Organic Geochemistry 85 (2015) 66–75

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Organic Geochemistry

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Predominance of archaea-derived hydrocarbons in an Early Triassic microbialite ⇑ Ryosuke Saito a, , Kunio Kaiho a, Masahiro Oba a, Megumu Fujibayashi b, Jinnan Tong c, Li Tian c a Institute of Geology and Paleontology, Tohoku University, Sendai 980-8578, Japan b Department of Civil and Environmental Engineering, Tohoku University, Tohoku 980-8579, Japan c State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China article info abstract

Article history: We investigated the distribution of lipids in Lower Triassic sedimentary rocks (252–247 myr) from Received 13 July 2014 South China, including a shallow water microbialite in the uppermost section of the outcrop. Received in revised form 12 December 2014 Archaeal derived hydrocarbons were the major constituents of the microbialite from the latest Early Accepted 16 May 2015 Triassic. Among these, we detected (i) abundant C acyclic and monocyclic biphytanes (possibly Available online 23 May 2015 40 derived from glycerol dialkyl glycerol tetraether lipids) and their degradation products, C30–39 pseudo-

homologues and (ii) a C25 head-to-tail linked (regular) isoprenoid hydrocarbon [possibly derived from Keywords: dialkyl glycerol diether lipids (DGDs)] and its degradation products, C pseudohomologues and Microbialite 21–24 abundant pristane and phytane. Through combination of compound-speciﬁc stable carbon isotope anal- Isoprenoid hydrocarbons 13 Early Triassic ysis of isoprenoid hydrocarbons, which had average d C values of À35‰ to À30‰, and their molecular Archaea distribution, it was not possible to unambiguously deﬁne the archaeal source for the biphytanes in the 13 Organic geochemistry microbialite. The d C values for pristane and phytane were similar to those for head-to-tail linked

C21–25 isoprenoids; potential source organisms for these compounds were halophilic archaea. Except for methane seep microbialites, no other ancient or recent phototrophic microbialites have been reported to contain predominantly archaeal isoprenoid hydrocarbons. Our ﬁndings suggest the presence of a new type of microbialite. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction their formation (Pruss et al., 2005). Grotzinger and Knoll (1995) first proposed the upwelling of deep alkaline waters onto a shal- The Early Triassic, which followed the latest Permian mass lower shelf as a mechanism for carbonate precipitation on the extinction, is the interval in which microbialites and other unusual shelf, as the alkalinity increased. Because deep alkaline water sedimentary structures, such as seafloor fans, occurred repeatedly may have contained abundant H2S, mixing with surface water in four successive events, the late Griesbachian to Dienerian, the would have poisoned any metazoans present; the resulting deposi- early Olenekian and the latest Early Triassic (Baud et al., 2007). tional environments lacking metazoans facilitated the formation of Around the end of the Early Triassic, microbialites (with a microbialites (Fischer, 1965; Awramik, 1971, 1992; Riding, 2006). thrombolytic texture) occurred on an isolated pelagic plateau of This mechanism explains the occurrence of carbonate fans in the the Western Tethys (Halstatt Limestone of Dobrogea, Romania; late Early Triassic (Woods et al., 1999). Atudorei et al., 1997), and microbialites (stromatolites and throm- In recent studies of microbialites, investigations based on bolites) occurred in the Virgin Limestone, while seafloor fans microbial 16S rRNA genes have indicated that modern (Union Wash Formation; Pruss and Bottjer, 2004, 2005; Pruss microbialite-forming mats contain a plethora of microbial species, et al., 2005) occurred on the eastern Panthalassa margin (western with species richness exceeding several thousand (e.g. Papineau USA). Pruss et al. (2005) and Pruss and Bottjer (2004) suggested et al., 2005). Often, the communities of so-called shallow water that the formation of microbialites is associated with an alkalinity phototrophic mats contain 5–7 key groups of microbes (Dupraz increase in seawater because they noticed that they occur during et al., 2009), including photolithoautotrophs (cyanobacteria), aero- transgressive phases, suggesting that the flooding of shallower bic heterotrophs, fermenters, anaerobic heterotrophs [predomi- depositional environments by deeper alkaline ocean waters fosters nantly sulfate reducing bacteria (SRB)], sulfide oxidizers, anoxygenic phototrophs (purple and green sulfur bacteria) and ⇑ Corresponding author. Tel.: +80 22 795 6615. methanogens. E-mail address: [email protected] (R. Saito). http://dx.doi.org/10.1016/j.orggeochem.2015.05.004 0146-6380/Ó 2015 Elsevier Ltd. All rights reserved. R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 67

The metabolism of cyanobacteria, anoxygenic phototrophs and The depositional environments of the Early Triassic successions

SRB may promote the precipitation of CaCO3, whereas aerobic het- now exposed in the study area included a distal offshore ramp, prox- erotrophs, sulﬁde oxidizers and fermenters promote the dissolu- imal ramp, lower shore face and marginal sea, with a water depth tion of CaCO3 (Dupraz et al., 2009). The interplay of all the ranging from 20 to 200 m (Chen et al., 2011). The upper unit contains metabolic activities in a single mat ultimately determines whether the microbialite, which has a carbonate content of >90%. The upper-

CaCO3 is precipitated or dissolved (Dupraz et al., 2009). Except for most part of this section is overlain by evaporite-solution breccia non-phototrophic methane-seep microbialites (e.g. Peckmann sediments of Middle Triassic age (Tong and Zhao, 2005), which et al., 1999, 2009; Thiel et al., 1999, 2001; Goedert et al., 2003), include large traces similar to the fish-swimming trail Undichna archaea are usually minor constituents (ca. 10%) of modern micro- (Chen et al., 2011). These lines of evidence suggest that the upper bial mat communities (e.g. Papineau et al., 2005). unit of the upper sequence in the section was a marginal sea with Biomarker analysis has been applied to few other ancient restricted circulation (Chen et al., 2011). non-methane seep microbialites (hereafter referred to as ‘‘micro- The 118 samples include carbonates, shales and marls from the bialites’’ because this study focusses on non-methane seep micro- 250 m thick sedimentary sequence at Majiashan–Pingdingshan bialites) (e.g. Keupp et al., 1993; Malinski et al., 2009; Allen et al., (Fig. 1). They were analyzed according Oba et al. (2006). Briefly, 2010). Such studies have revealed contributions from various bac- after any apparent surface contamination was cut away, the sam- teria (including Cyanobacteria), algae, higher plants and archaea to ples (10–100 g) were powdered. Solvent extracts were obtained microbialites. The contribution of archaeal lipids has been minor with a Soxhlet apparatus using CH2Cl2:MeOH (7.5:1 v/v) for 48 h. (Keupp et al., 1993; Allen et al., 2010) to moderate (Heindel Each extract was dried over Na2SO4 and concentrated by evapora- et al., 2013) or undetectable (Malinski et al., 2009). Most studies tion under reduced pressure. The concentrated extract was sepa- of microbialites have shown a predominance of n-alkanes or rated into nine fractions (Fs) on a silica gel column (0.6 g silica, n-fatty acids. However, it has been noted that the early Early 63–200 lm mesh) as follows: 2 ml hexane (F1a); 4 ml hexane Triassic microbial mats contain a relatively high proportion (ca. (F1b); 3 ml hexane/toluene, 3:1 v/v (F2); 3 ml hexane/EtOAc, 20%) of archaeal-derived isoprenoid hydrocarbons, including 19:1 v/v (F3); 3 ml hexane/EtOAc, 9:1 v/v (F4); 3 ml biphytane and pseudohomologues, and C21–25 regular isoprenoids hexane/EtOAc, 17:3 v/v (F5); 3 ml of hexane/EtOAc, 4:1 v/v (F6); (Heindel et al., 2013). Benthic microbial mats occur in hypersaline 3 ml hexane/EtOAc, 3:1 v/v (F7); and 10 ml MeOH (F8). The alipha- low O2 marine environments, although Heindel et al. (2013) imply tic hydrocarbon (F1a) and aromatic hydrocarbon fractions that the farnesane in microbialites could have been produced by (F1b + F2) were analyzed with gas chromatography–mass spec- benthic and/or planktonic anoxygenic phototrophic bacteria. trometry (GC–MS). The branched and cyclic compounds were sep- Here, we report on the biomarkers in the hydrocarbon fractions arated from the aliphatic hydrocarbon fraction using 5A molecular from an upper Triassic microbialite in Chaohu, South China and sieve, on the basis of the method by Murphy (1969). constrain the environmental changes that arose during the forma- Biomarkers were assigned and quantified using an Agilent 6893 tion of the microbialite. GC instrument interfaced with an Agilent 5973 mass selective detector with an ionizing electron energy of 70 eV, and scanning from m/z 50 to 600 with a scan time of 0.34 s. A fused silica 2. Geological setting and methods HP-5MS column (30 m, 0.25 mm i.d., 0.25 lm film thickness) was used with He as carrier gas. The samples were injected at 50 °C Samples were obtained from Lower Triassic sections in North and maintained at that temperature for 1.0 min. The temperature Pingdingshan, West Pingdingshan and South Majiashan in Chaohu, was then raised to 120 °Cat30°C/min and to 310 °C (held Anhui Province, South China (Fig. 1). During the Early Triassic, 20 min) at 5 °C/min. South China was located in the low latitude eastern Tethys Sea.

Fig. 1. Paleogeographic map of South China (modiﬁed from Song et al., 2013) and location of the Chaohu section. 68 R. Saito et al. / Organic Geochemistry 85 (2015) 66–75

Biphytanes and their pseudo homologues were assigned on the center to upper right) and unknown calcareous organisms were basis of retention times and mass spectra by comparison with observed at 150.1 m (Fig. 2E). results in Oba et al. (2006), Albaiges (1980). Lycopane, 2,6,10,14, 18-pentamethylicosane, and their derivatives were compared with 3.2. Lipid biomarkers in the Early Triassic succession results from Greenwood and Summons (2003), Sinninghe Damsté et al. (2003). The carbon isotopic composition of the aliphatic The typical aliphatic hydrocarbon fractions were dominated by hydrocarbon fraction (11 samples) was determined with a Delta C n-alkanes (Fig. 3A, B and D). Pristane (Pr) and phytane (Ph) V Advantage mass spectrometer (Thermo Fisher Scientiﬁc) coupled 14–31 were present in all samples (Fig. 3A–D). The most abundant com- to a Trace GC Ultra (Thermo Fisher Scientiﬁc) at Tohoku University. pounds, apart from n-alkanes, Pr and Ph, were C head-to-tail The GC conditions were as above. The d13C values (‰, relative to 21–25 linked isoprenoid hydrocarbons and branched alkanes such as Peedee Belemnite) were computed after injecting multiple peaks monomethylated heptadecanes (MMHs). Of the 118 samples, C of pure CO via a separate line to prevent their coelution with 40 2 acyclic biphytane was found only in the uppermost Lower the peaks from the gas chromatograph, and determining the d13C Triassic samples (142.5 m, 146.1 m; Figs. 3B and 4A–C) and in values of the CO peaks on separate runs by injecting n-alkane 2 the microbialite (Section 3.3), but not in the uppermost sediment standards into the gas chromatograph. All the samples were layers. Carotanes derived from anoxygenic photosynthetic bacteria analyzed twice, except sample 146.1 m. were detected only in limestone (micrite) from 146.1 to 142.5 m (Fig. 2A; see also Saito et al., 2014), just below the microbialite (Fig. 4). 3. Results

3.1. Mega- and macrostructures of the microbialite 3.3. Lipid biomarkers in microbialite

The microbialite (148.1–150.1 m; Fig. 2A) showed a horizon- The chromatogram of F1a from the microbialite (148.1– tally waved shape (Fig. 2C). The macrostructure consisted of nodu- 150.1 m) was dominated by isoprenoids, including C40 acyclic lar and columnar growth forms (Fig. 2C, lower and upper parts, biphytane, C30–39 head-to-head isoprenoids (presumably derived respectively), with a faint irregular laminar texture. No calcimi- via degradation of C40 acyclic biphytane) and C14–25 head-to-tail crobes were recognizable (Fig. 2D and E). The microbialite was isoprenoids (Fig. 3C). Predominant isoprenoid hydrocarbons were, ﬁlled with recrystallized calcite and/or dolomite (Fig. 2D and E). however, Pr and Ph (Fig. 3C). Monocyclic biphytanes (two isomers) Faintly visible spicules were recognizable at 148.1 m (Fig. 2D, were also detected, but at much lower content than acyclic

Fig. 2. Columnar section showing the stratigraphic distributions of the biomarkers, outcrop photograph, and the mega- and microstructures of the microbialite (148.1–

150.1 m). (A) Stratigraphic distributions of the microbialite, carotanes derived from green and purple sulfur bacteria, and archaea-derived hydrocarbons; C40 acyclic biphytane was detected in the uppermost Lower Triassic samples (142.5–150.1 m). (B) Outcrop photograph showing the microbialite. (C) Dark gray, laminated microbialite at 148.1 m. Arrows indicate the nodular and columnar structures of the lower and upper parts. (D and E) Thin section photomicrographs of the microbialite at 148.1 and 150.1 m, respectively. Note that the thin section from 150.1 m contains unknown fossils (indicated by arrow). Data on the photic zone euxinia and dibenzothiophenes (DBTs) are from Saito et al. (2014). Conodont zones are from Zhao et al. (2007). R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 69

Fig. 3. Total ion chromatogram (TIC) of the hydrocarbon fractions from the samples from 77.5 m (A), 142.5 m (B), 148.1 m (microbialite) (C) and 159 m (D). Triangles, n-alkanes; squares, head-to-tail isoprenoids; circles, head-to-head isoprenoids; Pr, pristane; Ph, phytane; MMHs, monomethyl heptadecanes.

biphytane (Fig. 3C). Apart from various isoprenoids, minor C13–28 Interestingly, the lower values (À3.6‰ to +0.8‰) were observed n-alkanes were present (Fig. 3C). exclusively at 142.5–150.1 m (prior to and within the microbialite), whereas the other horizons showed relatively high values (+1.4‰ to +6‰). 3.4. Compound speciﬁc isotope analysis

Since a prominent unresolved complex mixture (UCM) was pre- 4. Discussion sent in all samples, the compound-specific carbon isotope values may be biased and less accurate. However, the UCM was not signif- 4.1. Classification of the microbialite icant enough to blur the overall carbon isotope trend recorded (see below). Stromatolites are defined as ‘‘macroscopically layered authi- The overall d13C values of the hydrocarbons showed relatively genic microbial sediments with or without interlayered abiogenic light d13C values in the late Early Triassic (Olenekian) (77.5– precipitates’’ (Riding, 2011). The microbialite here was categorized 150.1 m) and slightly heavier values in the early Middle Triassic as stromatolite because it was composed of a fine-grained crust (Anisian; 153.1–159 m; Fig. 5 and Table 1). We suggest that this with an irregularly layered fabric (Fig. 2), indicating an essentially positive isotope excursion in hydrocarbons between 148.1 and microbial origin (cf. Riding, 2011). Lamination in stromatolite has 153.1 m (Fig. 5 and Table 1) identifies the horizons of the been interpreted to result from diurnal control associated with Olenekian–Anisian boundary, which is evident in a positive anom- photosynthetic activity (Folk et al., 1985; Guo and Riding, 1992; aly of d13C values of carbonate and characterizes this boundary Pentecost, 1994; Dupraz et al., 2009). Therefore, the structure is (e.g. Payne et al., 2004; Galfetti et al., 2007). considered to represent a shallow phototrophic microbialite. Ph was slightly enriched in 13C vs. Pr (Fig. 5 and Table 1). During 13 the late Early Triassic, the d C values of the C21–25 head-to-tail iso- 4.2. Unusual lipid biomarker features of the early Middle Triassic prenoid hydrocarbons were significantly higher than those of Pr microbialite and Ph (Fig. 5 and Table 1). In the early Anisian (153.1–159 m), 13 above the microbialite, the d C variation in the C21–25 regular iso- Because this microbialite is thought to be a shallow-water pho- prenoids, Pr and Ph were less significant than in horizons below totrophic microbialite (not a methane-seep microbialite), its high the microbialite (77.5–146.1 m; Fig. 5 and Table 1). Unlike in hori- relative abundance (Fig. 3C) of isoprenoids (C40 acyclic biphytane, zons below the microbialite-bearing horizon (148.1–150.1 m), the C30–39 head-to-head isoprenoids and C14–25 head-to-tail iso- 13 d C values of the C21–25 head-to-tail isoprenoid hydrocarbons in prenoids) relative to n-alkanes (derived from algae, bacteria and the microbialite did not differ much from those of Pr and Ph terrigenous plants) and MMHs (potentially derived from cyanobac- (Fig. 5 and Table 1). teria or SRB; e.g. Shiea et al., 1990; Bradley et al., 2009) was an We also investigated variation in d13C values of short chain unexpected feature. This observation distinguishes this horizon 13 n-alkanes, Pr and Ph (Fig. 6). The average d C values of C15–18 from most microbialites and from other, non-microbialite geologi- n-alkanes were subtracted from the average values for Pr and Ph cal samples, which are usually dominated by n-alkanes, as shown (Fig. 6). The resulting difference generally ranged from +4‰ to in the sediments below and above the microbialite À4‰, except for a value of +6‰ at 77.5 m (Fig. 6). The positive val- (Fig. 3A, B and D) and in the literature (e.g. Peters et al., 2005). ues occurred at depths of 77.5–139.5, 146.1 and 150.1–159 m, Among isoprenoid hydrocarbons, the head-to-head C40 biphy- whereas the negative values occurred at 142.5 and 148.1 m. tane, presumably derived from degradation of glycerol dialkyl 70 R. Saito et al. / Organic Geochemistry 85 (2015) 66–75

Fig. 4. Chromatograms and mass spectra of compounds from 146.1 m in the Chaohu section. (A–C) Total ion chromatogram (TIC) of saturated hydrocarbons, TIC after removal of n-alkanes with molecular sieve and partial ion chromatograms of m/z 309 (for lycopane) and 322 (for biphytane), respectively. (D) Mass spectrum of peak 1 in Fig. 4C (after background subtraction by using the spectrum of slope 3), assigned as lycopane. (E) Spectrum of peak 2 (after subtraction from peak 1), assigned as C40 acyclic biphytane; and

(F) Spectrum of peak 1 (after background subtraction), assigned as lycopane + C40 acyclic biphytane.

De Rosa et al., 1983; Dawson et al., 2012). Pseudohomologue series

of isoprenoid hydrocarbons (i.e. C30–40 head-to-head isoprenoids and C13–19 and C21–24 head-to-tail isoprenoids) are considered diagenetic products of isoprenoid hydrocarbons originally derived from GDGTs and DGDs (Albaiges, 1980; Rowland, 1990; Grice et al., 1998a; Birgel et al., 2006, 2008). In contrast to the sediments below the microbialite, Pr and Ph are considered to derive almost exclusively from archaea in the microbialite (Section 4.4), as indicated by isotopic relationships with other archaeal hydrocarbons. Thus, the archaeal biomass increased signiﬁcantly compared with that of cyanobacteria and bacteria, both of which presumably played an important role in phototrophic shallow water microbial mats during the formation of the microbialite (Figs. 2A and 3C, 148.1–150.1 m).

4.3. Source of isoprenoid hydrocarbons in sediments above and below Fig. 5. Stable carbon isotopic composition of C18–25 isoprenoid hydrocarbons from the microbialite upper Lower Triassic samples; reg.ix,Cx regular (head-to-tail) isoprenoid, where x is the number of carbon atoms. The source organisms of Pr and Ph in sedimentary rocks may be diverse and comprise (i) phytyl side chain of both bacterial and glycerol tetraethers (GDGTs), can be produced by numerous eukaryotic chlorophylls (Brooks et al., 1969), (ii) archaeal phytanyl archaea (e.g. De Rosa and Gambacorta, 1988; Schouten et al., chains in DGDs of euryarchaeota (e.g. halophiles and methano- 2013). The C25 head-to-tail isoprenoid is presumably derived from gens) (e.g. De Rosa and Gambacorta, 1988; Tachibana, 1994) and dialkyl glycerol diethers (DGDs) of halophilic euryarchaeota (e.g. (iii) tocopherols for Pr only (Goossens et al., 1984). The d13C values R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 71

Table 1

Carbon isotopic composition of hydrocarbons from Chaohu sections; reg.ix,Cx regular (head-to-tail) isoprenoids, where x is the number of carbons; HHix,Cx irregular (head-to- head) isoprenoids, where x is the number of carbons; C40:0 BP, C40 acyclic biphytane; C40:1 BP, C40 monocyclic biphytane (two isomers); n.m., not measured (concentration too low, excessive coelution, or below limit of detection).

Sample 77.5 m 93.1 m 110.4 m 133.2 m 139.5 m 142.5 m Compound d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r

n-C15 À32.6 0.27 À35.2 0.01 À31.9 0.00 À34.6 0.02 À32.6 0.13 37.3 0.75

n-C16 À33.3 0.01 À35.6 0.07 À31.8 0.00 À35.1 0.07 À33.4 0.07 37.0 0.13

n-C17 À30.9 0.10 À33.1 0.00 À32.8 0.10 À35.3 0.22 À34.3 0.47 36.2 0.35

n-C18 À32.7 0.23 À34.3 0.00 À34.4 0.18 À34.0 0.27 À33.0 0.33 36.6 0.00

n-C19 À33.4 0.01 À35.5 0.00 À33.2 0.03 À35.1 0.15 À33.3 0.02 35.9 0.01

n-C20 À34.3 0.03 À35.4 0.00 À33.7 0.00 À35.6 0.05 À31.5 0.10 33.5 0.01

n-C21 À34.6 0.06 À36.1 0.00 À33.6 0.01 À34.8 0.08 À31.1 0.53 34.9 0.17

n-C22 À34.8 0.06 À35.8 0.00 À33.4 0.03 À33.8 0.07 À31.3 0.00 35.5 0.01

n-C23 À35.2 0.01 À35.5 0.18 À33.7 0.01 À34.9 0.45 À32.0 0.05 35.6 0.03

n-C24 À34.7 0.02 À36.3 0.04 À35.4 0.06 À36.0 0.11 À33.0 0.02 33.0 0.19

n-C25 À34.3 0.14 À35.1 0.25 À35.0 0.61 À35.4 0.02 À33.8 0.04 32.1 0.00

n-C26 À35.2 0.01 À35.6 0.35 À34.2 0.13 À34.7 0.09 À34.8 0.43 33.8 0.06

n-C27 À35.0 0.00 À34.5 0.14 À32.5 0.05 À36.0 0.61 À31.2 0.00 35.0 0.13

n-C28 À34.6 0.05 À36.1 0.01 À35.2 0.01 À34.4 0.13 À32.0 0.03 36.1 0.48

n-C29 À35.7 0.02 À35.9 0.55 À34.0 0.14 À34.6 0.16 À33.6 0.36 37.4 0.07

n-C30 À35.2 0.02 À36.2 0.31 À36.1 0.00 À36.0 0.00 À33.5 0.00 34.0 0.00

n-C31 À35.4 0.04 À35.8 0.05 À34.7 0.14 À36.6 0.00 À33.4 0.00 33.6 0.13

n-C32 À35.5 0.01 À34.4 0.00 n.m. n.m. n.m. n.m. À33.4 0.00 34.4 0.08

n-C33 À34.3 0.05 À32.7 0.13 n.m. n.m. n.m. n.m. À31.3 0.00 35.7 0.09

n-C34 À35.6 0.02 n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. 35.8 0.03

n-C35 À34.8 0.29 n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. 33.7 0.00

n-C36 À34.7 0.37 n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. Norpristane À32.0 0.02 À34.4 0.12 À35.0 0.01 À33.9 0.00 À34.3 0.10 À30.9 0.47 Pr À38.0 0.11 À38.5 0.08 À36.4 0.04 À36.7 0.01 À37.2 0.00 À37.0 0.19 Ph À38.8 0.01 À37.9 0.03 À35.0 0.01 À36.7 0.00 À35.4 0.00 À33.5 0.06

reg.i21 n.m. n.m. À32.7 0.11 À32.3 0.26 À33.5 0.11 n.m. n.m. À32.6 0.01

reg.i22 n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. n.m. À34.2 0.35

reg.i23 À32.4 0.06 À33.7 0.16 À31.3 0.19 À31.5 0.21 À29.4 0.28 À33.3 0.08

reg.i24 n.m. n.m. À30.7 0.08 n.m. n.m. n.m.

reg.i25 À33.0 0.00 À34.1 0.58 À30.4 0.00 À33.3 0.00 À28.8 0.03 À31.9 0.19

HHi29 n.m. n.m. n.m. n.m. n.m. n.m.

HHi31 n.m. n.m. n.m. n.m. n.m. n.m.

HHi32 n.m. n.m. n.m. n.m. n.m. n.m.

HHi33 n.m. n.m. n.m. n.m. n.m. n.m.

HHi34 n.m. n.m. n.m. n.m. n.m. n.m.

HHi35 n.m. n.m. n.m. n.m. n.m. n.m.

HHi36 n.m. n.m. n.m. n.m. n.m. n.m.

HHi37 n.m. n.m. n.m. n.m. n.m. n.m.

HHi38 n.m. n.m. n.m. n.m. n.m. n.m.

HHi39 n.m. n.m. n.m. n.m. n.m. n.m.

C40:0BP n.m. n.m. n.m. n.m. n.m. n.m.

C40:1BP n.m. n.m. n.m. n.m. n.m. n.m.

C40:1BP n.m. n.m. n.m. n.m. n.m. n.m. Sample 146.1 m 148.1 m 150.1 m 153.1 m 159 m Compound d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r

n-C15 À36.0 – À35.9 0.07 À28.3 0.05 À26.1 0.0 À29.1 0.3

n-C16 À33.7 – À33.5 0.19 À29.9 0.48 À26.4 0.0 À29.9 0.3

n-C17 À33.0 – n.m. n.m. À27.3 0.0 À30.7 0.1

n-C18 À34.3 – n.m. n.m. À28.0 0.0 À30.9 0.0

n-C19 À32.8 – n.m. n.m. À28.9 0.0 À31.3 0.0

n-C20 À34.0 – n.m. n.m. À29.3 0.2 À30.4 0.2

n-C21 À34.5 – n.m. n.m. À30.1 0.3 À31.8 0.1

n-C22 À34.7 – n.m. n.m. À30.9 0.4 À31.5 0.3

n-C23 À36.2 – n.m. n.m. À31.4 0.2 À33.6 0.2

n-C24 À34.2 – 32.6 0.01 n.m. À31.0 0.0 À33.3 0.2

n-C25 À35.4 – 32.3 0.00 n.m. À31.1 0.0 À32.3 0.0

n-C26 À33.6 – n.m. n.m. À32.0 0.1 À33.4 0.3

n-C27 À35.4 – n.m. n.m. À32.1 0.0 À33.6 0.1

n-C28 À34.9 – n.m. n.m. À32.1 0.1 À32.6 0.0

n-C29 À31.1 – n.m. n.m. À32.0 0.2 À32.5 0.4

n-C30 À34.9 – n.m. n.m. À31.5 0.1 À31.6 0.0

n-C31 À35.0 – n.m. n.m. À32.3 0.1 À32.3 0.5

n-C32 À35.0 – n.m. n.m. À32.0 0.0 À31.5 0.3

n-C33 À33.2 – n.m. n.m. À31.6 0.3 À31.8 0.1

n-C34 n.m. n.m. n.m. À31.7 0.0 À30.5 0.1

(continued on next page) 72 R. Saito et al. / Organic Geochemistry 85 (2015) 66–75

Table 1 (continued)

Sample 146.1 m 148.1 m 150.1 m 153.1 m 159 m Compound d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r d13C(‰) r

n-C35 n.m. n.m. n.m. À30.5 0.0 n.m.

n-C36 n.m. n.m. n.m. n.m. n.m. Norpristane À33.2 – À32.0 0.42 À31.1 0.45 À27.5 0.1 À30.8 0.1 Pr À35.6 – À31.3 0.04 À30.4 0.06 À30.3 0.0 À32.4 0.0 Ph À34.4 – À30.9 0.00 À29.5 0.04 À28.4 0.0 À30.6 0.1

reg.i21 À33.1 – À31.1 0.04 À29.9 0.55 À27.0 0.3 À28.5 0.0

reg.i22 n.m. À33.2 0.43 À29.7 0.16 À26.7 0.0 À26.3 0.0

reg.i23 À30.4 – À30.8 0.33 À28.2 0.01 À27.2 0.2 À28.7 0.4

reg.i24 À28.8 – À30.8 0.28 À29.9 0.05 À26.7 0.0 À29.3 0.1

reg.i25 À29.1 – À30.5 0.23 À30.5 0.04 À25.8 0.2 À28.6 0.1

HHi29 n.m. À33.8 0.01 n.m. n.m. n.m.

HHi29 n.m. n.m. n.m. n.m. n.m.

HHi31 n.m. À34.9 0.03 n.m. n.m. n.m.

HHi32 n.m. À34.7 0.06 n.m. n.m. n.m.

HHi33 n.m. À34.2 0.03 n.m. n.m. n.m.

HHi33 n.m. À34.2 0.04 n.m. n.m. n.m.

HHi34 n.m. À34.3 0.06 À31.1 0.10 n.m. n.m.

HHi35 n.m. À35.9 0.00 n.m. n.m. n.m.

HHi35 n.m. À33.4 0.00 n.m. n.m. n.m.

HHi36 n.m. À34.9 0.01 n.m. n.m. n.m.

HHi37 n.m. À34.6 0.08 À29.6 0.51 n.m. n.m.

HHi38 n.m. À34.8 0.02 À30.2 0.00 n.m. n.m.

HHi38 n.m. À34.9 0.02 n.m. n.m. n.m.

HHi39 n.m. À35.1 0.16 À30.9 0.01 n.m. n.m.

C40:0BP n.m. À34.7 0.01 À29.8 0.19 n.m. n.m.

C40:1BP n.m. À35.0 0.05 n.m. n.m. n.m.

C40:1BP n.m. À35.3 0.18 n.m. n.m. n.m.

13 13 13 Fig. 6. Dd = (average d Cofn-C15–18) À (average d CofPr+d C of Ph) from upper Lower Triassic samples. The sample names (e.g. 77.5 m) correspond to their height in the stratigraphic column in Fig. 2.

of Pr are lower than those of Ph (Fig. 5 and Table 1), which might 2008). Their d13C values (or their Dd13C values in relation to other occur naturally due to the intramolecular isotopic heterogeneity compounds) can give insight into archaeal sources and their possi- of the parent compound, phytol, during loss of a C atom (cf. ble metabolism or carbon source (e.g. Grice et al., 1998a; Pancost Schouten et al., 2008); an analogous effect has been observed for et al., 2001; Schouten et al., 2001; Birgel et al., 2006, 2008, 2014; 6,10,14-trimethylpentadecan-2-one, which was depleted in 13C Stadnitskaia et al., 2008). Methanotrophic archaea can, however, relative to its parent compound, phytol, by 1–4‰ (cf. Schouten be definitely excluded as source organisms, on the basis of the et al., 2008). d13C values of archaeal hydrocarbons. In non-microbialite layers, 13 Plausible source organisms for the C21–25 head-to-tail linked C21–25 head-to-tail isoprenoid hydrocarbons are enriched in C isoprenoid hydrocarbons are halophilic archaea (e.g. De Rosa relative to Pr and Ph. This suggests the main source organisms of et al., 1983; Grice et al., 1998a; Dawson et al., 2012) or methan- the two groups of isoprenoid hydrocarbon are different. In addi- otrophic archaea (Birgel et al., 2006, 2008; Stadnitskaia et al., tion, the chromatograms from the non-microbialite layers show a R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 73 dominance of n-alkanes derived from higher plants, marine algae n-alkanes in the microbialite. As a consequence, we could not and bacteria (Fig. 3A, B and D). These lines of evidence suggest that apply the formula introduced by Grice et al. (2005) and 13 the main source organisms for Pr and Ph were likely phototrophs, Nabbefeld et al. (2010) – (average d Cofn-C17–18 alkanes) À (aver- 13 whereas those of the C21–25 head-to-tail isoprenoids were halophi- age d C of pristane + phytane) – through the stratigraphic 13 lic archaea. sequence. However, we could measure the d C values of C15 and C16 n-alkanes in the microbialite. As a result, we extended the 4.4. Source of isoprenoid hydrocarbons in the microbialite range of the carbon atoms to 15, and used the formula: (average 13 13 13 d Cofn-C15–18) À (average d CofPr+d C of Ph). The positive In contrast to all other samples, Pr and Ph contents are greater values (1.4–6‰) in the horizons below (77.5–139.5 m) and above than all other compounds. Similarly high contents are reported in (153.1–159 m) the microbialite indicate more vigorous hetero- euxinic environments due to sulfurization of functionalized lipids trophic activity and/or greater input of heavy bacterial biomass (cf. Keely et al., 1993; Kenig et al., 1995; Grice et al., 1996, during these intervals (Fig. 6). In contrast, the low to negative val- 1998a,b; Sepúlveda et al., 2009). Among others, Sepúlveda et al. ues (À3.6‰ to 0.8‰) in the photic zone euxinia horizons (Saito (2009) proposed that such high concentrations of Pr and Ph are et al., 2014) and the microbialite at 142.5–150.1 m indicate more attributable to a high productivity of phototrophic organisms in intense photosynthetic activity during these intervals (Fig. 6). their study due to the absence of other archaeal lipid biomarkers. However, as stated above, the main sources of Pr and Ph in the This observation contrasts, however, with our observations, where microbialite-bearing horizon (148.1–150.1 m) are considered to be the high content of Pr and Ph in the microbialite (Fig. 3C) was halophilic archaea, and the formula and its interpretation (more accompanied by a high content of head-to-tail C21–25 isoprenoid vigorous photosynthesis) might not be applied for this interval. 13 hydrocarbons. Further, the Dd C between Pr, Ph and the C21–25 isoprenoid hydrocarbons are minor (Fig. 5 and Table 1); and the 4.6. Microbialite occurrence within the Early Triassic succession concentration of n-alkanes (from algae, terrestrial plants, cyanobacteria and bacteria) are negligible compared with The occurrence of the microbialite in a shallow water environ- archaeal-derived isoprenoid hydrocarbons (C , biphytanes 21–25 ment in the latest Early Triassic at the Chaohu section corresponds and their derivatives; Fig. 3C). Therefore, potential source organ- to the latest of the four events described in the Early Triassic isms are also considered to be halophilic archaea. marked by microbialites and other unusual sedimentary structures It is more difficult to determine the archaeal sources of biphy- (cf. Baud et al., 2007). At the Chaohu sections, the environments tanes and their pseudo homologues in the microbialite. Since during the formation of the microbialite were marked by high d13C values were available only for two samples for biphytanes salinity and strongly reducing conditions, evidenced by a domi- and varied significantly, in contrast to the C and C isoprenoids, 20 25 nance of halophilic archaea (Section 4.4) and high concentration an assignment to a specific source is difficult (Table 1). A second of dibenzothiophenes (Fig. 2; Saito et al., 2014), respectively. In complication is that most archaeal strains contain GDGTs, except addition, vigorous photosynthetic activity possibly occurred during for Halobacteriales (halophilic archaea; see Schouten et al., 2013 the formation of the microbialite (Section 4.5). In addition to an and references therein). There are some isotope data for biphy- influence from global-scale environmental oscillations, such as tanes and a few interpretations for source archaea for the biphy- the intrusion of the deep alkaline water (rich in H2S and nutrients) tanes from various sites in the Mesozoic (Kuypers et al., 2001; during the latest Early Triassic, the local high salinity and reducing Birgel et al., 2006; Heindel et al., 2013). Isotope values of À35‰ conditions would reduce the activity of metazoans. Furthermore, to À30‰ for the biphytanes in the microbialite suggest neither the vigorous photosynthetic activity would increase the local alka- methanotrophic archaea (À72‰ to À105‰; Birgel et al., 2006) linity. The suppression of metazoan activity and increase in alka- nor marine planktonic archaea (around À20‰; Kuypers et al., linity ultimately would facilitate microbial formation of the 2001; Schouten et al., 2013 and references therein). Heindel et al. microbialite at the Chaohu sections. (2013) reported similar d13C values for À29‰ to À32‰ for biphy- Although the abundance of non-isoprenoid saturated hydrocar- tanes in the Lower Triassic microbialites and proposed that the bons (derived partly from cyanobacteria and SRB), such as archaeal sources of the biphytanes most likely include benthic, n-alkanes and the MMHs, is much smaller than that of the archaeal possibly methanogenic, archaea in addition to planktonic archaea. hydrocarbons in the microbialite (Fig. 3C), their presence could still Similarly, d13C values of À35‰ to À30‰ for the biphytanes in the imply that cyanobacteria and SRB played an important role in the microbialite here might suggest that the archaeal sources of the formation of the microbialite during archaeal blooming under the biphytanes include both benthic and planktonic archaea. high alkalinity and reduced metazoan activity conditions. A potential role of archaea in the formation of the microbialite is enig- 4.5. Heterotrophs vs. phototrophs during the late Early Triassic matic. Archaea are a minor constituent (ca. 10%) of modern phototrophic microbial mats (Papineau et al., 2005). In addition, The stratigraphic distribution of the differences in the d13C val- little is known about the metabolic diversity of archaea, and there ues of the n-alkanes, Pr and Ph (Fig. 6) reflects the different modes are many uncultivated archaea and bacteria with entirely of carbon cycling through the late Early Triassic–early Middle unknown function (i.e. the so-called ‘microbial dark matter’; Triassic. The n-alkanes are derived mainly from phototrophs and Rinke et al., 2013). Therefore, assessing their potential roles is dif- heterotrophs, and their d13C values are the weighted averages of ficult, even in modern stromatolites (Papineau et al., 2005). phototrophic and heterotrophic communities (Grice et al., 2005). If Pr and Ph are derived mainly from primary producers that use the classical mevalonate pathway, then their carbon isotope values 5. Conclusions should be enriched in d13C by ca. 1.5‰ relative to those of the

C14–18 n-alkanes (Hayes, 1993; Schouten et al., 1998; Nabbefeld et al., We have demonstrated that the studied microbialite can be 2010). However, if the C14–18 n-alkanes are derived mainly from classified as a stromatolite, and the irregular lamination suggests heterotrophs that utilize primary photosynthates or isotopically that it was formed through biological processes such as photosyn- heavy bacterial biomass, Pr and Ph should be depleted in 13C rela- thetic activity. We have shown that it contains much higher con- tive to the short chain n-alkanes (Grice et al., 2005). Due to the low centrations of archaeal hydrocarbons than n-alkanes. The 13 content, we could not measure the d C values of C17 and C18 predominance of archaeal hydrocarbons in this microbialite 74 R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 possibly suggests a significant mechanistic role of archaea in its Harris, P.M. (Eds.), Carbonate Cements. SEPM Special Publications 36, pp. 349– formation. It was formed just after a photic zone euxinic event 369. Galfetti, T., Bucher, H., Brayard, A., Hochuli, P.A., Weissert, H., Guodun, K., Atudorei, and an interval of vigorous anoxygenic photosynthetic activity. V., Guex, J., 2007. Late Early Triassic climate change: insights from carbonate The shallow environment in which it was formed had high salinity carbon isotopes, sedimentary evolution and ammonoid paleobiogeography. and reducing conditions, perhaps accompanied by vigorous photo- Palaeogeography, Palaeoclimatology, Palaeoecology 243, 394–411. Goedert, J.L., Thiel, V., Schmale, O., Rau, W.W., Michaelis, W., Peckmann, J., 2003. The synthetic activity. These conditions would have increased the local Late Eocene ‘Whiskey Creek’ methane-seep deposit (western Washington alkalinity and reduced the numbers of metazoans and thus facili- State). Facies 48, 223–239. tated the formation of the microbialite. Goossens, H., de Leeuw, J.W., Schenck, P.A., Brassell, S.C., 1984. Tocopherols as likely precursors of pristane in ancient sediments and crude oils. Nature 312, 440– 442. Acknowledgments Greenwood, P.F., Summons, R.E., 2003. GC–MS detection and significance of crocetane and pentamethylicosane in sediments and crude oils. Organic Geochemistry 34, 1211–1222. This work was supported by a Global Centre of Excellence Grice, K., Schaeffer, P., Schwark, L., Maxwell, J.R., 1996. Molecular indicators of Program on Global Education and Research at the Centre for palaeoenvironmental conditions in an immature Permian shale (Kupferschiefer, Earth and Planetary Dynamics, Tohoku University (led by E. Lower Rhine Basin, north-west Germany) from free and S-bound lipids. Organic Ohtani) and was financed by the Ministry of Education, Culture, Geochemistry 25, 131–147. Grice, K., Schouten, S., Nissenbaum, A., Charrach, J., Sinninghe Damsté, J.S., 1998a.

Sports, Science, and Technology, Japan, JSPS KAKENHI Grant Isotopically heavy carbon in the C21 to C25 regular isoprenoids in halite-rich Number (251482), the National Science Foundation of China deposits from the Sdom Formation, Dead Sea Basin, Israel. Organic (Grant Nos. 41172312, 41272372) and the ‘‘111’’ project (Grant Geochemistry 28, 349–359. Grice, K., Schouten, S., Peters, K.E., Sinninghe Damsté, J.S., 1998b. Molecular isotopic No. B08030). We thank D. Birgel and an anonymous reviewer for characterisation of hydrocarbon biomarkers in Palaeocene-Eocene evaporitic, constructive comments. lacustrine source rocks from the Jianghan Basin, China. Organic Geochemistry 29, 1745–1764. Grice, K., Cao, C., Love, G.D., Böttcher, M.E., Twitchett, R.J., Grosjean, E., Summons, Associate Editor—K.U. Hinrichs R.E., Turgeon, S.T., Dunning, W., Jin, Y., 2005. Photic zone euxinia during the Permian-Triassic superanoxic event. Science 307, 706–709. Grotzinger, J.P., Knoll, A.H., 1995. Anomalous carbonate precipitates: is the References Precambrian the key to the Permian? Palaios 10, 578–596. Guo, L., Riding, R., 1992. Aragonite laminae in hot water travertine crusts, Rapolano Terme, Italy. Sedimentology 39, 1067–1079. Albaiges, J., 1980. Identification and geochemical significance of long chain acyclic Hayes, J.M., 1993. Factors controlling 13C contents of sedimentary organic isoprenoid hydrocarbons in crude oils. Physics and Chemistry of the Earth 12, compounds: principles and evidence. Marine Geology 113, 111–125. 19–28. Heindel, K., Richoz, S., Birgel, D., Brandner, R., Klügel, A., Krystyn, L., Baud, A., Allen, M.A., Neilan, B.A., Burns, B.P., Jahnke, L.L., Summons, R.E., 2010. Lipid Horacek, M., Mohtat, T., Peckmann, J., 2013. Biogeochemical formation of calyx- biomarkers in Hamelin Pool microbial mats and stromatolites. Organic shaped carbonate crystal fans in the subsurface of the Early Triassic seafloor. Geochemistry 41, 1207–1218. Gondwana Research 27, 840–861. Atudorei, V., Baud, A., Crasquin-Soleau, S., Galbrun, B., Gradinaru, E., Mirauta, E., Keely, B.J., Sinninghe Damste, J.S., Betts, S.E., Yue, L., de Leeuw, J.W., Maxwell, J.R., Renard, M., Zerrari, S., 1997. Extended scientific report of the Peri-Tethys 1993. A molecular stratigraphic approach to palaeoenvironmental assessment project. In: Baud, A. (Ed.), The Triassic of North Dobrogea. Geological Museum and the recognition of changes in source inputs in marls of the Mulhouse Basin Lausanne, Switzerland, p. 64. (Alsace, France). Organic Geochemistry 20, 1165–1186. Awramik, S.M., 1971. Precambrian columnar stromatolite diversity: reflection of Kenig, F., Sinninghe Damsté, J.S., Frewin, N.L., Hayes, J.M., De Leeuw, J.W., 1995. metazoan appearance. Science 174, 825–827. Molecular indicators for palaeoenvironmental change in a Messinian evaporitic Awramik, S.M., 1992. The history and significance of stromatolites. In: Schidlowski, sequence (Vena del Gesso, Italy). II. High-resolution variations in abundances M., Kimberley, M.M., McKirdy, D.M., Trudinger, P.A. (Eds.), Early Organic and 13C contents of free and sulphur-bound carbon skeletons in a single marl Evolution: Implications for Energy and Mineral Resources. Springer, Berlin, bed. Organic Geochemistry 23, 485–526. pp. 435–449. Keupp, H., Jenisch, A., Herrmann, R., Neuweiler, F., Reitner, D.D.J., 1993. Microbial Baud, A., Richoz, S., Pruss, S., 2007. The lower Triassic anachronistic carbonate facies carbonate crusts-a key to the environmental analysis of fossil spongiolites? in space and time. Global and Planetary Change 55, 81–89. Facies 29, 41–54. Birgel, D., Thiel, V., Hinrichs, K.-U., Elvert, M., Campbell, K.A., Reitner, J., Farmer, J.D., Kuypers, M.M., Blokker, P., Erbacher, J., Kinkel, H., Pancost, R.D., Schouten, S., Peckmann, J., 2006. Lipid biomarker patterns of methane-seep microbialites Damsté, J.S.S., 2001. Massive expansion of marine archaea during a mid- from the Mesozoic convergent margin of California. Organic Geochemistry 37, Cretaceous oceanic anoxic event. Science 293, 92–95. 1289–1302. Malinski, E., Gasiewicz, A., Witkowski, A., Szafranek, J., Pihlaja, K., Oksman, P., Birgel, D., Himmler, T., Freiwald, A., Peckmann, J., 2008. A new constraint on the Wiinamäki, K., 2009. Biomarker features of sabkha-associated microbialites antiquity of anaerobic oxidation of methane: late Pennsylvanian seep from the Zechstein Platy Dolomite (Upper Permian) of northern Poland. limestones from southern Namibia. Geology 36, 543–546. Palaeogeography, Palaeoclimatology, Palaeoecology 273, 92–101. Birgel, D., Guido, A., Liu, X., Hinrichs, K.U., Gier, S., Peckmann, J., 2014. Hypersaline Murphy, M.T.J., 1969. Analytical methods. In: Eglinton, G., Murphy, M.T.J. (Eds.), conditions during deposition of the Calcare di Base revealed from archaeal di- Organic Geochemistry. Springer, Berlin, pp. 74–88. and tetraether inventories. Organic Geochemistry 77, 11–21. Nabbefeld, B., Grice, K., Twitchett, R.J., Summons, R.E., Hays, L., Böttcher, M.E., Asif, Bradley, A.S., Fredricks, H., Hinrichs, K.U., Summons, R.E., 2009. Structural diversity M., 2010. An integrated biomarker, isotopic and palaeoenvironmental study of diether lipids in carbonate chimneys at the Lost City Hydrothermal Field. through the Late Permian event at Lusitaniadalen, Spitsbergen. Earth and Organic Geochemistry 40, 1169–1178. Planetary Science Letters 291, 84–96. Brooks, J.D., Gould, K., Smith, J., 1969. Isoprenoid hydrocarbons in coal and Oba, M., Sakata, S., Tsunogai, U., 2006. Polar and neutral isopranyl glycerol ether petroleum. Nature 222, 257–259. lipids as biomarkers of archaea in near-surface sediments from the Nankai Chen, Z.Q., Tong, J., Fraiser, M.L., 2011. Trace fossil evidence for restoration of Trough. Organic Geochemistry 37, 1643–1654. marine ecosystems following the end-Permian mass extinction in the Lower Pancost, R.D., Telnæs, N., Sinninghe Damsté, J.S., 2001. Carbon isotopic composition Yangtze region, South China. Palaeogeography, Palaeoclimatology, of an isoprenoid-rich oil and its potential source rock. Organic Geochemistry 32, Palaeoecology 299, 449–474. 87–103. Dawson, K.S., Freeman, K.H., Macalady, J.L., 2012. Molecular characterization of core Papineau, D., Walker, J.J., Mojzsis, S.J., Pace, N.R., 2005. Composition and structure lipids from halophilic archaea grown under different salinity conditions. of microbial communities from stromatolites of Hamelin Pool in Shark Organic Geochemistry 48, 1–8. Bay, Western Australia. Applied and Environmental Microbiology 71, De Rosa, M., Gambacorta, A., 1988. The lipids of archaebacteria. Progress in Lipid 4822–4832. Research 27, 153–175. Payne, J.L., Lehrmann, D.J., Wei, J., Orchard, M.J., Schrag, D.P., Knoll, A.H., 2004. Large De Rosa, M., Gambacorta, A., Nicolaus, B., Grant, W.D., 1983. A C ,C diether core 25 25 perturbations of the carbon cycle during recovery from the end-Permian lipid from archae-bacterial haloalkaphiles. Journal of General Microbiology 129, extinction. Science 305, 506–509. 2333–2337. Peckmann, J., Thiel, V., Michaelis, W., Clari, P., Gaillard, C., Martire, L., Reitner, J., Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S., Visscher, P.T., 2009. 1999. Cold seep deposits of Beauvoisin (Oxfordian; southeastern France) and Processes of carbonate precipitation in modern microbial mats. Earth-Science Marmorito (Miocene; northern Italy): microbially induced authigenic Reviews 96, 141–162. carbonates. International Journal of Earth Sciences 88, 60–75. Fischer, A.G., 1965. NAS symposium on the evolution of the earth’s atmosphere: Peckmann, J., Birgel, D., Kiel, S., 2009. Molecular fossils reveal fluid composition and fossils, early life, and atmospheric history. Proceedings of the National Academy flow intensity at a Cretaceous seep. Geology 37, 847–850. of Sciences of the United States of America 53, 1205. Pentecost, A., 1994. Formation of laminate travertines at Bagno Vignone, Italy. Folk, R.L., Chafetz, H.S., Tiezzi, P.A., 1985. Bizarre forms of depositional and Geomicrobiology Journal 12, 239–251. diagenetic calcite in hotspring travertines, central Italy. In: Scheiderman, N., R. Saito et al. / Organic Geochemistry 85 (2015) 66–75 75

Peters, K.E., Walters, C.C., Moldowan, J.M., 2005. The Biomarker Guide. Cambridge Schouten, S., Hopmans, E.C., Sinninghe Damsté, J.S., 2013. The organic geochemistry University Press, Cambridge, UK, pp. 3–471. of glycerol dialkyl glycerol tetraether lipids: a review. Organic Geochemistry 54, Pruss, S.B., Bottjer, D.J., 2004. Late Early Triassic microbial reefs of the western 19–61. United States: a description and model for their deposition in the aftermath of Sepúlveda, J., Wendler, J., Leider, A., Kuss, H.J., Summons, R.E., Hinrichs, K.U., 2009. the end-Permian mass extinction. Palaeogeography, Palaeoclimatology, Molecular isotopic evidence of environmental and ecological changes across the Palaeoecology 211, 127–137. Cenomanian–Turonian boundary in the Levant Platform of central Jordan. Pruss, S.B., Bottjer, D.J., 2005. The reorganization of reef communities following the Organic Geochemistry 40, 553–568. end-Permian mass extinction. Comptes Rendus Palevol 4, 553–568. Shiea, J., Brassell, S.C., Ward, D.M., 1990. Mid-chain branched mono- and dimethyl Pruss, S.B., Corsetti, F.A., Bottjer, D.J., 2005. The unusual sedimentary rock record of alkanes in hot spring cyanobacterial mats: a direct biogenic source for branched the Early Triassic: a case study from the southwestern United States. alkanes in ancient sediments? Organic Geochemistry 15, 223–231. Palaeogeography, Palaeoclimatology, Palaeoecology 222, 33–52. Sinninghe Damsté, J.S., Kuypers, M.M., Schouten, S., Schulte, S., Rullkötter, J., 2003.

Riding, R., 2006. Microbial carbonate abundance compared with fluctuations The lycopane/C31 n-alkane ratio as a proxy to assess palaeoxicity during in metazoan diversity over geological time. Sedimentary Geology 185, sediment deposition. Earth and Planetary Science Letters 209, 215–226. 229–238. Song, H., Tong, J., Algeo, T., Horacek, M., Qiu, H., Song, H., Tian, L., Chen, Z.-Q., 2013. 13 Riding, R., 2011. The nature of stromatolites: 3500 million years of history and a Large vertical CDIC gradients in Early Triassic seas of the South China craton: century of research. In: Reitner, J., Trauth, M.H., Stüwe, K., Yuen, D. (Eds.), implications for oceanographic changes related to Siberian Traps volcanism. Advances in Stromatolite Geobiology. Springer, Berlin Heidelberg, pp. 29–74. Global and Planetary Change 105, 7–20. Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N.N., Anderson, I.J., Cheng, J.F., Stadnitskaia, A., Bouloubassi, I., Elvert, M., Hinrichs, K.U., Sinninghe Damsté, J.S., Darling, A., Malfatti, S., Swan, B.K., Gies, E.A., Dodsworth, J.A., Hedlund, B.P., 2008. Extended hydroxyarchaeol, a novel lipid biomarker for anaerobic Tsiamis, G., Sievert, S.M., Liu, W.-T., Eisen, J.A., Hallam, S.J., Kyrpides, N.C., methanotrophy in cold seepage habitats. Organic Geochemistry 39, 1007–1014. Stepanauskas, R., Rubin, E.M., Hugenholtz, P., Woyke, T., 2013. Insights into the Tachibana, A., 1994. A novel prenyltransferase, farnesylgeranyl diphosphate phylogeny and coding potential of microbial dark matter. Nature 499, 431–437. synthase, from the haloalkaliphilic archaeon, Natronobacterium pharaonis. Rowland, S.J., 1990. Production of acyclic isoprenoid hydrocarbons by laboratory FEBS Letters 341, 291–294. maturation of methanogenic bacteria. Organic Geochemistry 15, 9–16. Thiel, V., Peckmann, J., Seifert, R., Wehrung, P., Reitner, J., Michaelis, W., 1999. Saito, R., Oba, M., Kaiho, K., Schaeffer, P., Adam, P., Takahashi, S., Nara-Watanabe, F., Highly isotopically depleted isoprenoids: molecular markers for ancient Chen, Z.-Q., Tong, J., Tsuchiya, N., 2014. Extreme euxinia just prior to the Middle methane venting. Geochimica et Cosmochimica Acta 63, 3959–3966. Triassic biotic recovery from the latest Permian mass extinction. Organic Thiel, V., Peckmann, J., Richnow, H.H., Luth, U., Reitner, J., Michaelis, W., 2001. Geochemistry 73, 113–122. Molecular signals for anaerobic methane oxidation in Black Sea seep carbonates Schouten, S., Klein Breteler, W.C.M., Blokker, P., Schogt, N., Rijpstra, W.I.C., Grice, K., and a microbial mat. Marine Chemistry 73, 97–112. Baas, M., Sinninghe Damsté, J.S., 1998. Biosynthetic effects on the stable carbon Tong, J., Zhao, L., 2005. Triassic in Chaohu, Anhui Province guide to the mid- isotopic compositions of algal lipids: implications for deciphering the carbon symposium field excursion of the international symposium on the Triassic isotopic biomarker record. Geochimica et Cosmochimica Acta 62, 1397–1406. chronostratigraphy and biotic recovery (23–25 May 2005, Chaohu, China). Schouten, S., Hartgers, W.A., Lopez, J.F., Grimalt, J.O., Sinninghe Damsté, J.S., 2001. A Albertiana 33, 129–138. molecular isotopic study of 13C-enriched organic matter in evaporitic deposits: Woods, A.D., Bottjer, D.J., Mutti, M., Morrison, J., 1999. Lower Triassic large sea-floor

recognition of CO2-limited ecosystems. Organic Geochemistry 32, 277–286. carbonate cements: their origin and a mechanism for the prolonged biotic Schouten, S., Özdirekcan, S., van der Meer, M.T., Blokker, P., Baas, M., Hayes, J.M., recovery from the end-Permian mass extinction. Geology 27, 645–648. Sinninghe Damste, J.S., 2008. Evidence for substantial intramolecular Zhao, L., Orchard, M.J., Tong, J., Sun, Z., Zuo, J., Zhang, S., Yun, A., 2007. Lower Triassic heterogeneity in the stable carbon isotopic composition of phytol in conodont sequence in Chaohu, Anhui Province China and its global correlation. photoautotrophic organisms. Organic Geochemistry 39, 135–146. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 24–38.