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Project Progress

Co-evolution of microbial metabolisms in the Neoarchean and Paleoproterozoic

The relative evolution of various microbial metabolisms has been classically constrained through phylogenetic reconstructions and estimates of the rate of evolution of molecules that are widely distributed and highly conserved – the “molecular clock” approach (e.g., Ochman and Wilson, 1987; Sheridan et al., 2003). Such approaches, however, have come under great scrutiny because of issues such as lateral gene transfer and uncertainties in estimating “rates” of molecular evolution. Another approach, one taken by the Wisconsin team, is tracing the distribution of metabolisms using the abundances and isotopic compositions and metabolically cycled elements in sedimentary rocks, such as C, S, and Fe.

The largest excursions in kerogen C isotope compositions and mass-independent S isotope fractionations in sulfides occur between ~2.7 and 2.4 Ga (e.g., Farquhar and Wing 2003; Eigenbrode and Freeman 2006), suggesting major changes in the C and S cycles. It is now known that these changes are broadly accompanied by the largest Fe isotope excursion measured in the rock record (Fig. 1), but, prior to our work, C, S, and Fe isotopes have not been measured on the same sample. By combining multiple isotopes on the same samples, we are able to address the controversial interpretations of the Neoarchean and Paleoproterozoic Fe isotope record: one group interprets the Fe isotope compositions to directly reflect those of ancient seawater, produced by abiologic processes involving extensive precipitation of iron oxides (Rouxel et al. 2005; Anbar and Rouxel 2007), whereas another group favors microbial iron cycling, including dissimilatory Fe(III) reduction, where the isotopic compositions are unrelated to those of ancient seawater (Yamaguchi et al. 2005; Johnson et al. 2008a; Johnson et al. 2008b).

Our first completed study for this project during Year 2 involved C, O, and Fe isotope studies of Fe-rich carbonates (siderite; FeCO₃) from 2.5 b.y.-old banded iron formations (BIF) from South Africa (SA); these are correlative with the famed Hamersley Basin BIFs of NW Australia, but the SA BIFs were subjected to lower grades of metamorphism. Studies of BIFs provide an important test of the proposal that the major Fe isotope excursion towards negative Fe isotope compositions (Fig. 1) in ~2.7 to 2.4 Ga age marine sedimentary rocks record a period when DIR was extensive, because isotopically fractionated Fe-rich rocks are difficult to produce by the abiological oxidation mechanism proposed by other workers. Periods of BIF deposition represent times when marine Fe fluxes were very high, including very high rates of Fe-rich sediment deposition, dramatically different than those of the modern marine iron cycle (Trendall 2002; Klein 2005) (Trendall et al. 2004). These results showed that none of the siderites in the BIFs had C, O, or Fe isotope compositions that would reflect precipitation from seawater, but instead are well modeled through production of FeCO₃ through microbial reduction of Fe(III) oxides coupled to organic carbon oxidation (see equations in Fig. 2). Importantly, Fe isotope mass balance was demonstrated within the sample suite, where negative δ⁵⁶Fe values are interpreted to reflect “light” aqueous Fe mobilized by DIR, and positive δ⁵⁶Fe values seem likely to reflect the residue that remained after extraction of light Fe (Heimann et al., 2009), followed by reduction by DIR. This study provides strong evidence that DIR was a major metabolism involved during BIF formation in the Neoarchean, and does not support the abiological fractionation model of Rouxel et al. (2005) and Anbar and Rouxel (2007).

Our second completed study involved C, S, and Fe isotope studies of organic-rich black shales of the 2.7 to 2.5 b.y. Hamersley Basin, which records a period of time that precedes major BIF deposition discussed above and exactly coincides with the well known very large negative δ¹³C excursion for organic carbon (kerogen) in marine sedimentary rocks. Importantly, we compared the results from two cores that represented samples of the deep, central part of the basin, as well as the shallower basin margin. The results (Czaja et al., 2009) demonstrate that the different parts of the basin produced distinct isotopic trends, reflecting contrasts in depositional environments. These trends are difficult to explain by abiological processes, and, collectively, reflect the coupled C-S-Fe cycles that are expected by microbial metabolisms as related to basin geometry and timing relative to the anticipated increasing influence of photosynthesis (Figs. 3 and 4). For example, the negative δ⁵⁶Fe values for Fe-rich shales of the Jeerinah Formation in the deep part of the basin are best explained by accumulation of low-δ⁵⁶Fe Fe(II)_aq that was produced by DIR on the basin margin; by mass-balance, moderately positive δ⁵⁶Fe values are expected for the shallow parts of the basin, which reflect the residue from loss of light Fe to the center of the basin (Fig. 3). These relations are seen in the different cores, and are opposite to those that would be produced by abiological oxidation processes.

When variations in δ¹³C and δ³⁴S are considered along with δ⁵⁶Fe values, the picture that emerges is one of remarkable microbial diversity (Fig. 4). Processes that occurred in the photic zone included anaerobic photosynthesis coupled to Fe(II) oxidation, as well as oxygenic photosynthesis. Carbon isotope data, as well as molecular biomarkers measured on the same samples, provide support for aerobic methanotrophy (AMT) in shallow parts of the basin, indicating the presence of free O₂. Microbial Fe reduction in the shallow shelf regions was coupled to oxidation of organic carbon (DIR) or anaerobic oxidation of methane (AOM-IR). Support for bacterial sulfate reduction (BSR) or anaerobic oxidation of methane coupled to sulfate reduction (AOM-SR) under conditions of limited sulfate contents comes from the generally positive δ³⁴S values measured in the samples, where AOM-SR is ascribed to sediments that have highly negative δ¹³C values. The S isotope support for some, but limited, free O₂ is consistent with conditions required to transport aqueous Fe within the basin. Overall, the large range in C, S, and Fe isotopes indicate large sections of the environments co-existed under reduced and oxidized conditions, with mass transfer occurring between these environments. We propose that such conditions were ideal for supporting a strong radiation of microbial metabolisms during this time on the early Earth.