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Boron-Containing Organic Pigments from a Jurassic Red Alga

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Boron-Containing Organic Pigments from a Jurassic Red Alga Boron-containing organic pigments from a Jurassic red alga Klaus Wolkensteina,1, Jürgen H. Grossb, and Heinz Falkc aInstitute of Analytical Chemistry, Johannes Kepler University Linz, 4040 Linz, Austria; bInstitute of Organic Chemistry, University of Heidelberg, 69120 Heidelberg, Germany; and cInstitute of Organic Chemistry, Johannes Kepler University Linz, 4040 Linz, Austria Edited by Victoria J. Orphan, California Institute of Technology, Pasadena, CA, and accepted by the Editorial Board September 23, 2010 (received for review June 10, 2010) Organic biomolecules that have retained their basic chemical oxide (DMSO). The reddish-colored extracts were purified by structures over geological periods (molecular fossils) occur in a wide solid-phase extraction and characterized by HPLC–diode array range of geological samples and provide valuable paleobiological, detection–electrospray ionization–mass spectrometry (HPLC- paleoenvironmental, and geochemical information not attainable DAD-ESI-MS). From a large Solenopora sample (102.5 g) from from other sources. In rare cases, such compounds are even France, 1.1 mg of crude pigment isolate was obtained as an in- preserved with their specific functional groups and still occur within tensely crimson-colored organic residue (Fig. S1). HPLC analysis the organisms that produced them, providing direct information on of the pigments revealed numerous compounds with similar UV- the biochemical inventory of extinct organisms and their possible visible spectra, with the prominent group at retention time of evolutionary relationships. Here we report the discovery of an 8.0–10.0 min showing a major broad absorption band at 520 nm exceptional group of boron-containing compounds, the borolitho- and a minor one at 420 nm (Fig. 1B), but no Soret band at ~400 chromes, causing the distinct pink coloration of well-preserved nm (which is characteristic of porphyrins). In the negative-ion specimens of the Jurassic red alga Solenopora jurassica. The boroli- mass spectra, corresponding ions at mass-to-charge ratios (m/z) thochromes are characterized as complicated spiroborates (boric of 839, 853, and 867 were detected, indicating that the pigments acid esters) with two phenolic moieties as boron ligands, represent- consist of a homologous series of compounds and accompa- ing a unique class of fossil organic pigments. The chiroptical prop- nying isomers (Fig. 1C). Moreover, all compounds exhibited a EVOLUTION erties of the pigments unequivocally demonstrate a biogenic origin, characteristic isotope pattern indicative of the presence of a sin- at least of their ligands. However, although the borolithochromes gle boron atom (Fig. 1D). Based on accurate mass data obtained originated from a fossil red alga, no analogy with hitherto known by HPLC-MS and additional measurements using Fourier present-day red algal pigments was found. The occurrence of the transform ion cyclotron resonance mass spectrometry (FT-ICR- borolithochromes or their possible diagenetic products in the fossil MS) for the ions at m/z 839, 853, and 867, the molecular record may provide additional information on the classification and formulae C50H36O12B, C51H38O12B, and C52H40O12B were de- phylogeny of fossil calcareous algae. termined (Fig. 1D and Fig. S2). The boron could be readily removed from the borolithochromes CHEMISTRY fossil red algae | molecular preservation | phenolic boric acid esters | optical by reacting the pigments in methanol containing 0.1% tri- activity | liquid chromatography–mass spectrometry fluoroacetic acid. Several series of homologous pigments were isolated by HPLC for further analysis. Solvolysis (methanolysis/ he striking pink coloration of specimens of the fossil calcar- hydrolysis) of a fraction containing various isomers of the pigments Solenopora jurassica − − − − Teous red alga has been a matter of de- [C50H36O12B] ,[C51H38O12B] ,and[C52H40O12B] ([M] )(Fig. bate for decades and is well known from the Jurassic of Great 2A) resulted in the formation of only two HPLC peaks (Fig. 2B) − Britain (“Beetroot Stone”)(1–3) and France (4). Solenopora with ions at m/z 415 and 429 ([M–H] ), which could be assigned to C25H19O6 and C26H21O6 (Fig. 2C). Accordingly, solvolysis of specimens at the reported localities are well preserved and ex- − a fraction containing isomers of the pigments [C48H32O8B] , hibit preserved tissue structures and regular alternating bands − − – [C49H34O8B] , and [C50H36O8B] resulted in the formation of (2 4) that have been interpreted as seasonal growth structures − (3). The characteristic coloration associated with these bands is two HPLC peaks with ions at m/z 369 and 383 ([M–H] ), which A–C generally more intense in the inner portions of the algal nodules could be assigned to C24H17O4 and C25H19O4 (Fig. S3 ). (2, 3). Given that no traces of the pigments can be found in the Obviously, two equivalent homologous ligands with different surrounding sediment, consisting of white oolitic limestones at substitution patterns give rise to the combinatorial multitude of both locations, there can be no doubt that the pigments are of homologous and isomeric borolithochromes. All solvolysis endogenous origin. Previous reports speculated that the pig- products revealed UV-visible spectra similar to the boron- B Inset ments from the Beetroot Stone likely are porphyrins (2), gen- containing precursors (Fig. 2 , ) with a distinct bath- erally known from bituminous sediments and petroleum (5), ochromic shift of the long-wavelength absorption. Furthermore, whereas the coloration of specimens from France has been at- all borolithochromes and all solvolysis products exhibited deu- tributed to fossil hypericinoid pigments (fringelites) (6), poly- terium-exchangeable protons, indicating the presence of multiple hydroxy groups (Fig. S4). For the homologous borolithochromes cyclic quinones described from purple-colored fossil crinoids − − − (7, 8). Here we provide evidence that the pink coloration of S. [C50H36O12B] to [C52H40O12B] ([M] ), six H/D exchanges jurassica from both occurrences is in fact due to the presence of a unique class of complicated boron-containing organic pig- Author contributions: K.W. designed research; K.W. and J.H.G. performed research; K.W. ments, which we name borolithochromes. collected fossil material; J.H.G. contributed new reagents/analytic tools; K.W., J.H.G., and H.F. analyzed data; and K.W. and H.F. wrote the paper. Results and Discussion The authors declare no conflict of interest. S. jurassica We analyzed distinctly pink-colored specimens (Fig. This article is a PNAS Direct Submission. V.J.O. is a guest editor invited by the Editorial 1A) from two of the localities reported in the literature, in- Board. cluding a part of the neotype from the Beetroot Stone. Following 1To whom correspondence should be addressed. E-mail: [email protected]. dissolution of the carbonate matrix with HCl, crude extracts This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. were obtained by extraction of the residues with dimethyl sulf- 1073/pnas.1007973107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1007973107 PNAS Early Edition | 1of5 Downloaded by guest on October 1, 2021 A C DAD1 - C:Sig=520,4 161209_004.d )UAm 4 520 nm 3 ( .sbA 2 1 x105 6 - Scan Frag=200.0V 161209_004.d 5 m/z 839.23 ytisn 4 m/z 853.25 m/z 867.26 e 3 tnI 2 1 6 7 8 9 10 11 12 Retention time (min) B D 4 DAD1 - C:Sig=520,4 161209_004.d x10 -ESI Scan (8.585-8.750 min, 11 scans) Frag=200.0V 161209_004.d839.2306 Subtract 839.2306 ) ) 4 6 UA 7 UAm 5 - m(ecn 6 [CHOB]50 36 12 ( 4 3 mn025 3 ab 5 r y o 2 tisnetn s b 1 A 4 840.2334 t 2 0 840.2334 a 300 400 500 600 I ecnabrosbA 3 Wavelength (nm) 2 1 839.23044838.2327 838.2327 841.2356 1 841.2356 842.2382 842.2382 0 6 8 10 12 14 16 18 837 838 839 840 841 842 843 844 Retention time (min) m/z Fig. 1. Specimen of the Jurassic red alga S. jurassica with exceptional preservation of fossil boron-containing organic pigments (borolithochromes) and analytical data of extracted pigments (DMSO extract). (A) Polished slab of S. jurassica (MNHN 40091), Upper Jurassic, Tannay, France. (B) HPLC chromatogram (detection at 520 nm) of extracted fossil pigments (MNHN 23874) and UV-visible spectrum of the first peak in the chromatogram (Inset). (C) Section from the HPLC chromatogram shown in B (Upper) and extracted ion chromatograms (negative-ion ESI-MS) (Lower) of fossil pigments. (D) Mass spectrum of the main − 11 single isomeric pigment showing the characteristic isotope pattern of boron, observed m/z 839.2306 [M] , calculated for C50H36O12 B: 839.2305). Note the difference of 0.9979 Da (calculated for 11B − 10B: 0.9964) between m/z 838 and 839 and the difference of 1.0028 Da (calculated for 13C − 12C: 1.0034) between m/z 839 and 840. − were observed, compared with two H/D exchanges for homologs the borate but the solvolysis products form [M–H] ions, based − − − [C48H32O8B] to [C50H36O8B] ([M] ), suggesting a difference on the number of H/D exchanges, a quinoid structure can be of four hydroxy groups between the two series (Fig. S4 A and B). excluded. Characteristic fragmentation patterns were obtained The distinct hypsochromic shift of 15 nm observed in the UV- by collision-induced dissociation of the ions at m/z 415 and 429 visible spectra of the two series indicates that the hydroxy groups by means of ESI tandem MS (Fig. 2D). Compounds demon- are phenolic (Fig. S5). Accordingly, the corresponding products strated elimination of CH4 and C2H6, indicating the presence of – − C25H19O6 and C24H17O4 ([M H] ) (and their homologs) showed alkyl side chains, followed by elimination of CH2CO and CO2. four and two H/D exchanges, respectively (Fig. S4 C and D), Fragmentation of the ions at m/z 369 and 383 also led to the suggesting a difference of two hydroxy groups between the elimination of CH4 and C2H6 (Fig.
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