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The Enigmatic Structure of the Crenarchaeol Isomer ⇑ Jaap S

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The Enigmatic Structure of the Crenarchaeol Isomer ⇑ Jaap S Organic Geochemistry 124 (2018) 22–28 Contents lists available at ScienceDirect Organic Geochemistry journal homepage: www.elsevier.com/locate/orggeochem The enigmatic structure of the crenarchaeol isomer ⇑ Jaap S. Sinninghe Damsté a,b, , W. Irene C. Rijpstra a, Ellen C. Hopmans a, Mimi J. den Uijl c, Johan W.H. Weijers c, Stefan Schouten a,b a NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands b Utrecht University, Faculty of Geosciences, Department of Earth Sciences, P.O. Box 80.021, 3508 TA Utrecht, The Netherlands c Shell Global Solutions International B.V., Grasweg 31, 1031 HW Amsterdam, The Netherlands article info abstract Article history: Isolation of crenarchaeol and its isomer from marine surface sediments, followed by ether cleavage and Received 30 March 2018 GC–MS characterization using supersonic molecular beam (SMB) ionization of the biphytanes formed, Received in revised form 12 June 2018 revealed that the crenarchaeol isomer comprises a tricyclic biphytane that is stereochemically different Accepted 12 June 2018 from the tricyclic biphytane of crenarchaeol. This isomeric tricyclic biphytane was also released from the Available online 15 June 2018 crenarchaeol isomer in extant Thaumarchaeotal biomass. Reinterpretation of previously obtained 13C NMR data of the crenarchaeol isomer suggested that the cyclopentane moiety adjacent to the cyclohexyl Keywords: moiety of the tricyclic biphytane of the crenarcheaol isomers possesses the unusual cis stereochemistry in Crenarchaeol comparison to the trans stereochemistry of all cyclopentane moieties in crenarchaeol. This stereochem- Structural determination ical difference likely affects the packing of lipid membranes of Thaumarchaeota and therefore provides a TEX86 Archaea biophysical explanation for the role of the crenarchaeol isomer in the TEX86 palaeothermometer based on Thaumarchaeota fossilized Thaumarcheotal lipids. GDGTs Ó 2018 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 1. Introduction marine and lacustrine sediments are widely used in TEX86 palaeothermometry (Schouten et al., 2002). Thaumarchaeota regu- Glycerol dibiphytanyl glycerol tetraethers (GDGTs) form the late the chemical composition of their membrane to influence its core membrane lipids of many archaea and can therefore be used physical properties to optimally function at a specific temperature. as biomarker lipids. A ubiquitous group of archaea in marine envi- The TEX86 palaeothermometer is based on the fractional abun- ronments (e.g. Karner et al., 2001) are the Thaumarchaeota, which dances of four GDGTs that typically occur in lower abundances perform nitrification, i.e. oxidation of ammonium (Könneke et al., than crenarchaeol and GDGT-0 (i.e. a GDGT with no cyclopentane 2005; Wuchter et al., 2006). Their membrane lipids contain a moieties). These four GDGTs are GDGT-1, -2, -3, and an isomer of specific GDGT, called crenarchaeol (see Fig. 1 for structures), con- crenarchaeol, which typically occurs in low abundance relative to taining an uncommon cyclohexane moiety in addition to four crenarchaeol (i.e. up to 5%), although in some Thaumarchaeotal five-membered rings (Sinninghe Damsté et al., 2002). So far, cre- species they can be much more abundant (Pitcher et al., 2010; narcheaol has only been found in cultures of Thaumarchaeota Sinninghe Damsté et al., 2012). The crenarchaeol isomer plays an (see for a review Schouten et al., 2013b) but not in other archaeal important role in the TEX86 proxy as its abundance increases sub- cultures, indicating that it can be used as specific marker for Thau- stantially in tropical regions and plays a key role in reconstructing marchaeota. This is confirmed by studies of the marine water col- sea surface temperature from past greenhouse periods (e.g. O’Brien umn where the abundance of specific genes of Thaumarchaeota et al., 2017). and crenarchaeol containing polar head groups show the same The crenarchaeol isomer is characterized by a later retention depth and seasonal profiles (e.g. Pitcher et al., 2011a, 2011b). time than crenarchaeol but with an identical mass spectrum as Thaumarchaeotal GDGTs find an application in paleoceanogra- obtained by atmospheric pressure chemical ionization (APCI) mass phy and paleoclimatology since their fossilized GDGTs in both spectrometry (Sinninghe Damsté et al., 2002). It has been proposed to be a so-called regioisomer of crenarchaeol, i.e. where the glyc- erol units are not in a parallel but an anti-parallel configuration ⇑ Corresponding author at: NIOZ Royal Netherlands Institute for Sea Research, or vice versa, because the carbon signals in its 13C NMR spectrum Department of Marine Microbiology and Biogeochemistry, and Utrecht University, were identical to those in the 13C NMR spectrum of crenarchaeol PO Box 59, 1790 AB Den Burg, The Netherlands. (Sinninghe Damsté et al., 2002; Schouten et al., 2013b). Recently, E-mail addresses: [email protected], [email protected] (J.S. Sinninghe Damsté). https://doi.org/10.1016/j.orggeochem.2018.06.005 0146-6380/Ó 2018 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). J.S. Sinninghe Damsté et al. / Organic Geochemistry 124 (2018) 22–28 23 C1 H H O B3 B8 B20' B19' OH C2 B1 B7 H B9 B16 B17 B18 B11 C3 O A3 A7 B17' A8 B16'A20' H A1 A19'H B1' A16 H A17 H A11 A11' A18 A15' A10' B3' O A18' A17' C3' Crenarchaeol H A16' A14' A12' H A7' A1' C2' OH A19 A13' A8' O C1 HHB8 H H C1' O B3 B20' B19' OH C2 B1 B7 H B9 anti-parallel B16 B17 B18 B11 C3 O A3 A7 B17' A8 B16'A20' H A1 A19'H B1' A16 H C1' A17 H A11 A11' A10' B3' O C2' A18 A15' A18' A16' A17' OH H A14' A1' A19 A12' H A7' H A13' O C3' A8' H C1 H H parallel O B3 B8 B20' B19' OH C2 B1 B7 H B9 B16 B17 B18 B11 C3 O A3 A7 B17' A8 B16'A20' H A1 A19'H B1' A16 H A17 H A11 A11' A18 A15' A10' B3' O A18' A17' C3' Crenarchaeol isomer H A16' A14' A12' H A7' A1' C2' OH A19 A13' A8' O C1 HHB8 H H C1' O B3 B20' B19' OH C2 B1 B7 H B9 anti-parallel B16 B17 B18 B11 C3 O A3 A7 B17' A8 B16'A20' H A1 A19'H B1' A16 H C1' A17 H A11 A11' A10' B3' O C2' A18 A15' A18' A16' A17' OH H A14' A1' A19 A12' H A7' H A13' O C3' A8' H parallel Biphytanes H I H H H H II H H H H trans H III H H H H cis Fig. 1. Chemical structures of components mentioned in the text. The identification of the structure of crenarchaeol is based on the work of Sinninghe Damsté et al. (2002).It shows both possible regioisomers with the parallel and anti-parallel stereoisomerism since it was not possible to discern this based on detailed NMR studies. Based on the tentative identification of partial degradation products of crenarchaeol in sediments, Liu et al. (2018) have proposed that the parallel arrangement predominates. The structure of the crenarchaeol isomer is tentatively identified here and differs from that of crenarchaeol in that the cyclopentane moiety adjacent to the cyclohexyl moiety has the opposite stereochemistry (cis instead of trans). The structures of the BPs that can be formed from these GDGTs are also indicated. however, Liu et al. (2018) presented data based on the tentative commonly used electron impact ionization (Fialkov et al., 2008). identification of presumed partial degradation products of both In addition, we re-examined our previously obtained NMR data crenarchaeol and its isomer indicating that both possess predomi- to evaluate the hypothesis of Liu et al. (2018) that the structure nantly the parallel configuration. Liu et al. (2018) also character- of the crenarchaeol isomer is characterized by a different ring con- ized the biphytane (BP) moieties of the crenarchaeol isomer and figuration compared to crenarchaeol. suggested that it may possess a different ring configuration of the tricyclic BP. Here, we have repeated the experiments of Liu et al. (2018) on purified (>95%) crenarchaeol and its isomer and 2. Materials and methods studied the structure of these BPs by gas chromatography-mass spectrometry (GC–MS) using supersonic molecular beam (SMB) Crenarchaeol isomer was previously isolated from Arabian Sea ionization, which is a much softer ionization technique than the sediments as described by Sinninghe Damsté et al. (2002). Crenar- 24 J.S. Sinninghe Damsté et al. / Organic Geochemistry 124 (2018) 22–28 chaeol was isolated from Arabian Sea surface sediments following I a techniques described previously (Schouten et al., 2013a). Their II purity was checked by dissolving them in hexane/propanol (99:1, v/v), filtered over a 0.45 mm polytetrafluorethylene filter, and analysis by high performance liquid chromatography/APCI mass spectrometry (HPLC/APCI-MS) for GDGTs using a method described elsewhere (Hopmans et al., 2016) and by NMR (see Schouten et al., 2013a). Aliquots of the isolated crenarchaeol and the crenarchaeol isomer were subjected to ether cleavage (57% HI) as described by Lengger et al. (2014). The resulting alkyl iodides were reduced to hydrocarbons with H2/PtO2 (Kaneko et al., 2011), which were ana- lyzed with gas chromatography (GC) after on-column injection on an Agilent 7890B GC instrument and in splitless mode with GC–MS using an Agilent 7890A GC instrument equipped with a Agilent b 5975C VL MSD detector. A CP Sil 5CB column was used (25 m x 0.32 mm i.d.; film thickness 0.12 lm; He carrier gas).
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