pigment. of solar irradiation is high.6, 7 Photochemical This journal is © The Royal Society of Chemistry [year] [journal], [year], [vol], 00–00 | 1 Photochemical & Photobiological Sciences Page 2 of 9 The focus of this report is on the intrinsic photostability of 0.1% formic acid in acetonitrile. Aliquots of 5 μL were injected scytonemin, i.e. the photostability of scytonemin isolated from its onto the column and eluted with a gradient flow of 0.30 mL/min. natural environment. Thus, in this study, we report on the steady- A linear gradient from 10 to 100% B in 20 min was followed by state electronic spectroscopic properties of scytonemin and its 60 10 min of isocratic elution at 100% B. The column was 5 photostability in vitro. equilibrated with 10% B for 10 min between each run. NMR spectra were recorded on samples dissolved in Experimental deuterated chloroform (Chloroform-d). 1H-NMR spectra of compounds 1b, M1b and M1c and 13C-NMR spectra of Chemicals 65 compounds M1b and M1c were recorded on an Agilent 400 MHz Reagents and solvents were purchased from commercial vendors (101 MHz for 13C) spectrometer. 13C-NMR spectrum for and used as received for chemical synthesis, unless otherwise compound 1b was recorded on an Oxford 800 MHz (201 MHz 13 10 stated. Dry tetrahydrofuran (THF) was obtained via distillation for C) 4.2K magnet with Bruker Avance III HD and 5mm TXO over sodium under a nitrogen atmosphere. 2-Methyl-THF was cryoprobe. Residual non-deuterated chloroform was used as 1 13 distilled to remove stabilizer prior to spectroscopic 70 internal reference: H, δ = 7.26 ppm; C, δ = 77.0 ppm. The measurements. EtOH (95%) and ethyl acetate were used as following abbreviations, or a combination thereof, were used to Manuscript received for the spectroscopic measurements. characterize the multiplicities: s = singlet, d = doublet, t = triplet, q = quartet, m = multiplet, br = broad. Melting points (mp) were 15 Instrumentation and modes of analyses recorded on a Mettler FP 90/82 melting point apparatus and are Reactions were monitored by thin-layer chromatography (TLC) 75 uncorrected. IR spectra were recorded on a Bruker IFS 66v/S FT- carried out on 0.25 mm Merck silica gel plates (60–F254) using a IR spectrometer using KBr pellet sample preparation. HRMS mercury vapour UV-lamp to visualize the analytes. Fisher silica analyses were performed on either a QSTAR XL or a Waters gel (particle size 40 – 63 µm) was used for flash column Micromass Q-Tof micro instrument, using positive electrospray 20 chromatography. ionization and a tandem quadropole time-of-flight mass analyzer Accepted Absorption spectra were recorded on a Cary 5000 or Cary 80 (ESI+ qTOF). 4000 spectrophotometer, while fluorescence measurementes were Synthesis of di-O-methyl scytonemin 1b performed on a SPEX fluorolog 3 spectrofluorimeter (JY Horiba). Measurements were performed at room temperature To a mixture of diastereoisomers 2 (50 mg, 0.09 mmol) in dry 25 using 1x1 cm quartz cuvettes for all experiments except the THF (5.5 mL, 0.015 M) under air atmosphere was added neat photolysis/HPLC experiments where 1 mm quartz cuvettes were DDQ (60 mg, 0.26 mmol). The solution was stirred for 1 min, used. Concentrations were typically set to give an optical density 85 diluted with EtOAc (40 mL) and washed with NaHCO3 (4 × 10 of approximately 0.1 which corresponds to a concentration of mL) to remove DDQ-adducts. The organic phase was further Sciences approximately 1.5 µM as estimated using the extinction washed with brine (10 mL) and a dark precipitate was observed. -1 -1 10 30 coefficient of 112.6 L g cm for scytonemin in acetone. The layers were separated and the remaining precipitate was Photolysis experiments were also performed in a Solarlux™ dissolved in acetone (30 mL) and EtOAc (30 mL). The resulting Solar Simulation system from EYE Lighting International / 90 solution was washed with brine (15 mL) and combined with the Iwasaki Electric that generates the same spectral distribution as previously obtained organic layer.
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