Precambrian Research 196–197 (2012) 113–127
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Precambrian Research
journal homepage: www.elsevier.com/locate/precamres
Biomarkers of black shales formed by microbial mats, Late Mesoproterozoic
(1.1 Ga) Taoudeni Basin, Mauritania
Martin Blumenberg a,∗ , Volker Thiel a , Walter Riegel a , Linda C. Kah b , Joachim Reitner a
a
b
Geoscience Center, Geobiology Group, Georg-August-University Göttingen, Goldschmidtstr. 3, 37077 Göttingen, Germany
Department of Earth & Planetary Sciences, University of Tennessee, 1412 Circle Drive, Knoxville, TN 37996, USA
a r t i c l e
i n f o
Article history:
Received 6 May 2011
Received in revised form 31 October 2011
Accepted 18 November 2011
Available online 28 November 2011
Keywords:
Late Mesoproterozoic
Biomarkers
Hopanes
High aromaticity
Taoudeni Basin
Acritarchs
a b s t r a c t
Hydrocarbon biomarkers in Late Mesoproterozoic black shales from the Taoudeni Basin (Mauritania,
northwestern Africa) were analysed for palaeoenvironmental reconstruction. Within the Atar Group,
Touirist Formation shales showed the highest content of organic carbon (>20%) at very low maturity (Rc
less than 0.6). Microfacies and biomarker data indicate a shallow marine, high productivity, low oxygen
setting with benthic mats as key players for the accumulation of organic matter. Both, high C/S-ratios
and the occurrence of rearranged hopanes indicate that euxinic conditions were not prevalent, likely
reflecting the shallow depositional environment. Steranes were not observed, indicating only a minor
importance of modern, eukaryotic algae. Although low in abundance, a palynological survey, however,
reveals the presence of simple ornamented acritarchs. Input of highly aromatic biopolymers typical of
Mesoproterozoic acritarchs or microbial exopolymeric substances may be the origin of an unusually high
aromaticity observed for the biomarker extracts. High amounts of hopanes suggest that the benthic mats
were dominated by (cyano)bacteria. Furthermore, the presence of 2,3,6-trimethyl aryl isoprenoids points
at contributions of organic matter from anoxygenic phototrophic bacteria. However, low concentrations
of these compounds argue against major photic zone anoxia in the overlying water column and rather
suggest a role of anoxygenic phototrophs as part of the benthic microbial mat community.
The high abundances of hopanes in these samples suggest that nitrogen-limited conditions may have
been common in the Taoudeni Basin at 1.1 Ga. These results are consistent with ideas of widespread
nitrogen deficiency that emerged in Mesoproterozoic oceans due to high denitrification rates in anoxic
deep waters. Cyano- and other phototrophic bacteria, as well as a limited number of acritarch species
were able to cope with such conditions much better than modern algae with their higher nitrogen and
trace metal demands.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
A wide variety of metabolisms were established in the Earth’s
Oceans by 3.4 Ga (Allwood et al., 2006). However, the relative
importance of different prokaryotic metabolisms and the timing
of evolution and expansion of eukaryotic life remain controversial
(Rasmussen et al., 2008; Javaux et al., 2010). Prior to 2.4 Ga Earth’s
oceans harbored exceptionally low sulfate concentrations, and oxygen free deep waters with highly abundant ferrous Fe (Canfield,
2005). Although oxygen began to accumulate after about 2.4–2.2 Ga
(the “Great Oxidation Event”) it took at least until the end of the
Precambrian for deep oceanic water masses to show substantial
signs of increasing sulfate concentrations and oxygenation (Kah
et al., 2004; see Kah and Bartley (2011) for a review). Rather, it
∗ Corresponding author. Tel.: +49 0 551 3913756; fax: +49 0 551 397918.
E-mail address: [email protected] (M. Blumenberg).
0301-9268/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.precamres.2011.11.010
has been speculated that stable anoxic and potentially sulfide-rich
deeper ocean waters were overlain by a shallow oxygenated upper
water column for most of the Proterozoic (Canfield, 1998). Support for euxinic conditions in Proterozoic oceans comes from bulk
C/S-ratios (Imbus et al., 1992; Shen et al., 2002) and the occurrence of biomarkers in shales from the McArthur basin (1.64 Ga),
where euxinic conditions obviously extended into the photic zone
(Brocks et al., 2005). If persistent, photic zone euxinia may have
fueled anoxygenic phototrophy using H2 S as electron donor, yet
it is unclear whether this mode of primary production occurred
only in specific basins or, as it has been proposed, characterised the
entire Proterozoic (Johnston et al., 2009). A more complete understanding of the distribution of low-oxygen environments and their
associated microbial populations is also critical for understanding
the rise and importance of eukaryotic algae through Precambrian
times (Anbar and Knoll, 2002).
Biomarkers in sedimentary rocks and oils may persist over billions of years and can be valuable sources for information on
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M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
Fig. 1. Basemap showing the El Mreiti Gp. outcrops in Mauritania and the core site.
ancient environments. These molecular biosignatures and their
stable isotope signatures have the potential to shed light on the
prevailing organisms as well as on the metabolic pathways and carbon sources. Although biomarker data is still limited in its extent,
it provides substantial insights into life in Earth’s early oceans
(Mycke et al., 1988; Summons et al., 1988a,b, 1999; Pratt et al.,
1991; Logan et al., 1995, 2001; Brocks et al., 1999; Greenwood
et al., 2004; Eigenbrode et al., 2008; Waldbauer et al., 2009). Unfortunately, recent studies (Brocks et al., 2008; Rasmussen et al.,
2008; Brocks, 2011) have indicated that at least some of the
biomarkers inventories presented in the above mentioned studies were not syngenetic to their host rock but rather the result of
anthropogenic contaminations with hydrocarbons. Consequently,
some interpretations regarding the distribution of prokaryotic and
eukaryotic communities in the Precambrian are now being questioned (e.g., the early rise of modern eukaryotic algae based on
findings of abundant steranes; Brocks (2009)). This and the low
number of localities providing valuable biomarker information
stress the need of additional studies from a variety of Precambrian
settings.
The Taoudeni Basin, northwestern Africa, records a discontinuous sedimentation history from the Proterozoic to the Cenozoic,
and contains a thick succession of Proterozoic-aged sedimentary
rocks. These rocks of the Taoudeni Basin include two supergroups,
the lower of which (Supergroup 1) rests unconformably on Archean
to Paleoproterozoic basement and consists of the Char, Atar/El Mreiti, and Assabet el Hassiane/Bir Amrane Groups. Carbon-isotope
chemostratigraphy has determined the ∼800 m thick Atar/El Mreiti
Group to be late Mesoproterozoic in age (Teal and Kah, 2005; Kah
et al., 2009), which is consistent with Re-Os ages of 1107 ± 12 Ma,
1109 ± 22 Ma and 1105 ± 37 Ma for black shale within the Atar/El
Mreiti Group (Rooney et al., 2010). With the exception, however,
of ␦13 C analyses on stromatolitic fabrics of the Atar Group (Teal
and Kah, 2005; Kah and Bartley, 2011), recent facies analysis of
stromatolite-bearing strata (Kah et al., 2009), and a single report
on general geochemical characteristics of the Touirist Formation
organic matter (Doering et al., 2009), there has been little study concerning the biological make-up of Atar/ElMreiti Group strata and its
environmental interpretation. Here we report the first biomarker
studies of Taoudeni Basin strata (Touirist Formation) and use an
approach to the interpretation of depositional environments based
on biomarkers, stable isotope signatures, microfacies, and palynology. Results of this study provide compelling evidence on the
authenticity of the biosignatures and allow for a robust reconstruction of a Late Mesoproterozoic highly productive, shallow marine
setting.
2. Materials and methods
2.1. Rock samples
Core samples were drilled in 2007 (for site see Fig. 1). Bisects
of the core (4 samples) were used for biomarker, microfacies, and
palynological analyses (for positions in the lithological section see
Fig. 2). For biomarker studies, bisects were separated into exterior
and interior parts, and both samples were analysed individually.
A clean precision saw (Buehler IsoMet 1000) was used, which
was carefully cleaned after each saw step with clean water and
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
115
2.3. Gas chromatography–mass spectrometry (GC–MS) and gas
chromatography combustion isotope ratio-mass spectrometry
(GC–C–IRMS)
Fig. 2. Simplified lithologic section of the investigated core with TOC and Tmax trends
(unpublished results) and the position of the analysed rock samples.
acetone. Samples were then crushed and powdered using a pebble
mill (Retsch MM 301) that was pre-cleaned with solvents and
sand. Bulk C/N/S analysis was performed using a Hekatech Euro
EA CNS analyser. To determine the contents of TOC and carbonate
carbon (Ccarb ), each sample was analysed both before and after
acidification with HCl. Bulk ␦13 C and ␦15 N isotope analysis was
made via elemental analysis-isotope ratio mass spectrometry
(EA-IRMS, Delta plus, Thermo Finnigan).
For the detection of potential contaminations, the exterior and
interior parts of the drill core bisects were compared. Generally, both yielded similar hydrocarbon compositions indicating
only minor external contamination. Moreover, branched alkanes
with quarternary carbon (BAQCs) were not found in any sample,
which excludes the possibility of appreciable contamination from
polyethylene plastic bags (Brocks et al., 2008).
2.2. Extraction and fractionation
Ground samples (∼10 g) were subjected twice with distilled
dichloromethane (DCM)/n-hexane (9/1; ∼100 ml each) using ultrasonication followed by extraction of hydrocarbons with n-hexane
(100 ml). Extracts were combined and concentrated in a precleaned rotary evaporator, followed by reduction of the solvent to
near dryness in a stream of N2 . The resulting total extracts were separated by column chromatography into a saturated fraction (F1), an
aromatic fraction (F2) and a polar residue. 7.5 g of dry silica gel 60
were filled into a column with an internal diameter of about 1.5 cm.
The extract was absorbed onto 500 mg of silica gel 60 and placed
onto the column. F1 was eluted with 1.5 dead volumes of n-hexane
(15 ml), F2 with two dead volumes n-hexane/DCM (1/1; 20 ml) and
the polar residue with 20 ml DCM/methanol (1/1). Fractions were
concentrated by careful rotary evaporation, dried under a stream of
N2 and dissolved in 200 ␮l n-hexane (F1) and 1500 ␮l (F2), respectively. To remove elemental sulfur reduced copper was added to F1
and F2.
Saturated (F1) and aromatic (F2) hydrocarbons were analysed
by combined gas chromatography–mass spectrometry (GC–MS)
using a Varian CP-3800 gas chromatograph coupled to a Varian
1200L mass spectrometer. Biomarkers were identified by comparing mass spectra and retention times with published data
and/or reference compounds. The GC was equipped with a deactivated retention gap (internal diameter (i.d.) 0.53 mm) connected
to a fused silica capillary column (Phenomenex Zebron ZB-1MS,
60 m, 0.10 ␮m film thickness, 0.25 mm i.d.), with He as the carrier gas. The temperature program was 60 ◦ C (for 5 min), then
increased by 10 ◦ C/min to 150◦ (held 0 min), and finally increased
by 4 ◦ C/min to 310 (held for 25 min.). The MS source was operated at 200 ◦ C in electron impact mode at 70 eV ionisation energy.
Fractions were injected on column using a PTV injector. The injector was initially held at 80 ◦ C for 0.2 min and then heated at
150 ◦ C/min to 320 ◦ C (held for 15 min). Biomarkers were analysed (i) in total ion current mode (from 50 to 650 amu; TIC), (ii)
by selected ion monitoring (SIM) of nine ions (total cycle time
0.9 s), and (iii) by multiple reaction monitoring (MRM) with a total
cycle time of 1.6 s per scan for 16 transitions. Argon was used
as the collision gas. The collision energy was −10 eV. Typically,
biomarkers were identified from MRM and quantified from TIC.
Relative quantification of hopanes was achieved from SIM analyses,
because of better peak resolutions. The detection limit for steranes
was checked in MRM mode using authentic standards (5␣(H)cholestane and 4␣,23,24-trimethylcholestane (dinosterane)). The
limit of detection for the first was ∼10 pg, representing for the dilutions used, ∼0.5 ppm of the saturates fraction. For dinosterane it
was slightly higher (20 pg in general, representing ∼1 ppm of the
saturates fraction).
Trimethylated aryl isoprenoids were identified by selective
MRM transitions and comparison with the aromatic fraction of a
Jurassic black shale (Bächental, Toarcian), that contains abundant
isorenieratene and isorenieratene degradation products (Köster
et al., 1995).
The ␦13 C-values of hydrocarbons were analysed (minimum of
three replicates) using a Thermo Scientific Trace GC coupled to a
Delta Plus isotope-ratio MS. The combustion reactor contained CuO,
Ni, and Pt and was operated at 940 ◦ C. The GC was equipped with
a Zebron ZB-5MS (30 m; 0.25 ␮m film thickness, and 0.32 mm i.d.)
and runs using a temperature program identical to that described
above. The stable carbon isotope compositions are reported in the
delta notation (␦13 C) vs. the VPDB standard. Standard deviations for
␦13 C analyses were generally less than 1‰ and sometimes higher
due to bad peak separation or influences from co-eluting unresolved complex mixtures.
Selected samples were subjected to Laser-ICP-MS analyses performed according Sánchez-Beristain et al. (2010) and to micro
carbonate carbon stable isotope analyses according to Delecat et al.
(2010), respectively.
2.4. Palynology
One sample (sample MCS 4) was prepared for palynological
analysis by demineralisation with HCl and HF. In order to mechanically dissociate the organic matrix and disintegrate remaining
larger particles, the residue was crushed in a mortar, briefly boiled
in 15% H2 O2 and exposed to ultrasonic treatment. Fine detritus was
removed by screening at 15 ␮m mesh size. The residue was stored
in glycerine and three permanent preparations were mounted in
glycerine jelly. Because of their scarcity within the bulk matrix,
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Fig. 3. Images of palynomorph residuals (A–D) and microfacies (E–J) of the Touirist Fm. black shales. (A) Microbial mat microstructure showing typical oval growth form
in residue of sample MCS 4 and a relatively thick-walled leiosphaerid acritarch. (B) Leiosphaeridia sp. with lanceolate fold. (C) Leiosphaeridia sp. with concentric fold and
thinned central area (opening?). (D) Leiosphaeridia sp. with thin wrinkled wall and irregular compression folds. (E and F) Microfacies images from MCS 4. E (transmitted
light): The facies is characterised by undisturbed laminated organic-rich, silty sediments. The laminae are several millimetre-long condensed flakes of organic matter,
which formerly mostl likely represented benthic microbial mats. The laminae have a thickness of 50–100 ␮m and trapped silt and clay material. F (reflected light): Some of the
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
117
Laser micro-Raman spectroscopy was performed on selected palynomorphs (not shown). The spectra were dominated by stretching
band at 1600 cm−1 (typical for C C bonds like in aromatic rings)
with only weak signals at 1345 cm−1 (specific for CH3 ) (not shown).
3.3. Microfacies
Fig. 4. Statistical size distribution of palynomorphs in sample MCS 4.
palynomorphs were picked individually for photography under
transmitted light, SEM, and Laser micro-Raman spectroscopy.
3. Results
3.1. Bulk geochemical characteristics
TOC of the investigated Touirist Formation black shales were
high (10.1–22.2%; Table 1) and showed even more elevated concentrations in the stratigraphic highest section (see also Fig. 2).
Ccarb values were generally low (0.1–0.5%; Table 1) and sulfur concentrations were variable (0.8–3.1%), again with most elevated
concentrations high in the stratigraphic section. Bulk carbon ␦13 C
values showed an increasing trend from −33.9‰ vs. VPDB low in
the stratigraphic section to −29.7‰ in the stratigraphically highest
sample. Bulk nitrogen stable isotopes fluctuated between +4.9 and
+6.1‰ (vs. air) and showed no trend with respect to core depth.
3.2. Palynology
Palynomorphs recovered are predominantly simple more or less
smooth-walled sphaeromorph acritarchs without distinct opening
structure which can be classified as Leiosphaeridia sp. (Fig. 3A–D;).
Fig. 4 shows the statistical size range of palynomorphs in sample MCS 4 with a peak between 20 and 40 ␮m (n = 125). However,
individual larger leiospheres with a diameter up to 125 ␮m were
also observed. Rather well defined round to oval microstrucutres,
which are solid, lenticular in cross section and range in size mainly
between 200 ␮m and 400 ␮m (Fig. 3A) are a striking component of
the maceration residue. They occur isolated or in clusters and show
a distinct orange fluorescence with blue light irradiation. They are
tentatively considered here as growth forms of bacterial colonies
significantly contributing to the formation of the microbial mats.
Microfacies analyses revealed layered occurrences of organic
matter with occasionally abundant pyrite (Fig. 3). In the stratigraphically highest sample (MCS 1) the organic matter was,
compared to MCS 4, less finely dispersed and undisturbed
and revealed ripple-like structural appearances. In MCS 2 we
found additional interesting features (Fig. 3G–H). In this sample
autochthonous carbonates of dispersed distributed euhedral nonluminescent bright dolomites were observed which were most
likely diagenetically formed within the sediment. In addition,
luminescent early diagentic automicrites were also observed. The
automicrites form a halo around former microbial mat remains,
which contain very small sized (10–20 ␮m) strong luminescent
anhedral calcite crystals and are often arranged in rows (Fig. 3H).
Generally the strong luminescence is caused by high amounts of Mn
within the calcite crystals (Laser ICP-MS analyses; data not shown).
Assumably, these high Mn values are primary signals, reflecting negative redox conditions during mineralisation process. The
later diagenetic carbonate crystals do not show any luminescence,
demonstrating a different redox environment. Comparable structures were observed in methane-related carbonates from the Black
Sea which were formed under anoxic conditions (Reitner et al.,
2005). Therefore, the luminescent laminae are most likely lithified former biofilms with the strong luminescent anhedral calcites
to be probably small lithified microbial communities. Those are
embedded in a former matrix of exopolymeric substances, which
is now weakly calcified with only minor red luminescence. Comparable lithified microbial laminae are also known from the Sturtian
Rasthof cap carbonates from Namibia (Pruss et al., 2010). Pyrite
is occasionally associated with calcified microbial mats. The small
strong luminescent calcite crystals are probably lithified microbial
colonies located within the microbial mats. Selected carbon stable isotope analyses of the automicrite mineral exhibit relatively
13 C depleted values (␦13 C = −16‰ VPDB) which is in the range
described from carbonates formed during microbial sulfate reduction (Raiswell and Fisher, 2000) and are thus in agreement with
a similar source than that for abundant pyrite crystals within the
calcified microbial mats.
3.4. Biomarkers
Extractable hydrocarbons consisted mainly of saturated (nalkanes, cycloalkanes, methylated alkanes, isoprenoids) and
aromatic compounds, with generally low saturate/aromatic-ratios
(<0.1; Table 2).
3.4.1. Saturates (C15 +)
Patterns of saturated hydrocarbons differed slightly between
the samples, but all contain n-alkanes (C15 +) ranging from
C15 to C35 with maxima at C17 to C19 (Fig. 5). The carbon
laminae are enriched in small (10–50 ␮m) sized pyrite crystals often organised in flat clusters and framboids within the organic matter (white arrow). These laminated
pyrite occurrences hint to sulfate reducing microbes as an integral part of the mat community. (G and H) Microfacies images from MCS 2. G (transmitted light): The facies
is characterised by laminated and sometimes folded organic-rich sediments (“roll up structures”). The sediment is in some parts enriched in carbonates like euhedral single
crystal, non-luminescent dolomites (left arrow). The remains of the microbial mats are again some millimetre-sized organic flakes (right arrow). H (cathodoluminescence
– CL micrograph): The microbial mat remains contain very small (10–20 ␮m) sized strong luminescent anhedral calcite crystals which are often arranged in rows. The
strong luminescence is caused by high amounts of Mn within the calcite crystals. Pyrite is occasionally also present. The small calcite crystals are probably lithified microbes
located within the microbial mats. (I and J) Microfacies images from MCS 1. I (transmitted light): The facies is characterised by undulated and sometimes folded organic-rich
sediments with high amounts of fine siliciclastic material. Silicilclastics are concentrated in microrippels which are covered by and bound to former microbial mats. The
ripples are formed by moving sediments and overprinted by later compaction. Sand and silt grains are mostly angular which suppose a nearby source area. I (insert) “roll up
structures” in MCS 1. J (reflected light): The microbial mat remains contain pyrite enriched in framboids and larger lenses (arrow).
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Table 1
Geochemical parameters of black shales of the Touirist Formation (Taoudeni Basin).
Sample
MCS
MCS
MCS
MCS
1
2
3
4
Formation
TOC (%)
Ccarb (%)
S (%)
N (%)
C/N
C/S
␦13 C bulk
␦15 N bulk
Touirist (Atar Group)
Touirist (Atar Group)
Touirist (Atar Group)
Touirist (Atar Group)
22.2
17.2
16.1
10.1
0.1
0.1
0.1
0.2
3.1
2.1
0.9
0.8
0.5
0.4
0.4
0.2
45.8
43.4
40.7
44.1
7.3
8.3
17.9
12.3
−29.7
−30.6
−31.1
−33.8
+5.9
+5.2
+4.9
+6.1
Fig. 5. Total ion chromatograms (TICs) of the saturate hydrocarbon fractions (F1) of the black shales from the Touirist Formation (1.1 Ga). Filled circles denote n-alkanes,
triangles denote cyclohexylalkanes.
Table 2
Amounts of saturated and aromatic hydrocarbons.
Sample
Saturates (ppm)
Aromatics (ppm)
Saturates/aromatics
MCS
MCS
MCS
MCS
360
180
250
370
6040
3760
5330
4280
0.06
0.05
0.05
0.09
1
2
3
4
preference indices (CPI) were about 1 for all samples (0.95–1.05).
Cyclohexylalkanes demonstrated similar patterns as n-alkanes, but
maximized at slightly higher carbon numbers (Fig. 5; maximum
cyclohexyalkane C18 vs. C17 for n-alkanes). Phytane, pristane and
norpristane were observed in significant amounts (Fig. 5). Pristane to phytane ratios ranged from 0.64 to 1.01 (Table 3). Pristane
to C17 and phytane to C18 ratios ranged from 0.24 to 0.35 and
0.21 to 0.31, respectively (except for the topmost samples; Pr/nC17 = 1.21 and Ph/n-C18 = 0.74). Acyclic isoprenoids with carbon
0.79
0.56
0.66
0.18
3
3
5
4
1
1
1
2
Sample
MPI-1
Phen/MP
MPR
Rc (MPI-1)
MCS
MCS
MCS
MCS
0.49
0.51
0.43
0.36
0.03*
0.24
0.34
0.33
0.52
0.63
0.61
0.53
0.56
0.57
0.52
0.47
1
2
3
4
numbers higher than C20 (phytane), e.g. C40 -isoprenoids, were not
observed.
0.42
0.42
0.40
0.53
1.61
1.93
1.96
2.19
np: not present (confirmed by specific MS–MS transitions) and chei.: cheilanthanes (tricyclic terpanes).
a
2␣-MeC31/(2␣MeC31+C30) (%); from SIM (due to better peak resolution than from MRM), after Summons et al. (1999).
b
3␤-MeC31/(3␤MeC31+C30) (%); from SIM (due to better peak resolution than from MRM), after Eigenbrode et al. (2008).
c
17␣,21␤-hopane/(17␣,21␤-hopane+phytane); from TIC.
0.69
0.53
0.42
0.45
0.57
0.56
0.57
0.61
0.12
0.20
0.10
0.27
0.20
0.34
0.27
0.49
np
np
np
np
1.03
0.95
1.05
0.98
18
18
18
17
0.74
0.21
0.23
0.30
1.21
0.24
0.24
0.28
0.49
0.39
0.50
0.49
0.94
0.64
1.01
0.98
1
2
3
4
MCS
MCS
MCS
MCS
119
Table 4
Maturity indices (aromatic hydrocarbons) of black shales from the Touirist Fm. from
the Taoudeni Basin. *Most likely affected by biodegradation. Methylphenanthrene
Index (MPI-1) = 1.5 * (2-MP + 3-MP)/(Phen + 1-MP + 9-MP) (Radke and Welte, 1983).
Since Phenanthrene (Phen)/methylphenanthrenes (MP) were <1 computed vitrinite
reflectance was calculated after Boreham et al. (1988): Rc (MPI-1) = 0.7 * MPI-1 + 0.22.
0.09
0.12
0.24
0.35
3␤-Me-Index
(%)b
22S/22R (C32 )
C24tetra/C30
Tricyclics/17␣ hopanes
Steranes
CPI
n-Cmax
Ph/n-C18
Pr/n-C17
Pr/(Pr + Ph)
Pr/Ph
Sample
Table 3
Biomarker indices (saturated hydrocarbons) of black shales from the Touirist Fm. (Taoudeni Basin)..
chei24/23
chei22/21
Ts/(Ts + Tm)
Dia/C30
2␣-Me-Index
(%)a
Hopane
indexc
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
3.4.2. Aromatic steroids and steranes
Resolved sterane and steroid peaks were not observed. Only
small humps were found in the range were steranes usually elute.
These humps consist of unresolved complex mixtures (UCM) of
compounds. However, we cannot exclude that trace amounts of
steranes are obscured by this UCM, but if present they were under
detection limit. The lower level of detection of steranes was <1 ppm
of the saturates fraction for 5␣(H)-cholestane, which is in the same
range given in other studies (e.g., see SOM of Brocks et al., 2005).
Fig. 6 shows for comparison the SIM of the hopane specific fragment
at m/z 191 and the sterane specific fragment at m/z 217. 4-Methyl
steranes were also under detection limit, even when highly selective SIM or MRM modes were applied (according to Summons et al.,
1987). This includes dinosteranes, which could not be detected
using the 414 → 231 and 414 → 98 transitions.
The presence of aromatic steroids as well as aromatic ringmethylated (e.g. 4-methyl) steranes was also tested by specific
MS–MS transitions (m/z 344 → 231 (or 245; ring-methylated);
358 → 231 (or 245); 372 → 231 (or 245); 386 → 231 (or 245);
400 → 231 (or 245)). None of these transitions showed resolved
peaks.
3.4.3. Hopanes and cheilanthanes
The highest relative amounts of hopanes were observed in the
stratigraphically highest sample and were clearly detectable even
from total ion chromatograms (Fig. 5). Hopanes in all samples
consist of C27 –C35 compounds, and generally show most significant abundances of 17␣(H),21␤(H)-C30 (17␣(H),21␤(H)-hopane;
Fig. 7). 22S/22R-isomerisation ratios for homohopanes were at
about ∼0.6 (Table 3). Diahopanes were found in varying amounts,
with decreasing ratios of C30 -diahopane vs. 17␣(H),21␤(H)-hopane
from the lowermost to the topmost sample (from 0.35 to 0.09).
Minor to moderate concentrations of ring A methylated hopanes
were observed with a 2␣-methyl hopane index of 1–2% (calculated after Summons et al., 1999) and a 3␤-methyl hopane index
of 3–5% (calculated after Brocks et al., 2005). 29,30- and 28,30Bisnorhopanes (BNH) were only slightly above detection limit in
all samples (Fig. 7).
A suite of C19 –C25 tricyclic terpanes (cheilanthanes) were
also observed in all samples. Moreover, all samples showed an
abundance of tetracyclic C24 terpane (M+ 330), most likely 17,21secohopane (C24 ) (see Aquino Neto et al., 1983).
3.5. Aromatic hydrocarbons
Aromatic hydrocarbons were present in all samples and contained high relative concentrations of dimethyl- and trimethyl
naphthalenes, phenanthrene, dimethyl- and trimethyl phenanthrenes, chrysene and methylated chrysene(s) (Fig. 8) and
were used to calculate maturity indices (Table 4). In the
stratigraphically highest sample (MCS 1) low molecular weight
120
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
Hopanes and diahopanes
Ch21
Ch19
Ch20
Ch23
17,21-secohopane (C24)
Tm
Ts
e.g.
Ch24
Ch25
SIM m/z 191
no steranes and diasteranes
?
e.g.
??
SIM m/z 217
time
Fig. 6. Selected ion monitoring traces (SIM) from the saturated hydrocarbon fraction (F1) of MCS 4 (black shale from the lowermost Touirist Formation). m/z 191 shows
mainly pentacyclic triterpenoids (hopanes) and tricyclic terpanes (cheilanthanes), whereas m/z 217 is a typical fragment of steranes and diasteranes.
aromatics were clearly depleted relative to their concentration in
stratigraphically lower horizons.
Moreover, except for minor amounts of methylated chrysenes
no polycyclic aromatic hydrocarbons (PAHs) of higher molecular
weight were observed.
section, whereas the stratigraphically highest samples showed an
enrichment in 13 C of about 4–5‰ (similar to bulk stable carbon
isotopes; compare Table 1 and Table 5).
3.5.1. Aromatic carotenoids
Long-chain carotenoids (e.g. isorenieratene) and derivatives
were not detected even after application of specific SIM and MS–MS
transitions (according to Brocks and Schaeffer (2008)). However,
alkylated trimethylbenzenes with dominantly 2,3,6-methylation
were found after performing M+ → 134 transitions (exemplified
for sample MCS 4; Fig. 9). The methylation pattern was confirmed after coinjection with a black shale rich in isorenieratane
and its break-down products (Bächental, Toarcian; see also Köster
et al. (1995)). The alkylated trimethylbenzenes in the Bächental
sample are predominantly composed of 2,3,6-trimethyl aryl isoprenoids and exhibit similar distribution to other Toarcian black
shales (Schwark and Frimmel, 2004). In the Touirist Formation,
an additional short chain C21 diaryl isoprenoids (LIII in Koopmans
et al. (1996a)) was also observed. However, in Touirist Formation shales abundant other aryl isoprenoids and aryl alkanes,
in addition to 2,3,6-methylated isomers, were also found, much
higher than reported from Toarcian shales rich in isorenieratene
(Schwark and Frimmel, 2004). Those samples often exclusively
include 2,3,6-trimethyl aryl isoprenoids. All shales demonstrated
similar distributions of trimethylbenzenes (not shown).
4.1. Syngeneity of biomarkers
3.6. Stable carbon isotopes
4.2. Maturity and biodegradation
Stable carbon isotope signatures of saturated and aromatic
hydrocarbons were analysed for all shales. N-alkanes and acyclic
isoprenoids had ␦13 C values between approximately −30 and
−35‰ (VPDB; Table 5). Generally, n-alkyl hydrocarbons were similar in ␦13 C or slightly 13 C-depleted compared to phytane. Hopanes
were found to be slightly less depleted in 13 C compared to acyclic
compounds. Polycyclic aromatic hydrocarbons demonstrated similar ranges to that found for saturates. However, we did observe
that the strongest 13 C-depletions occurred low in the stratigraphic
Effects of biodegradation, namely an increase of phytane/nC18 and hopanes, and an apparent loss of low molecular weight
PAHs are indicated for the stratigraphically highest sample. Moreover, almost all samples exhibit pronounced unresolved complex
mixtures (UCM), although low molecular weight saturates (C15 +)
were still present in high amounts. Methyl phenanthrene ratios
(MPR) ranged between 0.52 and 0.63. Based on phenanthrene
to methyl phenanthrene ratios <1 (∼0.24 to 0.34) (Brocks et al.,
2003a) and methyl phenanthrene indices (MPI-1) between 0.36
4. Discussion
Establishing a syngenetic relationship of the bitumen with its
host rock is an underlying requirement for any attempt to interpret
Precambrian ecosystems by means of hydrocarbon biomarkers. A
number of observations allows the critical assessment of whether
the measured compounds were originally part of the host rock. (i)
First, the biomarker distributions in the exterior and interior parts
of the cores are virtually identical (Table 6), pointing to the absence
of drilling contamination. (ii) Second, the virtual lack of steranes
(including dinosterane) and of higher plant-derived triterpanes
suggest the absence of substantial contamination by Phanerozoic
organic matter. (iii) Thirdly, indices describing the maturity of the
bitumen (MPI-1; Ts/(Ts + Tm); see below) coincide and are in good
agreement with bulk geochemical maturity assessments (i.e. Tmax
values; Fig. 2). (iv) Finally, bulk ␦13 C and biomarker ␦13 C values are
similar, suggesting similar organic sources. In conjunction, these
indications yield compelling evidence that the saturated and aromatic hydrocarbons extracted from the Late Mesoproterozoic black
shales of the Touirist Formation are syngenetic and have not been
introduced at a later stage
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
121
Fig. 7. Multiple reaction monitoring (MRM) transitions typical for hopanes and norhopanes; MCS 4 (black shale from the lowermost Touirist Formation).
and 0.51, computed vitrinite reflectance (Rc (%)) of 0.47–0.57
were calculated after Boreham et al. (1988); see Table 4 for
details). These computed vitrinite reflectance values correspond
to low maturities (early oil window to peak oil window; Killops
and Killops (2005)) and references therein) and are consistent
with observed ratios of 18␣-22,29,30-trisnorneohopane (Ts) to
17␣-22,29,30-trisnorhopane (Tm); Ts/(Ts + Tm) of about 0.40–0.53
(Table 3). Three samples display relatively low pristane/n-C17 ratios
MP
TMN
diP
DMN
P
DMP
chrysene
TMP
methyl
chrysenes perylene
TIC
time
Fig. 8. Total ion chromatogram of the aromatic fraction (F2) of MCS 4 (black shale from the lowermost Touirist Formation). Individual aromatic hydrocarbons were identified
by use of selected ion traces. DMN: dimethyl napthalenes; TMN: trimethyl naphthalenes; diP: dihydro phenanthrene; P: phenanthrene; MP: methyl phenanthrenes; DMP:
dimethyl phenanthrenes; TMP: trimethyl phenanthrenes.
122
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
Table 5
Carbon stable isotope signatures of biomarkers (saturates and aromatics). Note that pristane and phytane were not base line separated from n-alkanes and should – due to
chromatographic reasons – in reality be slightly more enriched in 13 C.
Sample
MCS 1
n-C15
n-C16
Cyclohexyl-C10
n-C17
Pristane
Cyclohexyl-C11
n-C18
Phytane
Cyclohexyl-C12
n-C19
n-C20
n-C21
n-C22
n-C23
n-C24
18␣-22,29,30-Trisnorhopane (Ts)
17␣-22,29,30-Trisnorhopane (Tm)
30-Norhopane
17␣(H),21␤(H)-Hopane
22S-17␣(H),21␤(H)-Homohopane
Phenanthrene
3-Methylphenanthrene (3-MP)
2-Methylphenanthrene (2-MP)
9-Methylphenanthrene (9-MP)
1-Methylphenanthrene (1-MP)
Chrysene
MCS 2
␦13 C (mean)
±
−35.6
−35.2
−34.9
−35.4
−35.2
−34.5
−35.2
−34.3
−35.1
−34.7
−34.9
−34.2
−35.3
−33.9
−35.1
0.3
0.6
0.7
0.1
1.3
0.8
1.8
3.0
1.3
0.8
0.8
1.5
1.1
0.6
−33.1
−34.2
−34.9
−35.3
−33.6
−32.9
0.5
0.8
0.9
2.9
1.1
1.6
MCS 3
MCS 4
␦13 C (mean)
±
␦13 C (mean)
±
−32.9
−32.5
−33.5
−32.6
−32.8
−33.7
−32.1
−32.2
−33.9
−33.3
−32.1
−32.3
−31.2
−32.8
0.2
0.6
0.6
1.9
0.4
0.1
0.1
1.0
0.4
1.3
1.1
1.9
1.2
−33.2
−32.4
−34.3
1.8
1.1
1.4
−32.1
−33.4
−31.2
−29.8
−31.2
−32.3
−32.1
−31.9
−31.1
−30.6
0.6
0.6
1.7
0.1
0.6
1.8
2.1
1.7
0.0
0.8
−29.6
2.1
−28.8
1.5
−30.8
−32.3
−32.5
−32.3
−31.8
−30.9
1.0
0.4
0.8
1.8
2.4
1.0
−29.7
−30.5
−30.5
−30.8
−30.1
−28.5
1.1
0.3
0.4
0.4
0.8
0.1
(0.21–0.35), in line with other Proterozoic rock samples (Fowler and
Douglas, 1987; Summons et al., 1988b; Dutkiewicz et al., 2004). The
pristane/n-C17 ratio in the stratigraphically highest sample (MCS 1)
was considerably higher (1.21) than those of the other samples.
But, even for MCS 1 these values corresponded to only light –
most likely postdepositional biodegradation (PM 2) according to
the Peters–Moldowan biodegradation scale (Peters and Moldowan,
1993). However, we also must consider the potential impact from
calibration of this biodegradation scale for Phanerozoic organic
matter, which typically shows appreciable contributions of the
acyclic isoprenoids pristane and phytane. Low inputs of these
isoprenoids, as observed for the Mesoproterozoic samples, may
influence the pristane/n-C17 -ratios and phytane/n-C18 ratios a priori which makes it difficult to resolve the extent of biodegradation.
Due to the presence of unresolved complex mixtures and the pronounced loss of low molecular weight compounds (saturates and
aromatics), we assume that moderate biodegradation affected particularly the stratigraphically highest sample (MCS 1).
4.3. Palaeoenvironmental implications
4.3.1. General aspects
Black shales in the Taoudeni Basin were deposited in the
Late Mesoproterozoic at about 1.1 Ga (Rooney et al., 2010). The
shales studied contain high amounts of organic matter (10–22%)
and increase in the lithological section to almost 30% (Fig. 2).
They were formed in marine, epeiric water environments, under
potentially shallow water (Kah et al., in review; Bertrand-Sarfati
and Moussine-Pouchkine, 1988). Our data reveal additional
␦13 C (mean)
±
−30.5
−30.5
0.1
0.5
−30.5
−30.7
−29.2
−29.8
−29.9
−27.6
−30.2
−31.2
−30.0
−32.4
−31.3
−29.1
−28.5
−26.9
−31.9
−29.0
−29.7
1.1
0.8
0.3
0.9
3.3
0.6
−30.3
0.8
−30.8
0.4
information on the biota of the Taoudeni Basin and differences
between the four sampled periods of black shale formation within
the Touirist Formation. Increasing TOC and S-concentrations
suggest that the generally high primary production (and/or degree
of preservation) increased from the lower to the upper Touirist
Formation. Although C/S ratios have to be used with caution for Proterozoic samples (e.g. Shen et al., 2002), a comparison with modern
marine settings (e.g. euxinic Black Sea; <3; (Berner, 1984) suggests
the lack of extensive euxinic conditions in the water column during
deposition of the Touirist Formation (7.6–12.6). Euxinia, however,
is believed to be prevalent through the Proterozoic (Canfield, 1998;
Kah and Bartley, 2011). Absence of euxinia above the microbial
mats deposited in the Touirist Fm. may reflect the shallow-water
setting and the potential for diffusion of oxygen into the upper
water column from the atmosphere or the effects of episodic storm
mixing. Both the onset of widespread sulfate evaporite deposition
in the Mesoproterozoic (Kah et al., 2001; Goodman and Kah, 2004),
and depletion of Mo concentrations from similarly aged black shale
(Lyons et al., 2009) support the potential for suboxic conditions prevailing in shallow waters by the late Mesoproterozoic. Moreover,
a stable chemocline in the photic zone and euxinia below (photic
zone anoxia) was recently reconstructed for the Barney Creek
Formation (1.64 Ga), which yielded high amounts of biomarkers
of anoxygenic phototrophs, such as isorenieratane, okenane, and
respective break-down products (Brocks et al., 2005; Brocks and
Schaeffer, 2008). Intact carotenoid derivatives were not found in
the Touirist Formation black shales, thus evidence for photic zone
euxinia in the water column above the microbial mats is lacking.
Findings of potential break-down products of isorenieratane in
Table 6
Biomarker indices (saturated hydrocarbons) of the interior and exterior of a black shale sample from the Touirist Fm. (Taoudeni Basin).
Sample
Pr/Ph
Pr/n-C17
Ph/n-C18
n-Cmax
CPI
Steranes
Tricyclics/17␣-hopanes
22S/22R (C32 )
Ts/(Ts+Tm)
Dia/17␣-hopane
MCS 4 interior
MCS 4 exterior
0.98
0.75
0.28
0.28
0.30
0.31
17
18
0.98
1.05
np
np
0.49
0.43
0.61
0.61
0.53
0.53
0.35
0.35
np: not present.
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
123
depth (Table 3); however, maturity can be excluded as a major
control of the observed distribution, since all samples exhibit similar Rc values (∼0.5–0.6; Table 4). Likewise, biodegradation cannot
be positively linked to the presence of diahopanes since lowest
C30 diahopane/hopane-ratios were just observed in the potentially
most biodegraded sample (top; MCS 1). In the Taoudeni Basin the
abundant presence of diahopanes can be better explained by a shallow, suboxic depositional environment, where diahopanes often
occur in high amounts (Peters et al., 2004a). The water depth during deposition of benthic mats reflected in sample MCS 1 appear to
have been particularly shallow, since the occurrence of microripples suggests deposition above wave base (Fig. 3J).
Fig. 9. Trimethylated aryl isoprenoids and alkanes in the aromatic fraction (F2)
of MCS 4 (black shale from the lowermost Touirist Formation) as detected from
specific multiple reaction monitoring (MRM) transitions (a, b, c, d, e). The 2,3,6trimethylation pattern of the denoted benzenes was confirmed by coinjection of
MCS 4 with an aromatic hydrocarbon fraction from a Jurassic black shale (a , b ,
c , d , e ; Bächental, Toarcian; see Section 2). Asterisks denote 2,3,6-trimethyl aryl
isoprenoids identified from coinjection.
the Touirist Fm. shales may however be interpreted to reflect (i)
euxinia in deeper waters of the basin, (ii) intermittent euxinia
above the shallow-water microbial mats, and/or (iii) contributions
from green-sulfur bacteria living in the stratified mats.
Pristane/phytane ratios (0.8–1.0) neither suggest extremely
reductive (1) nor oxidative (1) conditions of early diagenesis
(Peters et al., 2004b). With appropriate caution considering problems of the use of pristane/phytane ratios to reconstruct oxidation
state (ten Haven et al., 1987), and our restricted knowledge on the
depositional environment, these data favor a suboxic depositional
environment of low redox conditions.
Further support for the idea of suboxic, shallow water depositional settings within the Taoudeni Basin comes from relatively
high amounts of 17␣(H)-diahopanes (rearranged hopanes) – that
also occur as R/S-doublets (Fig. 7). These compounds behave
relatively refractory and have thus often been described from
strongly biodegraded and/or highly mature bitumens (Brocks and
Summons, 2003). However, diahopanes have also been reported
from non-degraded and less mature samples, suggesting an
unknown biological source. In Proterozoic organic matter, diahopanes have been occasionally found (Summons et al., 1988a,b;
Dutkiewicz et al., 2004). In black shales of the Touirist Formation diahopane/hopane ratios conspicuously increase with core
4.3.2. Sources of organic matter
Archaea were most likely no important contributors of organic
matter, as indicated by the lack of C40 isoprenoids (i.e. biphytanes). Likewise, the prevalence of n-alkanes and cyclohexylalkanes
in the low molecular weight range (C17 –C18 ) suggests a setting
dominated by bacteria and/or algae. However, steranes (regulars,
diasteranes, and aromatic steranes) were not found suggesting
modern eukaryotic algae to be, if any, only a minor source of organic
matter in the Late Mesoproterozoic Taoudeni Basin. Our results differ from findings of eukaryote-derived steranes in several other
Mesoproterozoic and older rocks, for instance in the 1.1 Ga Nonesuch Formation (Pratt et al., 1991). It is possible, however, that the
presence of abundant steranes in these samples result from contaminations (Brocks et al., 2008). Body fossils of eukaryotic algae
are well-known from Mesoproterozoic-aged and even much older
rocks (Butterfield, 2000; Javaux et al., 2004, 2010), but our results
support the suggestion that low-oxygen conditions and nitrate limitation may have permitted only limited environmental expansion
of eukaryotic algae prior to the end of the Mesoproterozoic (Anbar
and Knoll, 2002; Johnston et al., 2009).
The presence of cheilanthanes in the otherwise observed
sterane-free samples from the Touirist Formation indicates that
modern algae are not the primary source of these compounds,
unlike the suggestion of earlier studies (e.g. Greenwood et al.,
2000). In the Taoudeni Basin the vast majority of organic matter
was likely contributed by bacteria, as indicated by the generally high abundance of hopanes. The observed suite of C30 to C35
homologues with 22S/R-isomers of 17␣(H),21␤(H)-homohopanes
includes 2␣-methylated analogues, which are suggested to be
sourced by cyanobacteria (Summons et al., 1999). The contributions of cyanobacteria are therefore frequently described by the
2␣-methyl hopane index, which can often exceed 10% for other
Proterozoic samples (Summons et al., 1999). In the Touirist Formation black shales 2-methyl hopane indices are much lower
(1–2%, Table 3). 2␣-methylated hopanes, however, are neither an
exclusive biomarker for cyanobacteria nor do all cyanobacteria produce (2-methylated) hopanoids. For instance, in a recent study C-2
methylated hopanes were also found in anoxygenic phototrophs
(Rashby et al., 2007) and the enzyme system necessary for C-2
methylated hopanoid synthesis was observed in few soil bacteria (Welander et al., 2010). On the other hand, many modern
cyanobacteria, particularly marine taxa appear free of C-2 methylated hopanoids (Talbot et al., 2008). Consequently, low 2-methyl
hopane indices as calculated for the black shales of the Touirist Formation do not exclude appreciable contributions of organic matter
by cyanobacteria. Further support for organic matter considerably
sourced by cyanobacteria comes from the very low abundance of
gammacerane. Gammacerane is a diagenetic product of tetrahymanol, which often co-occurs with 2-methyl hopane producing
proteobacteria (Bravo et al., 2001; Rashby et al., 2007).
Indications for aerobic methanotrophic bacteria, which live
at chemoclines, were found. Type I methanotrophic bacteria are
reported to produce C-3 methylated hopanoids (Rohmer et al.,
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M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
1984; Zundel and Rohmer, 1985). Recently, the relative importance of contributions of methanotrophic bacteria to organic matter
was proposed to be calculable by the 3␤-methyl hopane index
(Brocks et al., 2005). 3␤-Methyl hopane indices for Touirist Formation black shale ranged between 3 and 5%. These values are
similar to the 1.64 Ga Barney Creek setting (average 5.7%), where
active methane cycling most likely occurred at an oxic-anoxic interface in the water column (Brocks et al., 2005). However, due to
the lack of other indications for anoxia in the overlying water
column, we propose that methanotrophic bacteria likely thrived
within the benthic microbial mats, specifically at the boundary
between suboxic and anoxic conditions in the top layers of the
mats.
Whereas intact aryl isoprenoids of chlorobiaceae (e.g. isorenieratane) or chromatiaceae (okenane; Schaeffer et al., 1997)
were absent from the black shales studied, potential break-down
products of isorenieratane, namely 2,3,6-trimethylated aryl isoprenoids were found in all samples (Fig. 9). These compounds
have often been observed in black shales and oils with abundant isorenieratene. However, respective aryl isoprenoids do
not necessarily derive from isorenieratene precursors. It has
been shown that severe degradation of other non-aromatic
carotenoids of common phototrophs (e.g., ␤- and ␥-carotene)
might also induce the formation of trimethylated aryl isoprenoids, including 2,3,6-trimethyl homologues (Hartgers et al.,
1994; Koopmans et al., 1996a,b). Isorenieratene and its degradation products can be identified by relative 13 C-enrichments
(e.g. Summons and Powell, 1987). However, due to co-elution
with other aromatic low molecular weight components, ␦13 Canalyses were impossible for the aryl isoprenoids from the Touirist
Formation. The predominance of 2,3,6-trimethylbenzenes with
different alkyl chains (C14 –C18 ) and the finding of a C21 2,3,6trimethylated isoprenoid with two benzene rings (e.g., Koopmans
et al., 1996a; Grice et al., 1997; Sinninghe Damste et al., 2001),
however, may be interpreted to reflect minor contributions from
anoxygenic phototrophs. If sourced by anoxygenic phototrophs, we
propose the respective organisms played an active role within stratified microbial mats, similarly to recent microbial mats which often
include anoxygenic phototrophic bacteria in the photic, anoxic, and
sulfidic layer below the immediate surface of the mats (Brocks
and Pearson, 2005; Ohkouchi et al., 2005). Consequently, in conjunction with the general phototrophic character of the mats this
would require a very shallow environment (0–30 m), which is also
indicated by microfacies results (Fig. 3).
The saturated and aromatic hydrocarbons from the black shales
from the Touirist Formation revealed ␦13 C-values between about
−29 and −35‰ (VPDB). Similar ␦13 C-values were also observed
in the kerogen of the black shales (Doering et al., 2009) as well
as for other Proterozoic hydrocarbons, which most likely derived
from benthic microbial mats (Logan et al., 1999). Pristane, phytane and hopanes were in the same range or slightly enriched in
13 C, in line with reports from the relationship between acyl- and
isoprenoidal lipids from cyanobacteria and other bacteria (Sakata
et al., 1997; Hayes, 2001). Table 5 demonstrates an increase in
␦13 C-values from the stratigraphically lowest to the highest black
shale sample, which also exhibits the highest amounts of hopanes.
However, the isotopic differences between the samples are small,
and possible reasons for this variation are difficult to interpret.
Staal et al. (2007) reported a positive relationship between bulk
␦13 C and the thickness of microbial mats grown in freshwater,
while an opposite trend was observed for marine mats (explained
by different degrees of carbon limitation and importance of heterotrophic turnover; Staal et al. (2007)). Given that the benthic
microbial mats of the Taoudeni Basin grew in a dominantly marine
environment, the observed increase in ␦13 C-values might be better explained by relatively higher microbial primary productivity,
as recorded by mat thickness and enhanced TOC within the stratigraphically highest black shale (Fig. 3). This might have reduced
carbon fractionation (i.e., 13 C-depletion), because high productivity may result in carbon substrate limitation during fixation
(Schidlowski et al., 1994). Given the complexity of carbon isotope
fractionation processes during organic matter biosynthesis, deposition, and dia-/catagenesis (e.g., Hayes, 1993), care has to be taken
when interpreting relatively small isotope variations like those
observed for the biomarkers in the black shales from the Touirist
Formation.
A marked characteristic of the Touirist Formation black shales
is the high aromaticity of the bitumens. This feature has also
observed in Archean- and Proterozoic-aged kerogens, but the
causes are unclear (Imbus et al., 1992; Brocks et al., 2003b; Marshall
et al., 2007). One common interpretation invokes evaporative fractionation in gaseous solutions which selectively enriches light
aromatics in the residual oil, thus shifting it to higher aromaticity (Thompson, 1987). This process, however, appears to primarily
affect oils in reservoirs, rather than source rocks. Another possible explanation for the high aromaticity in the black shales of
the Touirist Formation is a specific input of acritarch biopolymers, although the number of acritarchs is low. Acritarchs did
not strongly diversify until the Neoproterozoic, they were present
and occasionally abundant through the Mesoproterozoic (Javaux
et al., 2004; Huntley et al., 2006) and were recently observed in
rocks of an age of 3.2 Ga (Javaux et al., 2010). However, studies using combined micro-Fourier transform infrared spectroscopy
(FTIR) and laser micro Raman spectroscopy indicated that particularly Mesoproterozoic acritarchs contain biopolymers composed
of highly condensed aromatic sub-structures (Arouri et al., 2000;
Marshall et al., 2005) which may have contributed to the high
aromaticity of the Touirist Formation black shales studied. And
indeed, laser micro-Raman spectroscopy of palynomorphs collected from the Touirist Formation black shales revealed also
highest abundances of stretching bands (data not shown) typical for highly aromatic kerogen (at 1600 cm−1 ) (Marshall et al.,
2005). Against this background, it is interesting to see that
4␣,23,24-trimethylcholestane (dinosterane) was not found in these
samples. Dinosterane is commonly attributed to dinoflagellates
(Summons et al., 1987), but it has been reported to be abundant
in early Cambrian rocks (Moldowan and Talyzina, 1998) that predate by far their advent and rapid spread during the Mesozoic.
These findings suggest that specific acritarchs may be ancestors
of modern dinoflagellates. Our results suggest that the simple
acritarchs preserved in the black shales of the Touirist Formation were either not related to dinoflagellates (including a non
eukaryotic origin of the palynomorphs; e.g., cysts of prokaryotes), were unable to produce (dino)sterane, or were too low in
abundance to be reflected in the biomarker record. Although quantitative estimates from findings of microfossils and of biomarker
abundances in extractable organic matter and kerogen are delicate, the latter possibility would require additional explanation
for the extraordinary high aromaticity of the Touirist Formation black shales than acritarch biopolymers. Polycyclic aromatic
hydrocarbons may be also sourced by proteins and polysaccharides (Almendros et al., 1997; Marynowski et al., 2001), which
are abundant in nature, and particularly abundant in exopolymeric substances of benthic microbial mats (Wieland et al., 2008).
In addition, if the organic matter has been mainly produced
by microbial mats, those labile biopolymers were compared to
aliphatic lipids less affected by biodegradation, than organic matter which had to be transported through a water column. Thus,
cyclized biopolymers may provide an additional source for aromatic hydrocarbons in the Touirist Formation and perhaps also
for other Proterozoic kerogens originating from benthic microbial
mats.
M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127
4.4. On the predominance of (hopanoid-producing) prokaryotes
vs. eukaryotic algae in the Mesoproterozoic Taoudeni Basin
In contrast to earlier findings (Summons et al., 1988a; Brocks
et al., 1999; Waldbauer et al., 2009), several biomarker studies suggest that eukaryotic algae were less important than prokaryotic
organisms in Archaean and Proterozoic seas (e.g. Dutkiewicz et al.,
2004; Brocks et al., 2005, 2008). This observation is consistent with
other geological records (Knoll et al., 2006), and is further supported
by new data from the Taoudeni Basin, which shows the prevalence
of bacterial hopanes and the virtual absence of (eukaryote-derived)
steranes.
Although it has to be considered that steranes and hopanes
behave differently during biodegradation and maturation, with
hopanes showing a greater resistance to degradation than steranes (Seifert and Michael Moldowan, 1978; Peters and Moldowan,
1993), this holds only true at Peters–Moldowan level (PM) maturation and degradation levels >7; (Peters and Moldowan, 1993).
This is far beyond the most degraded sample from the Taoudeni
Basin (PM level ≤ 2 for MCS 1). Thus, the ratio between hopanes
and steranes (including aromatic steranes) in immature and moderately biodegraded Precambrian samples may be applied as a
relevant indicator on the distribution of ancient organisms. Given
that selective loss of steranes was only weak, high amounts of
hopanes and the observed lack of sterane peaks hint to bacteria
as the predominating component of the microbial communities
in the Taoudeni Basin as well as to an increasing contribution of
hopanoid-producing bacteria to the organic matter with decreasing
core depth.
Whereas the function of hopanoids in bacteria is still under discussion (Berry et al., 1993; Moreau et al., 1997; Doughty et al.,
2009; Welander et al., 2009), a recent survey demonstrated a high
overlap of bacteria producing hopanoids and those being capable of nitrogen-fixation (Pearson et al., 2007). Although the direct
role of hopanoids in the nitrogen-fixation process is questionable
(Doughty et al., 2009), high rates of hopanoid production appear to
be related to times of nitrogen deficiency and thus increased bacterial nitrogen-fixation (Eigenbrode et al., 2008; Blumenberg et al.,
2009, 2010). The nitrogen cycle in the Proterozoic is only poorly
understood. Several lines of evidences, however, indicate nitrogen
limitation, which has been explained by high rates of denitrification
at widespread oxic-anoxic boundaries. Although recently questioned (Klotz and Stein, 2008), it is generally assumed that nitrogen
fixation is an ancient metabolism. Therefore, in nitrogen-limited
areas of the early oceans, N2 -fixing bacteria may have had an advantage over other bacteria (Zerkle et al., 2006), and particularly over
modern eukaryotes (Anbar and Knoll, 2002 and references cited
therein). This situation might have prevailed through the Proterozoic, when oxygen and nitrate concentrations began to rise.
Abundant hopanoids in the black shales of the Touirist Formation may therefore be seen in support of a nitrogen-limited,
bacterially dominated scenario for the Taoudeni Basin, as it has
been suggested for other Mesoproterozoic settings (Fennel et al.,
2005).
5. Conclusions
Biomarker, microfacies, and palynological analyses of black
shales from the Late Mesoproterozoic Touirist Formation demonstrate that the majority of the highly abundant organic matter
(>20% TOC) was produced by benthic bacterial mats thriving
within the photic zone. The organic matter is of low maturity
and biomarkers (e.g. high diahopanes, low aryl isoprenoids) and
bulk geochemical analyses (high C/S-ratios) argue against pervasive euxinic conditions, supporting growth of the mats in a shallow,
125
suboxic environment. Unusually high amounts of aromatic hydrocarbons likely reflect a selective preservation of labile biopolymers
like exopolymeric substances rich in polysaccharides or proteins
in the microbial mats. Aerobic methanotrophy is indicated by
relatively high ratios of 3␤-methylhopanes. Varying but generally high amounts of hopanes may be interpreted in terms of a
nitrogen-limited setting that favored bacteria able to fix atmospheric nitrogen (diazotrophic (cyano)bacteria). Such a scenario is
consistent with models of Proterozoic oceans containing low concentrations of bioavailable nitrogen (nitrate, ammonia) due to loss
by denitrification. The practical lack of steranes further demonstrates that the palaeoenvironment of the Taoudeni Basin was
unfavorable for eukaryotic algae other than acritarchs, supporting
recent hypotheses on generally bacterially dominated Proterozoic
Oceans.
Acknowledgements
We thank Sascha Döring, Patrick-Oliver Reynolds, Andreas
Frischbutter and Geoff Gilleaudeau (University of Knoxville, Tennessee) for helpful discussions. We are also indebted to Cornelia
Conradt, Andreas Reimer and Birgit Röring for analytical support, to
Nadine Schäfer for help with Laser Micro-Raman Spectroscopy, and
to Jens Dyckmans from the “Centre for Stable Isotope Research and
Analysis” at the University of Göttingen for help with bulk and compound specific stable carbon isotope analysis. Jochen Brocks and
an anonymous reviewer are thanked for their helpful comments
considerably improving the manuscript. This work was financially supported by the Deutsche Forschungsgemeinschaft (grant
BL971/1-2 and 1-3) and the Courant Research Center of the University Göttingen. This is publication 83 of the Courant Research
Center Geobiology.
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