“Biomarker geochemistry” describes a geoscience discipline investigating the molecular and isotopic composition of organic matter preserved in the sedimentary record. Its aim is to utilize structures, functions, and phylogenetic distributions of modern biomolecules in order to elucidate their role in fossil ecosystems. After embedding in sediments, biomolecules undergo well-known structural modifications, removing labile functional groups from their stable hydrocarbon skeletons. After the transition from the biosphere to the geosphere, such molecules can be traced back to their biological precursors (based on their characteristic carbon skeleton), and are called biomarkers or molecular fossils. In paleoenvironmental reconstructions, the study of biomarkers offers the advantage that these stable and non-reactive compounds can be preserved in the geological record for over a billion years, allowing us to establish who the key players have been in ancient microbial systems, and how these changed over time. There has been debate about the syngeneity of some of the oldest molecular fossils and the Proterozoic and Archaean sedimentary rocks in which they occur (Rasmussen et al., 2008; Waldbauer et al., 2009). This debate is based on the property of hydrocarbons to move within the sedimentary pore space, a process termed primary migration, and a critical prerequisite for the formation of oil and gas accumulations. Rigorous analytical protocols, however, have been established to verify the syngeneity of biomarkers and their containing sediments (Brocks, 2011), placing the oldest unequivocal occurrence of biomarkers in the 1.64 billion year old (Ga) Barney Creek Formation in the McArthur Basin, Australia. Biomarkers within fluid inclusions, where they are protected from contamination by migration (Dutkiewicz et al., 2006), still place the earliest occurrence of cyanophytes, and even eukaryotes, close to the Great Oxidation Event at 2.45–2.3 Ga, thus leaving considerable room for further research. Even with some reported oldest occurrences of biomarkers under discussion, a reliable record of molecular fossils is available for the study of fossil ecosystems and microbial ecology after 1.64 Ga. A re-analysis of biomarkers spanning the Mesoproterozoic through Ediacaran (ca. 1.6 -0.635 Ga) by Pawloswka et al. (2013, p. 103 in this issue of Geology), employing strict protocols to exclude contamination, reveals exceptional preservation due to the unique environments of pre-Ediacaran ecosystems. In Phanerozoic environments, excellent preservation of lipids results from a lack of benthic respiration due to oxygen deficiency in the sediment, commonly extending into the overlying water column. Under such conditions, reduced sulfur species, toxic for aerobic organisms, are produced by sulfur-reducing bacteria. The pre-Ediacaran ecosystems studied by Pawlowska et al. did not form under strictly anaerobic or even sulphidic conditions, but show evidence for a different mode of lipid preservation, initiated by the pervasive existence of microbial mats with a complex internal structure. Photoautotrophic cyanophytes preferably colonized the top of the mat, while heterotrophic bacteria consumed incoming organic material at its base. Therefore, lipids derived from planktonic organisms are under-represented in the sediment due to intensive respiration at the mat’s surface, whereas benthic microbial lipids are exceptionally enriched. Such features are in agreement with the unique carbon isotope distribution pattern observed in kerogen and bitumen in Proterozoic rocks. With the arrival of the first multicellular benthic grazing organisms during the Ediacaran, this selective preservation pathway was disrupted and the sedimentary influx of planktonic bioproduction increased, especially under anoxic/dysoxic conditions. A similar mode of preservation has been inferred by Hall et al. (2011) for the soft-bodied fossils in the Emu Bay Shale of southern Australia, an equivalent of the famous Burgess Shale Fauna at Mount Field in British Columbia, based on molecular geochemical studies. Pre-Ediacaran and unique later ecosystems will thus have to be investigated further to investigate implications of the “mat seal effect” (Pawlowska et al., 2013) in terms of restricted nutrient and oxygen cycling, constraints on benthic organism evolution, exchange of atmospheric trace gases, and substrate stabilization.
Reorganization of microbial community structures is not unique for the Neoproterozoic-Ediacaran transition, but occurred at multiple times in the sedimentary record. Intensive perturbations in macroevolution have been reported during global extinction events, some of which were associated with glaciation. It is reasonable to assume that these events were also linked to rearrangements in microbial ecology. The Late Ordovician mass extinction associated with the Hirnantian Glaciation (ca. 445 Ma) offers the possibility to test such a hypothesis. In an elegant study, Rohrssen et al. (2103, p. 127 in this issue of Geology) investigated three sections within Laurentia, none of which has evidence for localized methane sources (e.g., vents), covering the warm intervals before and after the Hirnantian cooling. None of the sections contained high amounts of sedimentary organic matter, but biomarker analysis is based on composition, not abundance. Exceptional preservation of trace amounts of biomarkers at all sites tracked a massive increase in bacterial (indicated by hopane biomarkers) versus algal (indicated by sterane biomarkers) marine plankton immediately before and after the glaciation. Bacterial productivity increased in the warm and shallow equatorial seas, where bacteria outcompete algae under nitrate limiting conditions (as prevailing in oxygen minimum zones), due to their ability to utilize ammonium and dinitrogen as substrate. Besides an increase in bacterial biomass in the Hirnantian oceans, a shift in bacterial community structure to species capable of utilizing methane as an energy substrate was recorded by a mass abundance of specific 3β-methylhopanes. Methane-oxidizing bacteria occurred at concentrations 10–20× above Phanerozoic average at all sites studied, despite substantial differences in paleoceanographic setting. This implies a significantly intensified global methane cycle with the potential of atmospheric methane release, with consequences for global warming. Positive paleotemperature excursions based on clumped carbon isotope paleothermometry corroborate the inferred climate effects before and after the Hirnantian glaciation. The glacial cooling event sees a massive decline in the shallow-water–high-temperature associated bacterial communities, and a replacement by eukaryotic algae, in particular chlorophytes adapted to cold-water environments, as evidenced in the sterane composition. The study by Rohrssen et al. (2013) thus provides a further example of how exceptional preservation of even trace amounts of biomarkers provides insight into processes affecting microbial ecology and associated geochemical cycling of essential elements and trace gases important in regulating global climate.
Exceptional preservation in the sediment, of organic matter produced in the photic zone in aquatic environments, occurs if the pore waters and the lower water column are not only oxygen-deficient but highly sulfidic. If such euxinic environments extend into the photic zone, as presently in the Black Sea, specific Chlorobi bacteria performing anoxygenic photosynthesis will thrive. Many sedimentary environments with photic zone euxinia (PZE) and excellent preservation of organic matter have been described, ranging from the present until the Mesoproterozoic (1.0–1.6 Ga; e.g., Summons and Powell, 1986; Schwark and Puettmann, 1990; Schaeffer et al., 1997; Brocks et al., 2005). The investigation by Melendez et al. (2013, p. 123 in this issue of Geology) goes a step further by identifying biomass from an invertebrate fossil encapsulated in a carbonate concretion of Devonian age from the Gogo Formation, in the Canning Basin of Western Australia, deposited under PZE conditions, whereby persistent PZE was identified based on aryl isoprenoid distributions in the fossil’s free bitumen and desulfurized polar fractions. Chlorobi, when conducting anoxygenic photosynthesis, not only employ a specific bacterio-chlorophyll but also utilize highly specific accessory pigments, in particular of the diaromatic carotenoid type (renieratene, isorenieratene, etc.). Whereas regular accessory pigments like β-carotene, due to their parallel function as photo-oxidants, are rarely preserved in sedimentary archives, the diaromatic carotenoids (after hydrogenation of the unsaturated isoprenoid chain) are stabilized to form biomarkers not only of the highest chemotaxonomic value but also with unique resolving power concerning reconstruction of redox conditions. Sediments of the Gogo Formation have been deposited under conditions favoring organic matter preservation, as seen by their high abundance of the PZE biomarkers renieratane, isorenieratane, and paleorenieratane. The carbonate concretions analyzed from the Gogo Formation revealed exceptionally high concentrations of C27 steranes, with thermally very immature isomerization patterns, associated with the invertebrate fossil. The extremely low thermal maturity and highly reducing conditions were corroborated by a massive dominance of the isoprenoid phytane over pristane in the sulfur-bound fraction. This indicates direct reduction of phytol to phytenes, and their subsequent “natural vulcanization” with reduced sulfur species (e.g., Hebting et al., 2006). The steranes detected in the concretions thus preserve a distribution pattern that is almost unaffected by diagenesis, and hence the predominance of the C27 isomers indicates an origin from the invertebrate fossil and not from marine algae. Common marine algae during the Devonian show a dominance of C29-steranes, with only samples rich in rhodophytes, not present in the Gogo Formation, being enriched in C27 (Schwark and Empt, 2006). All biomarkers, those from primary aquatic producers, from heterotrophs destroying primary organic matter, and from the invertebrate fossil, increased to the center of the concretion due to better preservation. However, the 10× increase in the C27 sterane has to originate from the diagenetic conversion of sterols derived from the invertebrate fossil biomass. The only likely producers of cholesterol in that environment were crustaceans or mollusks, and due to the lack of paleontological evidence for a mollusk, the enigmatic fossil could be chemo-taxonomically placed with crustaceans. This provides the currently oldest known evidence for the preservation of eumetazoan biomass in the sedimentary record.
The ever-increasing performance of analytical instrumentation, the application of sampling protocols designated to minimize or avoid potential contamination, and the coupling of structural information on biomarkers with their compound-specific C, H, N, or S-isotope signature opens avenues for investigating fossil microbial ecosystems (with increasing potential for macro-organisms) and past environmental conditions at unprecedented accuracy. Given a high level of preservation, samples with only trace amounts of organic matter that previously were discarded from further investigation can yield information highly complementary to established techniques when addressing questions of biological, atmospheric, and climatic evolution.
