Biomarkers of Black Shales Formed by Microbial Mats, Late Mesoproterozoic

Precambrian Research 196–197 (2012) 113–127

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Biomarkers of black shales formed by microbial mats, Late Mesoproterozoic

(1.1 Ga) Taoudeni Basin, Mauritania

a,∗ a a b a

Martin Blumenberg , Volker Thiel , Walter Riegel , Linda C. Kah , Joachim Reitner

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

a b s t r a c t

Article history: Hydrocarbon biomarkers in Late Mesoproterozoic black shales from the Taoudeni Basin (Mauritania,

Received 6 May 2011

northwestern Africa) were analysed for palaeoenvironmental reconstruction. Within the Atar Group,

Received in revised form 31 October 2011

Touirist Formation shales showed the highest content of organic carbon (>20%) at very low maturity (Rc

Accepted 18 November 2011

less than 0.6). Microfacies and biomarker data indicate a shallow marine, high productivity, low oxygen

Available online 28 November 2011

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

Keywords:

reﬂecting the shallow depositional environment. Steranes were not observed, indicating only a minor

Late Mesoproterozoic

Biomarkers importance of modern, eukaryotic algae. Although low in abundance, a palynological survey, however,

Hopanes reveals the presence of simple ornamented acritarchs. Input of highly aromatic biopolymers typical of

High aromaticity Mesoproterozoic acritarchs or microbial exopolymeric substances may be the origin of an unusually high

Taoudeni Basin aromaticity observed for the biomarker extracts. High amounts of hopanes suggest that the benthic mats

Acritarchs 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.

1. Introduction has been speculated that stable anoxic and potentially sulﬁde-rich

deeper ocean waters were overlain by a shallow oxygenated upper

A wide variety of metabolisms were established in the Earth’s water column for most of the Proterozoic (Canﬁeld, 1998). Sup-

Oceans by 3.4 Ga (Allwood et al., 2006). However, the relative port for euxinic conditions in Proterozoic oceans comes from bulk

importance of different prokaryotic metabolisms and the timing C/S-ratios (Imbus et al., 1992; Shen et al., 2002) and the occur-

of evolution and expansion of eukaryotic life remain controversial rence of biomarkers in shales from the McArthur basin (1.64 Ga),

(Rasmussen et al., 2008; Javaux et al., 2010). Prior to 2.4 Ga Earth’s where euxinic conditions obviously extended into the photic zone

oceans harbored exceptionally low sulfate concentrations, and oxy- (Brocks et al., 2005). If persistent, photic zone euxinia may have

gen free deep waters with highly abundant ferrous Fe (Canﬁeld, fueled anoxygenic phototrophy using H2S as electron donor, yet

2005). Although oxygen began to accumulate after about 2.4–2.2 Ga it is unclear whether this mode of primary production occurred

(the “Great Oxidation Event”) it took at least until the end of the only in speciﬁc basins or, as it has been proposed, characterised the

Precambrian for deep oceanic water masses to show substantial entire Proterozoic (Johnston et al., 2009). A more complete under-

signs of increasing sulfate concentrations and oxygenation (Kah standing of the distribution of low-oxygen environments and their

et al., 2004; see Kah and Bartley (2011) for a review). Rather, it 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 bil-

Corresponding author. Tel.: +49 0 551 3913756; fax: +49 0 551 397918.

E-mail address: [email protected] (M. Blumenberg). lions of years and can be valuable sources for information on

114 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 et al., 2009), which is consistent with Re-Os ages of 1107 ± 12 Ma,

stable isotope signatures have the potential to shed light on the 1109 ± 22 Ma and 1105 ± 37 Ma for black shale within the Atar/El

prevailing organisms as well as on the metabolic pathways and car- Mreiti Group (Rooney et al., 2010). With the exception, however,

bon sources. Although biomarker data is still limited in its extent, of ␦ C analyses on stromatolitic fabrics of the Atar Group (Teal

it provides substantial insights into life in Earth’s early oceans and Kah, 2005; Kah and Bartley, 2011), recent facies analysis of

(Mycke et al., 1988; Summons et al., 1988a,b, 1999; Pratt et al., stromatolite-bearing strata (Kah et al., 2009), and a single report

1991; Logan et al., 1995, 2001; Brocks et al., 1999; Greenwood on general geochemical characteristics of the Touirist Formation

et al., 2004; Eigenbrode et al., 2008; Waldbauer et al., 2009). Unfor- organic matter (Doering et al., 2009), there has been little study con-

tunately, recent studies (Brocks et al., 2008; Rasmussen et al., cerning the biological make-up of Atar/ElMreiti Group strata and its

2008; Brocks, 2011) have indicated that at least some of the environmental interpretation. Here we report the ﬁrst biomarker

biomarkers inventories presented in the above mentioned stud- studies of Taoudeni Basin strata (Touirist Formation) and use an

ies were not syngenetic to their host rock but rather the result of approach to the interpretation of depositional environments based

anthropogenic contaminations with hydrocarbons. Consequently, on biomarkers, stable isotope signatures, microfacies, and paly-

some interpretations regarding the distribution of prokaryotic and nology. Results of this study provide compelling evidence on the

eukaryotic communities in the Precambrian are now being ques- authenticity of the biosignatures and allow for a robust reconstruc-

tioned (e.g., the early rise of modern eukaryotic algae based on tion of a Late Mesoproterozoic highly productive, shallow marine

ﬁndings of abundant steranes; Brocks (2009)). This and the low setting.

number of localities providing valuable biomarker information

stress the need of additional studies from a variety of Precambrian 2. Materials and methods

settings.

The Taoudeni Basin, northwestern Africa, records a discontin- 2.1. Rock samples

uous sedimentation history from the Proterozoic to the Cenozoic,

and contains a thick succession of Proterozoic-aged sedimentary Core samples were drilled in 2007 (for site see Fig. 1). Bisects

rocks. These rocks of the Taoudeni Basin include two supergroups, of the core (4 samples) were used for biomarker, microfacies, and

the lower of which (Supergroup 1) rests unconformably on Archean palynological analyses (for positions in the lithological section see

to Paleoproterozoic basement and consists of the Char, Atar/El Mre- Fig. 2). For biomarker studies, bisects were separated into exterior

iti, and Assabet el Hassiane/Bir Amrane Groups. Carbon-isotope and interior parts, and both samples were analysed individually.

∼

chemostratigraphy has determined the 800 m thick Atar/El Mreiti A clean precision saw (Buehler IsoMet 1000) was used, which

Group to be late Mesoproterozoic in age (Teal and Kah, 2005; Kah 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)

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 com-

paring mass spectra and retention times with published data

and/or reference compounds. The GC was equipped with a deac-

tivated 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 car-

◦

rier 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 oper-

◦

ated at 200 C in electron impact mode at 70 eV ionisation energy.

Fractions were injected on column using a PTV injector. The injec-

◦

tor 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 ana-

lysed (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,

Fig. 2. Simpliﬁed lithologic section of the investigated core with TOC and Tmax trends

because of better peak resolutions. The detection limit for steranes

(unpublished results) and the position of the analysed rock samples.

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 dilu-

acetone. Samples were then crushed and powdered using a pebble

tions used, ∼0.5 ppm of the saturates fraction. For dinosterane it

mill (Retsch MM 301) that was pre-cleaned with solvents and

was slightly higher (20 pg in general, representing ∼1 ppm of the

sand. Bulk C/N/S analysis was performed using a Hekatech Euro

saturates fraction).

EA CNS analyser. To determine the contents of TOC and carbonate

Trimethylated aryl isoprenoids were identiﬁed by selective

carbon (Ccarb), each sample was analysed both before and after

13 15 MRM transitions and comparison with the aromatic fraction of a

acidiﬁcation with HCl. Bulk ␦ C and ␦ N isotope analysis was

Jurassic black shale (Bächental, Toarcian), that contains abundant

made via elemental analysis-isotope ratio mass spectrometry

isorenieratene and isorenieratene degradation products (Köster

(EA-IRMS, Delta plus, Thermo Finnigan).

et al., 1995).

For the detection of potential contaminations, the exterior and

␦13

The C-values of hydrocarbons were analysed (minimum of

interior parts of the drill core bisects were compared. Gener-

three replicates) using a Thermo Scientiﬁc Trace GC coupled to a

ally, both yielded similar hydrocarbon compositions indicating

Delta Plus isotope-ratio MS. The combustion reactor contained CuO,

only minor external contamination. Moreover, branched alkanes

◦

Ni, and Pt and was operated at 940 C. The GC was equipped with

with quarternary carbon (BAQCs) were not found in any sample,

a Zebron ZB-5MS (30 m; 0.25 ␮m ﬁlm thickness, and 0.32 mm i.d.)

which excludes the possibility of appreciable contamination from

and runs using a temperature program identical to that described

polyethylene plastic bags (Brocks et al., 2008).

above. The stable carbon isotope compositions are reported in the

delta notation (␦ C) vs. the VPDB standard. Standard deviations for

␦

2.2. Extraction and fractionation C analyses were generally less than 1‰ and sometimes higher

due to bad peak separation or inﬂuences from co-eluting unre-

∼

Ground samples ( 10 g) were subjected twice with distilled solved complex mixtures.

∼

dichloromethane (DCM)/n-hexane (9/1; 100 ml each) using ultra- Selected samples were subjected to Laser-ICP-MS analyses per-

sonication followed by extraction of hydrocarbons with n-hexane formed according Sánchez-Beristain et al. (2010) and to micro

(100 ml). Extracts were combined and concentrated in a pre- carbonate carbon stable isotope analyses according to Delecat et al.

cleaned rotary evaporator, followed by reduction of the solvent to (2010), respectively.

near dryness in a stream of N2. The resulting total extracts were sep-

arated by column chromatography into a saturated fraction (F1), an

aromatic fraction (F2) and a polar residue. 7.5 g of dry silica gel 60 2.4. Palynology

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 One sample (sample MCS 4) was prepared for palynological

onto the column. F1 was eluted with 1.5 dead volumes of n-hexane analysis by demineralisation with HCl and HF. In order to mechan-

(15 ml), F2 with two dead volumes n-hexane/DCM (1/1; 20 ml) and ically dissociate the organic matrix and disintegrate remaining

the polar residue with 20 ml DCM/methanol (1/1). Fractions were larger particles, the residue was crushed in a mortar, brieﬂy boiled

concentrated by careful rotary evaporation, dried under a stream of in 15% H2O2 and exposed to ultrasonic treatment. Fine detritus was

␮ ␮

N2 and dissolved in 200 l n-hexane (F1) and 1500 l (F2), respec- removed by screening at 15 ␮m mesh size. The residue was stored

tively. To remove elemental sulfur reduced copper was added to F1 in glycerine and three permanent preparations were mounted in

and F2. glycerine jelly. Because of their scarcity within the bulk matrix,

116 M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127

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 paly-

nomorphs (not shown). The spectra were dominated by stretching

−1

band at 1600 cm (typical for C C bonds like in aromatic rings)

−1

with only weak signals at 1345 cm (speciﬁc for CH3) (not shown).

3.3. Microfacies

Microfacies analyses revealed layered occurrences of organic

matter with occasionally abundant pyrite (Fig. 3). In the strati-

graphically 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 non-

luminescent 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

Fig. 4. Statistical size distribution of palynomorphs in sample MCS 4.

within the calcite crystals (Laser ICP-MS analyses; data not shown).

Assumably, these high Mn values are primary signals, reﬂect-

palynomorphs were picked individually for photography under

ing negative redox conditions during mineralisation process. The

transmitted light, SEM, and Laser micro-Raman spectroscopy.

later diagenetic carbonate crystals do not show any luminescence,

demonstrating a different redox environment. Comparable struc-

3. Results tures were observed in methane-related carbonates from the Black

Sea which were formed under anoxic conditions (Reitner et al.,

3.1. Bulk geochemical characteristics 2005). Therefore, the luminescent laminae are most likely lithi-

ﬁed former bioﬁlms with the strong luminescent anhedral calcites

TOC of the investigated Touirist Formation black shales were to be probably small lithiﬁed microbial communities. Those are

high (10.1–22.2%; Table 1) and showed even more elevated con- embedded in a former matrix of exopolymeric substances, which

centrations in the stratigraphic highest section (see also Fig. 2). is now weakly calciﬁed with only minor red luminescence. Compa-

Ccarb values were generally low (0.1–0.5%; Table 1) and sulfur con- rable lithiﬁed microbial laminae are also known from the Sturtian

centrations were variable (0.8–3.1%), again with most elevated Rasthof cap carbonates from Namibia (Pruss et al., 2010). Pyrite

␦13

concentrations high in the stratigraphic section. Bulk carbon C is occasionally associated with calciﬁed microbial mats. The small

−

values showed an increasing trend from 33.9‰ vs. VPDB low in strong luminescent calcite crystals are probably lithiﬁed microbial

−

the stratigraphic section to 29.7‰ in the stratigraphically highest colonies located within the microbial mats. Selected carbon sta-

sample. Bulk nitrogen stable isotopes ﬂuctuated between +4.9 and ble isotope analyses of the automicrite mineral exhibit relatively

13 13

+6.1‰ (vs. air) and showed no trend with respect to core depth. C depleted values (␦ C = −16‰ VPDB) which is in the range

described from carbonates formed during microbial sulfate reduc-

3.2. Palynology tion (Raiswell and Fisher, 2000) and are thus in agreement with

a similar source than that for abundant pyrite crystals within the

Palynomorphs recovered are predominantly simple more or less calciﬁed microbial mats.

smooth-walled sphaeromorph acritarchs without distinct opening

structure which can be classiﬁed as Leiosphaeridia sp. (Fig. 3A–D;). 3.4. Biomarkers

Fig. 4 shows the statistical size range of palynomorphs in sam-

␮

ple MCS 4 with a peak between 20 and 40 m (n = 125). However, Extractable hydrocarbons consisted mainly of saturated (n-

␮

individual larger leiospheres with a diameter up to 125 m were alkanes, cycloalkanes, methylated alkanes, isoprenoids) and

also observed. Rather well deﬁned round to oval microstrucutres, aromatic compounds, with generally low saturate/aromatic-ratios

which are solid, lenticular in cross section and range in size mainly (<0.1; Table 2).

between 200 ␮m and 400 ␮m (Fig. 3A) are a striking component of

the maceration residue. They occur isolated or in clusters and show 3.4.1. Saturates (C15+)

a distinct orange ﬂuorescence with blue light irradiation. They are Patterns of saturated hydrocarbons differed slightly between

tentatively considered here as growth forms of bacterial colonies the samples, but all contain n-alkanes (C15+) ranging from

signiﬁcantly contributing to the formation of the microbial mats. 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).

118 M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127

Table 1

Geochemical parameters of black shales of the Touirist Formation (Taoudeni Basin).

13 15

Sample Formation TOC (%) Ccarb (%) S (%) N (%) C/N C/S ␦ C bulk ␦ N bulk

MCS 1 Touirist (Atar Group) 22.2 0.1 3.1 0.5 45.8 7.3 −29.7 +5.9

MCS 2 Touirist (Atar Group) 17.2 0.1 2.1 0.4 43.4 8.3 −30.6 +5.2

MCS 3 Touirist (Atar Group) 16.1 0.1 0.9 0.4 40.7 17.9 −31.1 +4.9

MCS 4 Touirist (Atar Group) 10.1 0.2 0.8 0.2 44.1 12.3 −33.8 +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.

preference indices (CPI) were about 1 for all samples (0.95–1.05).

Cyclohexylalkanes demonstrated similar patterns as n-alkanes, but

Table 2 maximized at slightly higher carbon numbers (Fig. 5; maximum

Amounts of saturated and aromatic hydrocarbons.

cyclohexyalkane C18 vs. C17 for n-alkanes). Phytane, pristane and

norpristane were observed in signiﬁcant amounts (Fig. 5). Pris-

Sample Saturates (ppm) Aromatics (ppm) Saturates/aromatics

tane to phytane ratios ranged from 0.64 to 1.01 (Table 3). Pristane

MCS 1 360 6040 0.06

to C17 and phytane to C18 ratios ranged from 0.24 to 0.35 and

MCS 2 180 3760 0.05

MCS 3 250 5330 0.05 0.21 to 0.31, respectively (except for the topmost samples; Pr/n-

MCS 4 370 4280 0.09 C17 = 1.21 and Ph/n-C18 = 0.74). Acyclic isoprenoids with carbon

M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127 119

Table 4

Maturity indices (aromatic hydrocarbons) of black shales from the Touirist Fm. from

the Taoudeni Basin. *Most likely affected by biodegradation. Methylphenanthrene 0.79 0.56 0.66 0.18

Hopane index

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.

b Sample MPI-1 Phen/MP MPR R (MPI-1)

-Me-Index c ␤

3 3 5 4

3 (%)

MCS 1 0.49 0.03* 0.52 0.56

MCS 2 0.51 0.24 0.63 0.57

MCS 3 0.43 0.34 0.61 0.52

MCS 4 0.36 0.33 0.53 0.47 a -Me-Index ␣

2 (%) 1 1 1 2

numbers higher than C20 (phytane), e.g. C40-isoprenoids, were not

observed. 0.09 0.12 0.24 0.35 Dia/C30

3.4.2. Aromatic steroids and steranes

Tm)

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 0.42 0.42 0.40 0.53 Ts/(Ts

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

chei22/21 1.61 1.93 1.96 2.19

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 0.69 0.53 0.42 0.45 chei24/23

steranes were also under detection limit, even when highly selec- )

tive SIM or MRM modes were applied (according to Summons et al., (C

1987). This includes dinosteranes, which could not be detected

→ →

. using the 414 231 and 414 98 transitions. . 0.57 0.56 0.57 0.61

22S/22R

The presence of aromatic steroids as well as aromatic ring-

(2008) methylated (e.g. 4-methyl) steranes was also tested by speciﬁc

(1999)

al.

→ MS–MS transitions (m/z 344 231 (or 245; ring-methylated); al.

→ → → et 358 231 (or 245); 372 231 (or 245); 386 231 (or 245);

400 → 231 (or 245)). None of these transitions showed resolved 0.12 0.20 0.10 0.27 C24tetra/C30

peaks. Summons Eigenbrode

3.4.3. Hopanes and cheilanthanes hopanes after after

terpanes). ␣ The highest relative amounts of hopanes were observed in the

Basin)..

stratigraphically highest sample and were clearly detectable even MRM), MRM),

from total ion chromatograms (Fig. 5). Hopanes in all samples

(tricyclic

consist of C –C compounds, and generally show most signif-

from from 27 35

(Taoudeni

0.20 0.34 0.27 0.49

Tricyclics/17

icant abundances of 17␣(H),21␤(H)-C30 (17␣(H),21␤(H)-hopane;

Fm. than than

Fig. 7). 22S/22R-isomerisation ratios for homohopanes were at

∼

about 0.6 (Table 3). Diahopanes were found in varying amounts, Steranes np np np np

cheilanthanes

␣ ␤ Touirist

with decreasing ratios of C -diahopane vs. 17 (H),21 (H)-hopane 30

resolution resolution

the from the lowermost to the topmost sample (from 0.35 to 0.09).

chei.: 0.95 0.98 CPI 1.03 1.05

Minor to moderate concentrations of ring A methylated hopanes peak peak

from

and ␣

were observed with a 2 -methyl hopane index of 1–2% (calcu- max

TIC. C

␤ - lated after Summons et al., 1999) and a 3 -methyl hopane index better better n 18 18 18 17

shales

to to of 3–5% (calculated after Brocks et al., 2005). 29,30- and 28,30-

from

Bisnorhopanes (BNH) were only slightly above detection limit in -C

black transitions)

(due (due n

of all samples (Fig. 7).

0.74 0.21 0.23 0.30 Ph/

SIM SIM

A suite of C19–C25 tricyclic terpanes (cheilanthanes) were 17 MS–MS

also observed in all samples. Moreover, all samples showed an

-C from from

n +

abundance of tetracyclic C24 terpane (M 330), most likely 17,21- 0.24 0.24 0.28 Pr/ 1.21 (%); (%);

-hopane+phytane); secohopane (C ) (see Aquino Neto et al., 1983). speciﬁc 24

␤ hydrocarbons)

Ph)

,21 +

␣

3.5. Aromatic hydrocarbons 0.49 0.39 0.50 0.49 Pr/(Pr MeC31+C30) MeC31+C30) (saturated

␣ ␤

Aromatic hydrocarbons were present in all samples and con- (conﬁrmed

tained high relative concentrations of dimethyl- and trimethyl -hopane/(17 0.94 0.64 0.98 Pr/Ph 1.01 indices ␤

naphthalenes, phenanthrene, dimethyl- and trimethyl phenan-

,21 present

1 2 3 4

-MeC31/(2 -MeC31/(3

␣ threnes, chrysene and methylated chrysene(s) (Fig. 8) and

␣ ␤ not

2 3 17

were used to calculate maturity indices (Table 4). In the c a Sample b MCS MCS MCS MCS

Table np:

Biomarker stratigraphically highest sample (MCS 1) low molecular weight

120 M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127

Hopanes and diahopanes

Ch23 Ch21 17,21-seco- Tm Ch 19 hopane (C24) Ts e.g. Ch20 Ch24

Ch25 SIMm /z 191

no steranes and diasteranes e.g.

? ? ? SIMm /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 section, whereas the stratigraphically highest samples showed an

stratigraphically lower horizons. enrichment in C of about 4–5‰ (similar to bulk stable carbon

Moreover, except for minor amounts of methylated chrysenes isotopes; compare Table 1 and Table 5).

no polycyclic aromatic hydrocarbons (PAHs) of higher molecular

weight were observed. 4. Discussion

3.5.1. Aromatic carotenoids 4.1. Syngeneity of biomarkers

Long-chain carotenoids (e.g. isorenieratene) and derivatives

were not detected even after application of speciﬁc SIM and MS–MS Establishing a syngenetic relationship of the bitumen with its

transitions (according to Brocks and Schaeffer (2008)). However, host rock is an underlying requirement for any attempt to interpret

alkylated trimethylbenzenes with dominantly 2,3,6-methylation Precambrian ecosystems by means of hydrocarbon biomarkers. A

→

were found after performing M 134 transitions (exempliﬁed number of observations allows the critical assessment of whether

for sample MCS 4; Fig. 9). The methylation pattern was con- the measured compounds were originally part of the host rock. (i)

ﬁrmed after coinjection with a black shale rich in isorenieratane First, the biomarker distributions in the exterior and interior parts

and its break-down products (Bächental, Toarcian; see also Köster of the cores are virtually identical (Table 6), pointing to the absence

et al. (1995)). The alkylated trimethylbenzenes in the Bächental of drilling contamination. (ii) Second, the virtual lack of steranes

sample are predominantly composed of 2,3,6-trimethyl aryl iso- (including dinosterane) and of higher plant-derived triterpanes

prenoids and exhibit similar distribution to other Toarcian black suggest the absence of substantial contamination by Phanerozoic

shales (Schwark and Frimmel, 2004). In the Touirist Formation, organic matter. (iii) Thirdly, indices describing the maturity of the

an additional short chain C21 diaryl isoprenoids (LIII in Koopmans bitumen (MPI-1; Ts/(Ts + Tm); see below) coincide and are in good

et al. (1996a)) was also observed. However, in Touirist Forma- agreement with bulk geochemical maturity assessments (i.e. Tmax

13 13

tion shales abundant other aryl isoprenoids and aryl alkanes, values; Fig. 2). (iv) Finally, bulk ␦ C and biomarker ␦ C values are

in addition to 2,3,6-methylated isomers, were also found, much similar, suggesting similar organic sources. In conjunction, these

higher than reported from Toarcian shales rich in isorenieratene indications yield compelling evidence that the saturated and aro-

(Schwark and Frimmel, 2004). Those samples often exclusively matic hydrocarbons extracted from the Late Mesoproterozoic black

include 2,3,6-trimethyl aryl isoprenoids. All shales demonstrated shales of the Touirist Formation are syngenetic and have not been

similar distributions of trimethylbenzenes (not shown). introduced at a later stage

3.6. Stable carbon isotopes 4.2. Maturity and biodegradation

Stable carbon isotope signatures of saturated and aromatic Effects of biodegradation, namely an increase of phytane/n-

hydrocarbons were analysed for all shales. N-alkanes and acyclic C18 and hopanes, and an apparent loss of low molecular weight

␦13 isoprenoids had C values between approximately −30 and PAHs are indicated for the stratigraphically highest sample. More-

−

35‰ (VPDB; Table 5). Generally, n-alkyl hydrocarbons were sim- over, almost all samples exhibit pronounced unresolved complex

␦13 13 ilar in C or slightly C-depleted compared to phytane. Hopanes mixtures (UCM), although low molecular weight saturates (C15+)

were found to be slightly less depleted in C compared to acyclic were still present in high amounts. Methyl phenanthrene ratios

compounds. Polycyclic aromatic hydrocarbons demonstrated sim- (MPR) ranged between 0.52 and 0.63. Based on phenanthrene

∼ ilar ranges to that found for saturates. However, we did observe to methyl phenanthrene ratios <1 ( 0.24 to 0.34) (Brocks et al.,

that the strongest C-depletions occurred low in the stratigraphic 2003a) and methyl phenanthrene indices (MPI-1) between 0.36

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 and Killops (2005)) and references therein) and are consistent

␣

were calculated after Boreham et al. (1988); see Table 4 for with observed ratios of 18 -22,29,30-trisnorneohopane (Ts) to

␣

details). These computed vitrinite reﬂectance values correspond 17 -22,29,30-trisnorhopane (Tm); Ts/(Ts + Tm) of about 0.40–0.53

to low maturities (early oil window to peak oil window; Killops (Table 3). Three samples display relatively low pristane/n-C17 ratios

MP chrysene P DMP TMN methyl chrysenes perylene DMN diP TMP 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 C.

Sample MCS 1 MCS 2 MCS 3 MCS 4

␦13 13 13 13

C (mean) ± ␦ C (mean) ± ␦ C (mean) ± ␦ C (mean) ±

n-C15 −35.6 0.3 −30.5 0.1

− −

n-C16 35.2 0.6 32.9 0.2 −33.2 1.8 −30.5 0.5

Cyclohexyl-C10 −34.9 0.7 −32.5 0.6 −32.4 1.1

n-C17 −35.4 −33.5 0.6 −34.3 1.4 −30.5

Pristane −35.2 0.1 −32.6 1.9 −30.7

Cyclohexyl-C11 −34.5 1.3 −32.8 0.4 −32.1 0.6 −29.2 1.1

n-C18 −35.2 0.8 −33.7 0.1 −33.4 0.6 −29.8

−

Phytane −34.3 1.8 32.1 0.1 31.2 1.7 −29.9

− −

Cyclohexyl-C12 35.1 3.0 32.2 1.0 −29.8 0.1 −27.6

n-C19 −34.7 1.3 −33.9 0.4 −31.2 0.6 −30.2 0.8

n-C20 −34.9 0.8 −33.3 1.3 −32.3 1.8 −31.2 0.3

n-C21 −34.2 0.8 −32.1 1.1 −32.1 2.1 −30.0 0.9

n-C22 −35.3 1.5 −32.3 1.9 −31.9 1.7 −32.4 3.3

n-C23 −33.9 1.1 −31.2 1.2 −31.1 0.0 −31.3 0.6

n-C24 −35.1 0.6 −32.8 −30.6 0.8 −29.1

18␣-22,29,30-Trisnorhopane (Ts) −28.5

17␣-22,29,30-Trisnorhopane (Tm) −26.9

30-Norhopane −31.9

17␣(H),21␤(H)-Hopane −29.6 2.1 −28.8 1.5 −29.0

22S-17␣(H),21␤(H)-Homohopane −29.7

Phenanthrene −33.1 0.5 −30.8 1.0 −29.7 1.1

3-Methylphenanthrene (3-MP) −34.2 0.8 −32.3 0.4 −30.5 0.3

2-Methylphenanthrene (2-MP) −34.9 0.9 −32.5 0.8 −30.5 0.4

9-Methylphenanthrene (9-MP) −35.3 2.9 −32.3 1.8 −30.8 0.4 −30.3 0.8

−

1-Methylphenanthrene (1-MP) 33.6 1.1 −31.8 2.4 −30.1 0.8

Chrysene −32.9 1.6 −30.9 1.0 −28.5 0.1 −30.8 0.4

(0.21–0.35), in line with other Proterozoic rock samples (Fowler and information on the biota of the Taoudeni Basin and differences

Douglas, 1987; Summons et al., 1988b; Dutkiewicz et al., 2004). The between the four sampled periods of black shale formation within

pristane/n-C17 ratio in the stratigraphically highest sample (MCS 1) the Touirist Formation. Increasing TOC and S-concentrations

was considerably higher (1.21) than those of the other samples. suggest that the generally high primary production (and/or degree

But, even for MCS 1 these values corresponded to only light – of preservation) increased from the lower to the upper Touirist

most likely postdepositional biodegradation (PM 2) according to Formation. Although C/S ratios have to be used with caution for Pro-

the Peters–Moldowan biodegradation scale (Peters and Moldowan, terozoic samples (e.g. Shen et al., 2002), a comparison with modern

1993). However, we also must consider the potential impact from marine settings (e.g. euxinic Black Sea; <3; (Berner, 1984) suggests

calibration of this biodegradation scale for Phanerozoic organic the lack of extensive euxinic conditions in the water column during

matter, which typically shows appreciable contributions of the deposition of the Touirist Formation (7.6–12.6). Euxinia, however,

acyclic isoprenoids pristane and phytane. Low inputs of these is believed to be prevalent through the Proterozoic (Canﬁeld, 1998;

isoprenoids, as observed for the Mesoproterozoic samples, may Kah and Bartley, 2011). Absence of euxinia above the microbial

inﬂuence the pristane/n-C17-ratios and phytane/n-C18 ratios a pri- mats deposited in the Touirist Fm. may reﬂect the shallow-water

ori which makes it difﬁcult to resolve the extent of biodegradation. setting and the potential for diffusion of oxygen into the upper

Due to the presence of unresolved complex mixtures and the pro- water column from the atmosphere or the effects of episodic storm

nounced loss of low molecular weight compounds (saturates and mixing. Both the onset of widespread sulfate evaporite deposition

aromatics), we assume that moderate biodegradation affected par- in the Mesoproterozoic (Kah et al., 2001; Goodman and Kah, 2004),

ticularly the stratigraphically highest sample (MCS 1). and depletion of Mo concentrations from similarly aged black shale

(Lyons et al., 2009) support the potential for suboxic conditions pre-

vailing in shallow waters by the late Mesoproterozoic. Moreover,

4.3. Palaeoenvironmental implications

a stable chemocline in the photic zone and euxinia below (photic

zone anoxia) was recently reconstructed for the Barney Creek

4.3.1. General aspects

Formation (1.64 Ga), which yielded high amounts of biomarkers

Black shales in the Taoudeni Basin were deposited in the

of anoxygenic phototrophs, such as isorenieratane, okenane, and

Late Mesoproterozoic at about 1.1 Ga (Rooney et al., 2010). The

respective break-down products (Brocks et al., 2005; Brocks and

shales studied contain high amounts of organic matter (10–22%)

Schaeffer, 2008). Intact carotenoid derivatives were not found in

and increase in the lithological section to almost 30% (Fig. 2).

the Touirist Formation black shales, thus evidence for photic zone

They were formed in marine, epeiric water environments, under

euxinia in the water column above the microbial mats is lacking.

potentially shallow water (Kah et al., in review; Bertrand-Sarfati

Findings of potential break-down products of isorenieratane in

and Moussine-Pouchkine, 1988). Our data reveal additional

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 0.98 0.28 0.30 17 0.98 np 0.49 0.61 0.53 0.35

MCS 4 exterior 0.75 0.28 0.31 18 1.05 np 0.43 0.61 0.53 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 sim-

ilar 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 shal-

low, suboxic depositional environment, where diahopanes often

occur in high amounts (Peters et al., 2004a). The water depth dur-

ing deposition of benthic mats reﬂected in sample MCS 1 appear to

have been particularly shallow, since the occurrence of microrip-

ples suggests deposition above wave base (Fig. 3J).

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. biphy-

tanes). 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 dif-

fer from ﬁndings of eukaryote-derived steranes in several other

Mesoproterozoic and older rocks, for instance in the 1.1 Ga None-

such Formation (Pratt et al., 1991). It is possible, however, that the

presence of abundant steranes in these samples result from con-

taminations (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 lim-

itation 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,

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 unlike the suggestion of earlier studies (e.g. Greenwood et al.,

speciﬁc multiple reaction monitoring (MRM) transitions (a, b, c, d, e). The 2,3,6- 2000). In the Taoudeni Basin the vast majority of organic matter

trimethylation pattern of the denoted benzenes was conﬁrmed by coinjection of

was likely contributed by bacteria, as indicated by the gener-

MCS 4 with an aromatic hydrocarbon fraction from a Jurassic black shale (a , b ,

ally high abundance of hopanes. The observed suite of C30 to C35

c , d , e ; Bächental, Toarcian; see Section 2). Asterisks denote 2,3,6-trimethyl aryl

␣ ␤

isoprenoids identiﬁed from coinjection. 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 contribu-

the Touirist Fm. shales may however be interpreted to reﬂect (i) tions of cyanobacteria are therefore frequently described by the

␣

euxinia in deeper waters of the basin, (ii) intermittent euxinia 2 -methyl hopane index, which can often exceed 10% for other

above the shallow-water microbial mats, and/or (iii) contributions Proterozoic samples (Summons et al., 1999). In the Touirist For-

from green-sulfur bacteria living in the stratiﬁed mats. mation black shales 2-methyl hopane indices are much lower

Pristane/phytane ratios (0.8–1.0) neither suggest extremely (1–2%, Table 3). 2␣-methylated hopanes, however, are neither an

reductive ( 1) nor oxidative ( 1) conditions of early diagenesis exclusive biomarker for cyanobacteria nor do all cyanobacteria pro-

(Peters et al., 2004b). With appropriate caution considering prob- duce (2-methylated) hopanoids. For instance, in a recent study C-2

lems of the use of pristane/phytane ratios to reconstruct oxidation methylated hopanes were also found in anoxygenic phototrophs

state (ten Haven et al., 1987), and our restricted knowledge on the (Rashby et al., 2007) and the enzyme system necessary for C-2

depositional environment, these data favor a suboxic depositional methylated hopanoid synthesis was observed in few soil bacte-

environment of low redox conditions. ria (Welander et al., 2010). On the other hand, many modern

Further support for the idea of suboxic, shallow water depo- cyanobacteria, particularly marine taxa appear free of C-2 methy-

sitional settings within the Taoudeni Basin comes from relatively lated hopanoids (Talbot et al., 2008). Consequently, low 2-methyl

high amounts of 17␣(H)-diahopanes (rearranged hopanes) – that hopane indices as calculated for the black shales of the Touirist For-

also occur as R/S-doublets (Fig. 7). These compounds behave mation do not exclude appreciable contributions of organic matter

relatively refractory and have thus often been described from by cyanobacteria. Further support for organic matter considerably

strongly biodegraded and/or highly mature bitumens (Brocks and sourced by cyanobacteria comes from the very low abundance of

Summons, 2003). However, diahopanes have also been reported gammacerane. Gammacerane is a diagenetic product of tetrahy-

from non-degraded and less mature samples, suggesting an manol, which often co-occurs with 2-methyl hopane producing

unknown biological source. In Proterozoic organic matter, dia- proteobacteria (Bravo et al., 2001; Rashby et al., 2007).

hopanes have been occasionally found (Summons et al., 1988a,b; Indications for aerobic methanotrophic bacteria, which live

Dutkiewicz et al., 2004). In black shales of the Touirist Forma- at chemoclines, were found. Type I methanotrophic bacteria are

tion diahopane/hopane ratios conspicuously increase with core reported to produce C-3 methylated hopanoids (Rohmer et al.,

124 M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127

1984; Zundel and Rohmer, 1985). Recently, the relative impor- as recorded by mat thickness and enhanced TOC within the strati-

tance of contributions of methanotrophic bacteria to organic matter graphically highest black shale (Fig. 3). This might have reduced

was proposed to be calculable by the 3␤-methyl hopane index carbon fractionation (i.e., C-depletion), because high produc-

(Brocks et al., 2005). 3␤-Methyl hopane indices for Touirist For- tivity may result in carbon substrate limitation during ﬁxation

mation black shale ranged between 3 and 5%. These values are (Schidlowski et al., 1994). Given the complexity of carbon isotope

similar to the 1.64 Ga Barney Creek setting (average 5.7%), where fractionation processes during organic matter biosynthesis, depo-

active methane cycling most likely occurred at an oxic-anoxic inter- sition, and dia-/catagenesis (e.g., Hayes, 1993), care has to be taken

face in the water column (Brocks et al., 2005). However, due to when interpreting relatively small isotope variations like those

the lack of other indications for anoxia in the overlying water observed for the biomarkers in the black shales from the Touirist

column, we propose that methanotrophic bacteria likely thrived Formation.

within the benthic microbial mats, speciﬁcally at the boundary A marked characteristic of the Touirist Formation black shales

between suboxic and anoxic conditions in the top layers of the is the high aromaticity of the bitumens. This feature has also

mats. observed in Archean- and Proterozoic-aged kerogens, but the

Whereas intact aryl isoprenoids of chlorobiaceae (e.g. isore- causes are unclear (Imbus et al., 1992; Brocks et al., 2003b; Marshall

nieratane) or chromatiaceae (okenane; Schaeffer et al., 1997) et al., 2007). One common interpretation invokes evaporative frac-

were absent from the black shales studied, potential break-down tionation in gaseous solutions which selectively enriches light

products of isorenieratane, namely 2,3,6-trimethylated aryl iso- aromatics in the residual oil, thus shifting it to higher aromatic-

prenoids were found in all samples (Fig. 9). These compounds ity (Thompson, 1987). This process, however, appears to primarily

have often been observed in black shales and oils with abun- affect oils in reservoirs, rather than source rocks. Another pos-

dant isorenieratene. However, respective aryl isoprenoids do sible explanation for the high aromaticity in the black shales of

not necessarily derive from isorenieratene precursors. It has the Touirist Formation is a speciﬁc input of acritarch biopoly-

been shown that severe degradation of other non-aromatic mers, although the number of acritarchs is low. Acritarchs did

carotenoids of common phototrophs (e.g., ␤- and ␥-carotene) not strongly diversify until the Neoproterozoic, they were present

might also induce the formation of trimethylated aryl iso- and occasionally abundant through the Mesoproterozoic (Javaux

prenoids, including 2,3,6-trimethyl homologues (Hartgers et al., et al., 2004; Huntley et al., 2006) and were recently observed in

1994; Koopmans et al., 1996a,b). Isorenieratene and its degra- rocks of an age of 3.2 Ga (Javaux et al., 2010). However, stud-

dation products can be identiﬁed by relative C-enrichments ies using combined micro-Fourier transform infrared spectroscopy

(e.g. Summons and Powell, 1987). However, due to co-elution (FTIR) and laser micro Raman spectroscopy indicated that partic-

with other aromatic low molecular weight components, ␦ C- ularly Mesoproterozoic acritarchs contain biopolymers composed

analyses were impossible for the aryl isoprenoids from the Touirist of highly condensed aromatic sub-structures (Arouri et al., 2000;

Formation. The predominance of 2,3,6-trimethylbenzenes with Marshall et al., 2005) which may have contributed to the high

different alkyl chains (C14–C18) and the ﬁnding of a C21 2,3,6- aromaticity of the Touirist Formation black shales studied. And

trimethylated isoprenoid with two benzene rings (e.g., Koopmans indeed, laser micro-Raman spectroscopy of palynomorphs col-

et al., 1996a; Grice et al., 1997; Sinninghe Damste et al., 2001), lected from the Touirist Formation black shales revealed also

however, may be interpreted to reﬂect minor contributions from highest abundances of stretching bands (data not shown) typi-

−1

anoxygenic phototrophs. If sourced by anoxygenic phototrophs, we cal for highly aromatic kerogen (at 1600 cm ) (Marshall et al.,

propose the respective organisms played an active role within strat- 2005). Against this background, it is interesting to see that

␣

iﬁed microbial mats, similarly to recent microbial mats which often 4 ,23,24-trimethylcholestane (dinosterane) was not found in these

include anoxygenic phototrophic bacteria in the photic, anoxic, and samples. Dinosterane is commonly attributed to dinoﬂagellates

sulﬁdic layer below the immediate surface of the mats (Brocks (Summons et al., 1987), but it has been reported to be abundant

and Pearson, 2005; Ohkouchi et al., 2005). Consequently, in con- in early Cambrian rocks (Moldowan and Talyzina, 1998) that pre-

junction with the general phototrophic character of the mats this date by far their advent and rapid spread during the Mesozoic.

would require a very shallow environment (0–30 m), which is also These ﬁndings suggest that speciﬁc acritarchs may be ancestors

indicated by microfacies results (Fig. 3). of modern dinoﬂagellates. Our results suggest that the simple

The saturated and aromatic hydrocarbons from the black shales acritarchs preserved in the black shales of the Touirist Forma-

␦13 from the Touirist Formation revealed C-values between about tion were either not related to dinoﬂagellates (including a non

−29 and −35‰ (VPDB). Similar ␦ C-values were also observed eukaryotic origin of the palynomorphs; e.g., cysts of prokary-

in the kerogen of the black shales (Doering et al., 2009) as well otes), were unable to produce (dino)sterane, or were too low in

as for other Proterozoic hydrocarbons, which most likely derived abundance to be reﬂected in the biomarker record. Although quan-

from benthic microbial mats (Logan et al., 1999). Pristane, phy- titative estimates from ﬁndings of microfossils and of biomarker

tane and hopanes were in the same range or slightly enriched in abundances in extractable organic matter and kerogen are deli-

C, in line with reports from the relationship between acyl- and cate, the latter possibility would require additional explanation

isoprenoidal lipids from cyanobacteria and other bacteria (Sakata for the extraordinary high aromaticity of the Touirist Forma-

et al., 1997; Hayes, 2001). Table 5 demonstrates an increase in tion black shales than acritarch biopolymers. Polycyclic aromatic

␦13

C-values from the stratigraphically lowest to the highest black hydrocarbons may be also sourced by proteins and polysaccha-

shale sample, which also exhibits the highest amounts of hopanes. rides (Almendros et al., 1997; Marynowski et al., 2001), which

However, the isotopic differences between the samples are small, are abundant in nature, and particularly abundant in exopoly-

and possible reasons for this variation are difﬁcult to interpret. meric substances of benthic microbial mats (Wieland et al., 2008).

Staal et al. (2007) reported a positive relationship between bulk In addition, if the organic matter has been mainly produced

␦13

C and the thickness of microbial mats grown in freshwater, by microbial mats, those labile biopolymers were compared to

while an opposite trend was observed for marine mats (explained aliphatic lipids less affected by biodegradation, than organic mat-

by different degrees of carbon limitation and importance of het- ter which had to be transported through a water column. Thus,

erotrophic turnover; Staal et al. (2007)). Given that the benthic cyclized biopolymers may provide an additional source for aro-

microbial mats of the Taoudeni Basin grew in a dominantly marine matic hydrocarbons in the Touirist Formation and perhaps also

␦13

environment, the observed increase in C-values might be bet- for other Proterozoic kerogens originating from benthic microbial

ter explained by relatively higher microbial primary productivity, mats.

M. Blumenberg et al. / Precambrian Research 196–197 (2012) 113–127 125

4.4. On the predominance of (hopanoid-producing) prokaryotes suboxic environment. Unusually high amounts of aromatic hydro-

vs. eukaryotic algae in the Mesoproterozoic Taoudeni Basin carbons likely reﬂect a selective preservation of labile biopolymers

like exopolymeric substances rich in polysaccharides or proteins

In contrast to earlier ﬁndings (Summons et al., 1988a; Brocks in the microbial mats. Aerobic methanotrophy is indicated by

et al., 1999; Waldbauer et al., 2009), several biomarker studies sug- relatively high ratios of 3␤-methylhopanes. Varying but gener-

gest that eukaryotic algae were less important than prokaryotic ally high amounts of hopanes may be interpreted in terms of a

organisms in Archaean and Proterozoic seas (e.g. Dutkiewicz et al., nitrogen-limited setting that favored bacteria able to ﬁx atmo-

2004; Brocks et al., 2005, 2008). This observation is consistent with spheric nitrogen (diazotrophic (cyano)bacteria). Such a scenario is

other geological records (Knoll et al., 2006), and is further supported consistent with models of Proterozoic oceans containing low con-

by new data from the Taoudeni Basin, which shows the prevalence centrations of bioavailable nitrogen (nitrate, ammonia) due to loss

of bacterial hopanes and the virtual absence of (eukaryote-derived) by denitriﬁcation. The practical lack of steranes further demon-

steranes. strates that the palaeoenvironment of the Taoudeni Basin was

Although it has to be considered that steranes and hopanes unfavorable for eukaryotic algae other than acritarchs, supporting

behave differently during biodegradation and maturation, with recent hypotheses on generally bacterially dominated Proterozoic

hopanes showing a greater resistance to degradation than ster- Oceans.

anes (Seifert and Michael Moldowan, 1978; Peters and Moldowan,

1993), this holds only true at Peters–Moldowan level (PM) mat-

uration and degradation levels >7; (Peters and Moldowan, 1993). Acknowledgements

This is far beyond the most degraded sample from the Taoudeni

≤

Basin (PM level 2 for MCS 1). Thus, the ratio between hopanes We thank Sascha Döring, Patrick-Oliver Reynolds, Andreas

and steranes (including aromatic steranes) in immature and mod- Frischbutter and Geoff Gilleaudeau (University of Knoxville, Ten-

erately biodegraded Precambrian samples may be applied as a nessee) for helpful discussions. We are also indebted to Cornelia

relevant indicator on the distribution of ancient organisms. Given Conradt, Andreas Reimer and Birgit Röring for analytical support, to

that selective loss of steranes was only weak, high amounts of Nadine Schäfer for help with Laser Micro-Raman Spectroscopy, and

hopanes and the observed lack of sterane peaks hint to bacteria to Jens Dyckmans from the “Centre for Stable Isotope Research and

as the predominating component of the microbial communities Analysis” at the University of Göttingen for help with bulk and com-

in the Taoudeni Basin as well as to an increasing contribution of pound speciﬁc stable carbon isotope analysis. Jochen Brocks and

hopanoid-producing bacteria to the organic matter with decreasing an anonymous reviewer are thanked for their helpful comments

core depth. considerably improving the manuscript. This work was ﬁnan-

Whereas the function of hopanoids in bacteria is still under dis- cially supported by the Deutsche Forschungsgemeinschaft (grant

cussion (Berry et al., 1993; Moreau et al., 1997; Doughty et al., BL971/1-2 and 1-3) and the Courant Research Center of the Uni-

2009; Welander et al., 2009), a recent survey demonstrated a high versity Göttingen. This is publication 83 of the Courant Research

overlap of bacteria producing hopanoids and those being capa- Center Geobiology.

ble of nitrogen-ﬁxation (Pearson et al., 2007). Although the direct

role of hopanoids in the nitrogen-ﬁxation process is questionable

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