 2006 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or editing@geosociety.org. Geology; January 2006; v. 34; no. 1; p. 37–40; doi: 10.1130/G22012.1; 3 figures. 37 Hydrogen-based carbon fixation in the earliest known photosynthetic organisms Michael M. Tice Donald R. Lowe    Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, USA ABSTRACT Thin carbonaceous laminations preserved in shallow-water facies of the 3416 Ma Buck Reef Chert, South Africa, have been interpreted to represent some of the oldest-known mats constructed by photosynthetic microbes. Preservation of these mats within a unit containing facies deposited at water depths ranging from 0 m to 200 m provides an opportunity to explore the electron donors employed in early microbial photosynthesis. The presence of siderite (FeCO 3 ) as a primary sediment, lack of hematite (Fe 2 O 3 ), and lack of cerium anomalies throughout the Buck Reef Chert imply that the entire water column was anoxic despite the presence of photosynthetic organisms. Authigenic uranium (Ua  U–Th/3) correlates inversely with siderite abundance, suggesting that variations in carbonate rather than oxygen activity controlled uranium mobility. The inferred lack of oxygen and ferric minerals and the presence of dissolved Fe 2 in the water column imply that H 2 O, Fe 2 , and H 2 S could not have served as primary electron donors for carbon fixation. It is most likely that Buck Reef Chert bacteria utilized H 2 as the primary reduc- tant for photosynthesis. Keywords: photosynthesis, Archean, hydrogen, evolution. Figure 1. Measured section through Buck Reef Chert (Tice and Lowe, 2004) with rep- resentative whole-rock rare earth element (REE) abundances (normalized to post- archean average shale) and authigenic ura- nium ( estimated error). La (leftmost) point is aligned with sample height. REE scale il- lustrates relative abundances within individ- ual distributions. Base of section is sand- stone representing coastal system. Lowest 15 m of section is evaporite facies; 15–180 m of section is mostly shallow to deep shelf facies; 180–235 m of section is basin facies. Elemental abundances determined by in- ductively coupled plasma–mass spectrom- etry at Washington State University Geoan- alytical Laboratory (Pullman, Washington). INTRODUCTION While recent phylogenetic studies indicate that anoxygenic photosynthesis evolved be- fore oxygenic photosynthesis (Raymond et al., 2002; Xiong et al., 2000), most interpretations of the earliest geologic record of life infer an extremely ancient origin for oxygenic cyano- bacteria (Rosing and Frei, 2004; Schopf and Packer, 1987), perhaps as old as 3.7 Ga. Such an ancient origin, perhaps within 100 m.y. of the last Earth-sterilizing impact (Sleep et al., 1989), would require a surprisingly brief period of evolution from the first primitive metabolism to the complex molecular machin- ery required for oxygenic photosynthesis (Blankenship, 2002). It is possible that this paradox is artificial, simply reflecting a basic lack of appreciation for the potential pace of evolution. However, if geological interpreta- tions of early oxygenic photosynthesis are cor- rect, they would have an important practical consequence for studies of early evolution: geological investigation of intermediate or- ganisms and ecosystems in the evolution of photosynthesis would be practically impossible. Tice and Lowe (2004) reported that the Buck Reef Chert in the Barberton greenstone belt, South Africa, preserves a record of chemical and biological sedimentation atop a subsiding open-marine volcanic platform. Buck Reef Chert sediments were deposited on a subsiding volcanic platform in environments that evolved from evaporitic coastal lagoons through a wave- and storm-dominated shelf to a low-energy deep-water basin. They provide evidence that organic carbon preserved in these rocks was fixed by photosynthetic mat- forming microorganisms in shallow-water en- vironments and suggest that the widespread presence of siderite (FeCO 3 ) as a primary sed- iment and absence of hematite (Fe 2 O 3 ) throughout the Buck Reef Chert are most con- sistent with the hypothesis that Buck Reef Chert photosynthetic organisms were anoxygenic. The distribution of redox-sensitive trace el- ements provides a powerful means for testing this hypothesis. The abundance of Ce relative to the other rare earth elements and the abun- dance of U relative to Th were determined for rocks from each of the main facies of the Buck Reef Chert. These data, combined with our mineralogical data (Tice and Lowe, 2004), constrain the chemical species that could have been used as a primary electron donor for car- bon fixation. RARE EARTH ELEMENT DISTRIBUTIONS Bulk-rock rare earth element (REE) distri- butions (Fig. 1) normalized to post-Archean average Australian shale (Taylor and Mc- Lennan, 1985) of nearly all cherts from the Buck Reef Chert show relative depletion of light REEs (La through Sm), a feature char- acteristic of other Precambrian cherts (Derry and Jacobsen, 1990; Sugitani, 1992) and sim- ilar to modern seawater (Piepgras and Jacob- sen, 1992). Cherts from the base of the Buck Reef Chert do not show the same depletion because of contamination by admixed light REE–enriched felsic volcanic debris (Tice and Lowe, 2004). All cherts show a small enrich- ment in Eu relative to Sm and Gd. Although similar Eu enrichment in Archean cherts has been interpreted as indicating local hydrother- mal sources of Eu-enriched fluids (Sugitani, 1992), the magnitude of Buck Reef Chert Eu enrichment does not vary with depositional setting and is therefore unlikely to reflect mix- ing of marine fluids with local hydrothermal sources. It is more likely that Archean marine waters were characterized by a slight Eu en- richment (e.g., Derry and Jacobsen, 1990;