Sulfur and carbon isotopic evidence for metabolic pathway evolution and a four-stepped Earth system progression across the Archean and Paleoproterozoic
Introduction
Microbial life gains energy and converts inorganic carbon into organic molecules through the use of sunlight (phototrophy) or chemical reactions (chemotrophy) that take advantage of redox reactions. Sulfur exhibits a wide range of oxidation states (from + 6 to − 2), and is released from the mantle via volcanism predominantly as SO2 (+ 4) and H2S (− 2). Sulfur released via subaerial volcanism is predominantly in the form of SO2, while sulfur released in the subsurface can react with volcanic gases containing H2 to form H2S (Table 1). As such, the potential simultaneous delivery of sulfur in two different redox states from the mantle has provided a ready sulfur redox gradient across all of earth history. In addition, life has evolved multiple metabolic pathways to exploit a wide range of sulfur compounds for generating energy (e.g., McCollom and Shock, 1997, Shock et al., 2005, Sleep and Bird, 2007). These metabolic pathways likely played an important role in the progressive oxidation of the earth's surface, and in resulting geochemical and geologic signals of this progression in the rock record (Kasting, 2013). Sulfur-coupled metabolisms are some of the most important microbially mediated processes, and are either directly or indirectly linked with carbon-coupled metabolisms, with both modifying redox conditions on Earth's surface. The rock record, while incomplete, provides our best framework for understanding the redox history of the Earth's surface (e.g, Farquhar et al., 2001, Hannisdal and Peters, 2011, Halevy, 2013), with isotopes of sulfur (including the mass independent fractionation of sulfur, or MIF-S signal) and carbon isotopes providing convincing evidence for the timing of the transition from an oxygen depleted/reducing atmosphere to one with free oxygen.
The isotopic values of carbon and sulfur recovered over the time period exhibit wide ranges. Sulfide mineral δ34S values span a minimum of − 45.5‰ (at ~ 2.40 Ga) to a maximum of 54.9‰ (at ~ 2.09 Ga), while sulfate mineral δ34S values span a minimum of − 13.6‰ (at ~ 2.43 Ga) to a maximum of 46.6‰ (at ~ 2.05 Ga). These values, however, are muted compared to extreme δ34S values found in more recent units such as sulfide minerals ranging from − 72‰ in sediments overlying mid ocean ridge basalts (Lever et al., 2013) to 114.8‰ in pyrites enriched by microorganisms that couple sulfate reduction to anaerobic oxidation of methane (Lin et al., 2016); or sulfate δ34S values of 135‰ in interstitial pore waters from ocean drilling cores as a result of slow sulfate reduction rates in low sulfate concentration environments (Rudnicki et al., 2001). Organic carbon δ13C values ranged from a minimum of − 60.9‰ (at ~ 2.75 Ga) to a maximum of − 4.6‰ (at ~ 2.07 Ga), while carbonate δ13C values ranged from a minimum of − 18.5‰ (at ~ 1.60 Ga) to a maximum of 29.6‰ (at ~ 2.10 Ga). As with sulfur, these rock values are muted compared to extremes measured in more recent samples. Methanotrophic biomass has been measured at δ13C values as low as − 85‰, while natural cyanobacterial biomass has been measured at values as high as − 3‰, and methanogenic biomass as high as 6‰ (Schidlowski, 2001). Carbonate δ13C values have been documented at values as low as − 125‰ from deposition from carbon-poor groundwater related to sulfate-dependent anaerobic methane oxidation (Drake et al., 2015) and as high as 34‰ in cements associated with dissolved inorganic carbon influenced by methanogenesis (Budai et al., 2002). Given these wide ranges that have been found to date associated with the complex systematics of sulfur and carbon isotope fractionations and distillations, it is imperative that we interpret rock record values carefully and consider the ranges of values that we can associate directly to known metabolic pathways (e.g., carbon fixation pathways, biological sulfate reduction, microbially mediated disproportionation, etc.) measured from pure culture experimental work.
By merging comprehensive geochemical datasets from the literature with our current understanding of microbial sulfur and carbon transformations, we can better constrain the onset of the biological innovations. To do so, we draw on three lines of evidence: i) sulfur and carbon major stable isotope data, ii) geochemical contextual evidence for progressive though not necessarily linear (e.g., Kump, 2008, Lyons et al., 2014, Gumsley et al., 2017) oxidation of the earth's surface, including the sulfur isotope mass-independent fractionation (MIF-S) signal recorded in the rock record, and iii) the microbial metabolic machinery recorded in the genomic record of extant life and the isotopic signals they generate.
First we present sulfur and carbon stable isotope data, summarizing background information on each isotope system as it relates to global surface redox and describing trends observed from data compiled from the literature. Next we discuss the connection between microbial metabolism and sulfur compounds, followed by a section that lays out the relationship between carbon fixation metabolisms and the carbon isotope system, and then a brief treatment of molecular clock calculations. Other select information from the rock record that relate to the oxidation of the Earth's surface and the Great Oxidation Event (GOE) are briefly described in the Rock Record Contextual Information section. Finally, we provide a synthesis of all the geochemical, biological, and geologic information in four time periods: Period 1: 4.0 to 2.8 Ga-the beginnings of modern Earth system dynamics, with relatively small differences between δ34S values of sulfide and sulfate minerals (Fig. 1A, B), organic carbon δ13C values that range between − 13.1 and − 44.3‰ (Fig. 1C), carbonate δ13C values near 0‰ (Fig. 1D), and Δ33S and Δ36S values of sulfides and sulfates contain mass independent fractionation signals (Fig. 2A, B); Period 2: 2.8 to 2.45 Ga-the buildup to the GOE), where we observe an expansion in the range of sulfide and sulfate mineral δ34S values (Fig. 1A, B) as well as Δ33S and Δ36S values (Fig. 2A, B), an increase in occurrence of more negative δ13C values in both organic carbon (minimum of − 60.9‰) and carbonate minerals (minimum of − 15.0‰) (Fig. 1C, D); Period 3: 2.45 to 2.0 Ga-The GOE, characterized by a further expansion in the range in δ34S values in both sulfide and sulfate minerals (Fig. 1A, B), a collapse in the Δ33S and Δ36S values in both sulfide and sulfate minerals (Fig. 2A, B), and a shift towards positive δ13C values in both organic carbon and carbonate minerals (Fig. 1C, D); and Period 4: after 2.0 Ga-Earth system quiescence, when sulfide mineral δ34S values trend to the positive (Fig. 1A), and the ranges of organic carbon and carbonate mineral δ13C values decrease dramatically (Fig. 1C, D).
Section snippets
Sulfur and carbon stable isotope data
Carbon is present as two stable isotopes, 12C and 13C, with 12C accounting for 98.93%, and 13C for 1.07%. Sulfur is present as four stable isotopes, including 32S (94.93%), 33S (0.76%), 34S (4.29%), and 36S (0.02%). All isotopic data are reported as isotope ratios, relative to standards of known value, using the equation [(isotope ratio of sample) / (isotope ratio of standard) − 1] × 1000, expressed in delta notation (δ) and reported as per mil (‰). For sulfur, the standard is the Vienna Canyon
Biology of S metabolisms
The wide range of oxidation states of sulfur (− 2 to + 6) provide many intermediates for biological oxidation, reduction, and disproportionation. The dissimilation of sulfur compounds may have been one of the earliest biological strategies for energy generation (e.g., Canfield and Raiswell, 1999, Canfield et al., 2006, Grein et al., 2013). Although sulfate concentrations were probably much lower during the Archaean (e.g., Habicht et al., 2002, Crowe et al., 2014, Jamieson et al., 2013), reduced
Biology of C metabolisms
Key early evolving carbon metabolisms include carbon fixation (conversion of inorganic C into organic C), methanogenesis (metabolisms that result in the production of CH4), and fermentation (anaerobic breakdown of organic material). Carbon fixation allowed the conversion of oxidized carbon (as CO2) into reduced carbon, and the burial of reduced organic carbon is one of the fundamental forces that helped drive the oxidation of the Earth's surface. Methanogenesis would have provided a
Electron transfer and geologic processes
A simplified conceptual cartoon to illustrate the movement of electrons (e−) through the surface system of earth and means for transporting reducing power between the mantle and surface is presented (Fig. 4). For the carbon system, volcanism releases CO2 into the atmosphere, which can be reduced to organic carbon (represented by CH2O) through either oxygenic photosynthesis (utilizing photons to break the HO bonds in water, and producing O2) or anoxygenic photosynthesis (represented by the
Rock record and theoretical contextual information
Multiple lines of direct and indirect contextual information relating to the redox evolution of the Earth's surface are available from the literature to elucidate the setting for and effects of the evolving earth and developing biosphere on the sulfur and carbon isotope systems. These include geologic and geochemical analyses and interpretation of the rock record, including mantle cooling; crustal thickness, cycling, and formation; and redox-related evidence. This section briefly describes and
Interpretation of sulfur isotope data
Using a mass balance modeling approach, we can interpret some of the trends observed in the δ34S values in the rock record. The first order trends that we observe in the data in periods 2, 3, and 4 (2.8 Ga to 1.5 Ga) are: an increase in the δ34S of sulfate minerals from approximately + 10‰ to + 40‰, a roughly parallel increase in the upper envelope of δ34S values of sulfide minerals, and a decline of the lower envelope of δ34S values of sulfide minerals from about 0‰ to − 40‰ followed by an increase
Interpretation of carbon isotope data
The carbon isotope signal preserved in the rock record is the product of many processes. One process that is directly linked to and driven by the action of life is the isotopic value of carbonates and organic carbon. Mantle-derived carbon has a δ13C value of − 8 to − 5‰ (Exley et al., 1986, Javoy et al., 1986, Deines, 2002, Horita and Polyakov, 2015), and is released to the surface as CO2 via volcanism. Through the study of the better-preserved Phanerozoic rock record and modern carbon cycling
Synthesis: interpreting carbon and sulfur isotopes through the Archean and Paleoproterozoic
The isotopic records of carbon and sulfur as well as the evolutionary history of biologically mediated carbon and sulfur cycling discussed above aid in interpreting signals imparted in the rock record by biogeochemical cycles over time represented by the rock record. Below we discuss these data in the framework of the periods defined before. The following synthesis represents the culmination of our interpretations of the patterns we have observed in the compiled data. We acknowledge there are
Concluding thoughts
The geochemical upheaval in sulfur and carbon isotopes that characterizes the first half of the Paleoproterozoic lies in stark contrast to the quiescence that typifies the second half. Furthermore, geologic and geochemical evidence for dramatic changes in the oxidation state of the surface environment occur during the first half, with no major changes observed to date in the second half. From this, perhaps it is useful to recognize and signify these differences by dividing the Paleoproterozoic
Acknowledgements
JRH would like to thank the Penn State Astrobiology Research Center for generous support, the University of Cincinnati for support, and Dr. Chris House for support and encouragement. TLH graciously acknowledges support from the University of Cincinnati.
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Present address: Department of Geosciences, Stanford University, Stanford, CA.