Exceptional preservation of microbial lipids in Paleozoic to Mesoproterozoic sediments

“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 modifi cations, 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 fl uid 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 defi ciency 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 fi rst multicellular benthic grazing organisms during the Ediacaran, this selective preservation pathway was disrupted and the sedimentary infl ux of planktonic bioproduction increased, especially under anoxic/dysoxic conditions. A similar mode of preservation has been inferred by Hall et al. (2011) for the softbodied 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 specifi c 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 signifi cantly intensifi ed 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