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Monoaromatic, Diaromatic, Triaromatic, and Tetraaromatic Hopanes in Kukersite Shale and Their Stable Carbon Isotopic Composition Jing Liao,†,‡ Hong Lu,*,† Guoying Sheng,† Ping’an Peng,† and Chang Samuel Hsu*,§,∇,⊥ †
State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, People’s Republic of China ‡ University of Chinese Academic of Sciences, Beijing 100049, People’s Republic of China § Department of Chemical and Biomedical Engineering, Florida A&M University/Florida State University, Tallahassee, Florida 32310, United States ∇ State Key Laboratory of Heavy Oil Processing, China University of Petroleum, Beijing, 102249 China ⊥ Petro Bio Oil Consulting, Tallahassee, Florida 32312, United States ABSTRACT: Abundant monoaromatic, diaromatic, triaromatic, and tetraaromatic hopanes as well as benzohopanes occurred in the Ordovician Estonia Kukersite shale. They were present in sufficient concentrations for reliable stable carbon isotopic composition measurements. There was almost no difference between steroids and monoaromatic steranes, but 13C enrichments of 2‰−4‰ were observed in aromatized hopanes, compared with hopanoids. Regular hopanes (C27−C35) generally are proposed to be sourced from the bacteriohopanetetraols (C35), while aromatic hopanes were derived from the diplopterol and/or diploptenes (both C30). Hopanoids were aromatized via a progressive pathway from the D-ring to the A-ring with increasing aromaticity, with successive losses of four angular methyl groups on the A-, B-, C-, and D-rings, as well as one of the gemdimethyl groups at C-4 (i.e., C-23 and C-24). Thus, different hopanoid precursors with their own δ13C values as well as the successive losses of up to five carbon atoms in the aromatization pathway help to explain the ca. 2‰−4‰ 13C isotopic enrichment in the aromatized hopanes, relative to the nonaromatized hopanoids in the Kukersite shale. In contrast, the angular methyl group at C-18 in the steroid nucleus is not removed but migrated to C-17 in the formation of the C-ring monoaromatic steranes. Moreover, more rearrangement (75%) and less aromatization (25%), mainly for the formation of the C-ring aromatic steranes, occurred in steroid compounds. Thus, the δ13C values of the C-ring monoaromatic steranes exhibit no significant difference from those of the diasterenes in Kukersite shale. These monoaromatic, diaromatic, triaromatic, and tetraaromatic hopanes, as well as benzohopanes, in the Estonia Kukersite shale were the microbially mediated aromatization products of hopanoids in the early diagenetic stage. Their precursors of diplopterol or diploptene and abundant methylhopanes found in this study strongly indicate that cyanobacteria that previously had been suggested to have colonized with Gloeocapsomorpha prisca, was probably responsible for the microbially mediated aromatization.
1. INTRODUCTION Studies of the occurrence of aromatic compounds in geological samples can help elucidate source input, age, maturation, depositional environment, and microbial alteration, because organisms do not biosynthesize aromatic compounds in appreciable quantities. Aromatization during diagenesis may significantly alter the structures of these precursor compounds through alkylation, dealkylation (demethylation), isomerization, and ring opening.1−5 The transformation mechanism was suggested to be either microbial in the initial stages of diagenesis, or diagenetic during subsequent burial in which the precursors experienced the effects of temperature, pressure, and catalytic action of the mineral surroundings.2,6,7 Aromatization pathways are closely dependent on the specific structural features of the precursors.8,9 Three pathways have been elucidated for common biological markers in geological samples: (i) Steroid aromatization starting at the C-ring and progressing to the A-ring; at higher temperature they lose side chains, with subsequent cracking to form mainly 1,2dimethylphenanthrenes.10−13 © 2015 American Chemical Society
(ii) Aromatization of hopanoids proceeding via diagenetic alteration or binding of the precursors (e.g., diploptene to neohopene with bacteriohopanetetraol) and successive dehydrogenation from the D-ring to the A-ring.14−16 (iii) Aromatization of higher-plant triterpenoids (terrigenous source), generally commencing at the A-ring, and progressing to the E-ring either directly or after loss of the A-ring, because of initial photochemical or thermochemical reactions.8,9,17−19 The stable carbon isotopic composition of organic compounds is dependent basically on their origin and fate in the sedimentary environment.20,21 Stable carbon isotopic fractionation might be associated with diagenetic aromatization and thus their δ13C values could be correlated with the extent of aromatization. Freeman et al.22 investigated the stable carbon isotopic composition of hydrocarbons in the Eocene Messel shale, attempting to use the number of double bonds as the Received: January 18, 2015 Revised: April 27, 2015 Published: April 28, 2015 3573
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2.2. Instrumental Analysis. Gas chromatography−mass spectroscopy (GC-MS) analyses of the saturated and aromatic fractions were performed using a Thermo DSQII mass spectrometer interfaced with Trace Ultra GC instrument. A HP-5 column (30 m × 0.25 mm i.d. × 0.25 μm film thickness) was used. MS analysis was conducted in full scan mode to obtain mass spectra for interpretation. Tentative assignment for aromatic hopanes was based on the published mass spectra provided mainly by Greiner et al.14,15 GC-irMS analysis was performed on the saturated and aromatic hydrocarbon fractions for compound-specific stable carbon isotopic composition measurements. It was conducted using an Isoprime irMS instrument interfaced to a HP6890 GC instrument via a combustion interface. A HP-5 column (30 m × 0.32 mm i.d. × 0.25 μm film thickness) was used for chromatographic separation. Individual compounds were quantitatively converted to CO2 at 860 °C using CuO as a catalyst. A standard mixture of n-alkanes (C12, C14, C16, C18, C20, C22, C25, C28, C30, and C32) from Indiana University was measured twice a day to monitor the repeatability and accuracy of GC-irMS measurements. Precision for stable carbon isotopic analysis was better than 0.3‰ in standard deviation, and the deviation in δ13C values from the calibrated values of the working standard was generally 10% TOC). Its principal and featured biologic component is G. prisca, a microorganism with enigmatic phylogeny, which has long been disputed with prokaryotic (cyanobacteria) and eukaryotic (green microalga B. braunii) organisms.36−38,53−55 For the former viewpoint, since its first recognition in Kukersite shale, Zalessky56 made the first link between the morphology of the microfossils and the extant cyanobacteria Gloeocapsa, and thus named this microfossil G. prisca. Reed et al.36 thought G. prisca as a “primitive” prokaryotic organism and suggested that it was either nonphotosynthetic or fixed light using chlorophyll that did not contain a phytol side chain (e.g., bacteriochlorophyll). Based on investigations of G. prisca in Estonian samples, Foster et al.53,57 suggested that G. prisca were colonial cyanobacteria
with close biochemical similarity to the modern mat-forming cyanobacterium Entophysalis, mainly living in intertidal environment. Stasiuk and Osadetz58 suggested that the microfossils probably originated from a photosynthetic cyanophyte with a complex three-stage life cycle. Blokker et al.55 studied the molecular structure of G. prisca and suggested it belonging to fossil cyanobacteria. For the viewpoint of eukaryotic organism,37 B. braunii,54,59−61 or a related alga as the selectively preserved algaenan cell walls (such as coccoidal cyanophyte62) was suggested as a possible source organism for the G. prisca microfossils, because of the presence of a resistant algaenan in the green microalga B. braunii and some morphological similarities between this alga and G. prisca. Regardless of the affiliation of algae, the information illustrated by high abundance of hopenes, hopanes, benzohopanes, and aromatic hopanes in the Kukersite shale should be analyzed first, because this is associated with the evidence of prokaryotic organism with strong microbial activity in Kukersite 3580
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Figure 8. Stable carbon isotopic composition of n-alkanes, steroids, hopanoids, and aromatic hopanoids in Kukersite shale.
shale, which can also help explain what type of bacterial microbe is related to the microbially mediated aromatization. Apparently, the detection of abundant 2α-methylhopanes in Kukersite shale possibly indicates the occurrence of cyanobacteria.63−68 In the cultures of the cyanobacterium Synechocystis UTEX 2470, C30 diplopterol and diploptene were reported to have slightly heavier (0.9‰−2.3‰) δ13C values, relative to bacteriohoptetrol,69 which is consistent with the 2‰−4‰ enrichment on the aromatic hopanes in Kukersite shale in our studies. Foster et al.53,57 considered the G. prisca in Estonia Kukersite shales to be a colonial cyanobacteria organism with the origin of prokaryotic microbial mat; thus, cyanobacteria might be responsible for the generation of abundant monoaromatic, diaromatic, triaromatic, and tetraaromatic hopanes, as well as benzohopanes, and correspondingly, the microbially mediated aromatization in the Estonia Kukersite shale.
Table 3. Abundance, and the Ratios of Steroids and Hopanoids in the Saturated Hydrocarbon Fraction of Kukersite Shale indicator
ratio
∑steroids/∑hopanoids ∑rearranged cholestenes/∑steroids ∑rearranged cholestenes/∑monoaromatic steroids ∑σmonoaromatic steranes/∑steroids
0.30 0.75 3.00 0.25
5. CONCLUSIONS Abundant monoaromatic (C27), diaromatic (C26−28), triaromatic (C25−27), and tetraaromatic (C24−26) hopanes are present in the aromatic fraction of a Kukersite shale extract; thus, their δ13C values of individual compounds are determined. Benzohopanes with two structures derived from cyclization at C-16 and C-20 of hopanes are also abundant in this sample. Their occurrences, as well as the coexistence of hopenes, indicate that aromatization producing aromatic hopanes in Kukersite shale occurred rapidly during early diagenesis, which was a microbially mediated diagenetic process with strong microbial activity, rather than thermal reaction. The increase of aromatic hopanes from diaromatic (20%) to triaromatic (22%) then to tetraaromatic (40%) confirms a previous conclusion that the hopanoid skeleton undergoes progressive aromatization pathway from the D-ring to the Aring. In this aromatization pathway of hopanoids, four angular
Figure 9. Aromatization pathways of (a) steroids (after Mackienze et al.10) and (b) hopanoids (after Greiner et al.14,15 and Spyckerelle et al.16).
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methyl groups on the A-, B-, C-, and D-rings plus one of the gem-dimethyls at C-4 (C-23 and C-24) are successively lost with increasing aromaticity. Generally, regular hopanes (C27− C35) are proposed to be sourced from bacteriohopanetetraol (C35), while aromatic hopanes are derived from the diplopterol and/or diploptenes (both C30). Thus, different hopanoid precursors and the loss of up to five C atoms in the aromatization pathway help explain the ca. 2‰−4‰ 13C isotopic enrichment in aromatized hopanes, compared to nonaromatized hopanoids in the shale. By contrast, the angular methyl at C-18 position in the steroid nucleus is not removed but migrated to C-17 position in the formation of the C-ring monoaromatic steranes. In addition, more rearrangement (75%) and less aromatization, mainly for the formation of the C-ring monoaromatic steranes (25%) with no loss of C atoms, limited the variations in their stable carbon isotopic compositions. Hence, monoaromatic steranes exhibit similar δ13C values as the diasterenes in Kukersite shale. The presence of abundant 2α-methylhopanes implies that cyanobacteria occurred in the Kukersite shale, which might have occurred as previously suggested colonial microbes of the characteristic G. prisca. Thus, cyanobacteria might be responsible for the abundant occurrence of hopanoids, benzohopanes, diaromatic, triaromatic, and tetraaromatic hopanes and, thus, the microbially mediated aromatization of hopanoids as shown in this study.
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AUTHOR INFORMATION
Corresponding Authors
*Tel.: +86 20 85290191. E-mail:
[email protected] (Hong Lu). *Tel.: (860) 410-6684. E-mail:
[email protected] (Chang Samuel Hsu). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS
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REFERENCES
Financial support from NSFC (Nos. 41173053, 41473045) and State 973 Project (No. 2012CB214706) is acknowledged. This is contribution No. IS-2070 from GIGCAS.
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