Late Archean rise of aerobic microbial ecosystems Jennifer L. Eigenbrode*†‡ and Katherine H. Freeman* *Department of Geosciences and Penn State Astrobiology Research Center, Pennsylvania State University, University Park, PA 16802; and †Geophysical Laboratory, Carnegie Institution of Washington, Washington, DC 20015 Communicated by John M. Hayes, Woods Hole Oceanographic Institution, Woods Hole, MA, August 30, 2006 (received for review January 18, 2006) We report the 13C content of preserved organic carbon for a 150 zone. Thus, we focus this work on relative water-column depth, million-year section of late Archean shallow and deepwater sedi- and we present kerogen ␦13C data for a well preserved, 150 ments of the Hamersley Province in Western Australia. We find a million-year stratigraphic section from the late Archean, in 13C enrichment of Ϸ10‰ in organic carbon of post-2.7-billion-year- which we distinguish isotopic signatures of shallow versus deep- old shallow-water carbonate rocks relative to deepwater sedi- water sedimentary environments. We specifically evaluate this ments. The shallow-water organic-carbon 13C content has a 29‰ isotopic record after the pronounced depletion in organic 13C range in values (؊57 to ؊28‰), and it contrasts with the less signatures at 2.72 Ga, and we compare it with published isotopic variable but strongly 13C-depleted (؊40 to ؊45‰) organic carbon records from other regions to assess global changes in microbial in deepwater sediments. The 13C enrichment likely represents ecosystems during this important time. microbial habitats not as strongly influenced by assimilation of methane or other 13C-depleted substrates. We propose that con- Results tinued oxidation of shallow settings favored the expansion of Kerogen ␦13C values for 175 samples from a 2.72- to 2.57-Ga aerobic ecosystems and respiring organisms, and, as a result, section in the Hamersley Province, Western Australia, vary isotopic signatures of preserved organic carbon in shallow settings between Ϫ57‰ and Ϫ28‰ (Fig. 2 A–D), spanning the pub- approached that of photosynthetic biomass. Facies analysis of lished range for late Archean organic carbon. Large variations published carbon-isotopic records indicates that the Hamersley (5–16‰) occurred at 1- to 10-m scales, and they are correlated shallow-water signal may be representative of a late Archean with lithology (Fig. 2 A–D). For example, in the WRL1 core, global signature and that it preceded a similar, but delayed, 13C increases and decreases in dolomitic siltstone relative to shale are enrichment of deepwater deposits. The data suggest that a global- accompanied by enrichment and depletion of ␦13C in kerogens, scale expansion of oxygenated habitats accompanied the progres- respectively. Similar ␦13C–lithologic relationships have been sion away from anaerobic ecosystems toward respiring microbial observed for the 2.52- to 2.46-Ga Transvaal rocks on the communities fueled by oxygenic photosynthesis before the oxy- Kaapvaal Craton (9, 10), although they have a narrower range in genation of the atmosphere after 2.45 billion years ago. carbon isotopic compositions for bulk organic matter (␦org) range. organic carbon ͉ isotopes ͉ methanotrophy ͉ oxygen Facies were defined by sedimentological characteristics, and they were grouped into shallow-water deposits and deeper slope GEOLOGY esolving changes in early ecosystems and their geochemical and distal basin deposits. Briefly, the upper Carawine Dolomite Rcontext is critical to understanding both the means and pace with abundant stromatolites is well recognized as a shelf deposit of events that culminated in atmospheric oxygenation beginning having platform architecture (11). The Tumbiana very shallow possibly as early as 2.45 gigaannum (Ga) before the present, carbonate environment flanked a large, southerly subsiding rift based on the sulfur isotopic record (1) but certainly by 2.3 Ga, basin (12), and it received a high flux of terrestrial detritus. The based on other geochemical observations (2). Oxygenic photo- Tumbiana Formation has been interpreted as a fluvial– synthesis must have evolved before this event, but conjectures for lacustrine deposit (13) (but others suggest that it may also its onset range from pre-3.5 Ga (3, 4) to 2.7 Ga (5, 6) to 2.4 Ga contain shallow marine deposits; see ref. 14 and Supporting (7). Whenever it occurred, its inevitable impact on ecosystems Discussion, which is published as supporting information on the must have been profound. PNAS web site). The Warrie Member overlies a transgressive The 13C content of sedimentary organic matter represents shoreline deposit in northern exposures, and it contains sedi- mixed contributions from many biological materials. Isotopic mentary structures consistent with a shallow marine shelf envi- signatures within modern and Phanerozoic marine sediments ronment (see Supporting Discussion). Carbonates of the Witte- generally fall in a narrow range, and they reflect those of noom Dolomite and lower Carawine Dolomite largely consist of phytoplankton (8) because heterotrophic respiration imparts platform (shelf) detritus within turbidite deposits (11). Finely small, if any, isotopic shifts in the preserved organic matter. In laminated, dolomite-rich black shales (10–60 wt % dolomite), contrast, late Archean organic carbon displays a wide range in interbedded with platform carbonate deposits in the Carawine 13 ␦13 ϭ 3 13 ͞13 C content (expressed as C, ‰ 10 ( Rsample Rstandard Dolomite, reflect lagoonal or other localized, restricted- Ϫ1), and 13R ϭ 13C͞12C; Fig. 1), with values generally below Ϫ35 circulation settings on the platform. Other finely laminated black to Ϫ40‰ in shales (9, 10) and even lower in some shallow-water shales and dolomitic and tuffaceous siltstones characterize deep- deposits at Ϸ2.7 Ga (Fig. 1). As hypothesized by Hayes (5, 6), strong 13C depletion in organic matter, either in bulk or as the insoluble fraction (kerogen; ␦ker), indicates that late Archean Author contributions: J.L.E. and K.H.F. designed research; J.L.E. performed research; K.H.F. ecosystems incorporated 13C-depleted substrates, particularly contributed new reagents͞analytic tools; J.L.E. analyzed data; and J.L.E. and K.H.F. wrote methane. the paper. If kerogen ␦13C patterns in different sedimentary environ- The authors declare no conflict of interest. ␦ ␦ ments reflect differences in the dominant pathways for carbon Abbreviations: carb, carbon isotopic composition of inorganic carbon of carbonates; ker, ␦ assimilation and cycling, then the isotopic record may also reflect carbon isotopic composition of kerogen; org, carbon isotopic composition of bulk organic matter; Ga, gigaannum before present; Rubisco, ribulose-bisphosphate carboxylase͞ secular changes in microbial communities within different en- oxygenase. vironmental settings. Unlike carbonate isotopic records, which ‡To whom correspondence should be addressed at: Geophysical Laboratory, Carnegie are highly sensitive to marine versus lacustrine distinctions, Institution of Washington, 5251 Broad Branch Road NW, Washington, DC 20015. E-mail: organic-carbon isotopic signatures record the influence of bio- [email protected]. logical productivity and recycling within and below the photic © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0607540103 PNAS ͉ October 24, 2006 ͉ vol. 103 ͉ no. 43 ͉ 15759–15764 Downloaded by guest on September 30, 2021 13 Fig. 1. Compilation of published kerogen and total organic carbon ␦ C values (␦org) for all sedimentary rock types. Data from this work are included, and the geochronology is updated (see also Supporting References, which are published as supporting information on the PNAS web site). The top curve is the mean inorganic carbon ␦13C composition for marine carbonate rocks published by Shields and Veizer (16). Values are not corrected for postdepositional alteration. water slope deposits, whereas massive, pyritic black shales were Discussion deposited in basin settings more distal to the shelf. Observational data and computational models suggest that the The isotopic record shown in Fig. 2 A–D reveals both facies- Archean atmosphere was composed of N2,CO2,CH4, and H2 and time-related signals. Over the entire period, the shallow (17, 18), consistent with the suggestion that the carbon cycle was ␦ facies show a wide range of ker values, with dolomitic shales of dominated by autotrophy, fermentation, acetogenesis, and 13 the restricted platform facies 2–14‰ depleted in C relative to methanogenesis (19, 20). Moderately high CO2 levels (up to 10ϫ the platform carbonates immediately above and below. Kerogens the present atmospheric level) (18, 20, 21) provided ample 13 ␦ in deepwater shales are strongly depleted in C, whereas ker substrate for autotrophs, such that isotope fractionation likely values for the slope facies are intermediate to those for basin and approached maximum values. Assuming an 8‰ difference shallow-water carbonate shelf facies (Fig. 2E). Sedimentology between carbonate and dissolved CO2, carbon fixation by suggests that the slope facies may have received organic matter ribulose-bisphosphate carboxylase͞oxygenase (Rubisco) and the transported and deposited from shallower environments, which Calvin–Benson cycle could account for ␦ker values as low as was mixed with autochthonous inputs. Ϫ37‰, as in most modern eukaryotes (form IB; maximum ␦ To assess temporal changes in ker, we merged the records in Fig. fractionation, Ϸ29‰; refs. 22