Geobiology (2007), 5, 101–117 DOI: 10.1111/j.1472-4669.2007.00105.x © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd 101 Blackwell Publishing Ltd ORIGINAL ARTICLE Pre-photosynthetic biosphere Niches of the pre-photosynthetic biosphere and geologic preservation of Earth’s earliest ecology NORMAN H. SLEEP 1 AND DENNIS K. BIRD 2 1 Department of Geophysics, Stanford University, Stanford, California 94305, USA 2 Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, USA ABSTRACT The tree of terrestrial life probably roots in non-photosynthetic microbes. Chemoautotrophs were the first primary producers, and the globally dominant niches in terms of primary productivity were determined by availability of carbon dioxide and hydrogen for methanogenesis and sulfite reduction. Methanogen niches were most abundant where CO 2 -rich ocean water flowed through serpentinite. Black smoker vents from basalt supplied comparable amount of H 2 . Hydrogen from arc volcanoes supported a significant methanogenic niche at the Earth’s surface. SO 2 from arc volcanoes reacted with organic matter and hydrogen, providing a significant surface niche. Methane ascended to the upper atmosphere where photolysis produced C-rich haze and CO, and H escaped into space. The CO and C-rich haze supported secondary surface niches. None of these ecologies were bountiful; less than 1% of the CO 2 vented by ridge axes, arcs, and metamorphism became organic matter before it was buried in carbonate. In contrast, a photosynthetic biosphere leaves copious amounts of organic carbon, locally concentrated in sediments. Black shales are a classic geologic biosignature for photosynthesis that can survive subduction and high-grade metamorphism. Received 16 June 2006; accepted 20 February 2007 Corresponding author: N. H. Sleep, Tel.: 650-723-0882; fax: 650-725-7344; e-mail: norm@pangea.stanford.edu. INTRODUCTION The ecology of modern Earth is so dominated by photo- synthesis that it is difficult to envision the biosphere before this metabolic innovation. Throughout geologic time, the consequences of photosynthesis have significantly modified the composition of Earth’s atmosphere and hydrosphere, and, ultimately, chemical reactions between Earth’s fluid envelopes and the lithosphere (cf. Holland, 1962, 1984; Cloud, 1968, Garrels & MacKenzie, 1971; Garrels & Perry, 1974; more recently: Dismukes et al ., 2001; Hoehler et al ., 2001b; Kasting & Siefert, 2002; Berner et al ., 2003; Knoll, 2003; Holland, 2004; Canfield, 2005; Kopp et al ., 2005; Rosing et al ., 2006). Evidence for photosynthesis appears in even the oldest rocks (cf. Des Marais 2000; Rosing & Frei, 2004; Tice & Lowe, 2004; Olson, 2006; Westall & Southam, 2006). Although the tree of life roots in non-photosynthetic microbes (e.g. Woese et al ., 1990; Pace, 1991, 1997; Reysenbach & Shock, 2002; Olson & Blankenship, 2004; Nealson & Rye, 2004), geologic evidence of extant life that is not at least peripherally affected by the products of photosynthesis is rare. Thus, characterizing sources of energy for metabolic processes independent of photosynthesis is critical to understanding the ecology of early Earth (Shock 1997; Shock & Schulte, 1998), and to developing search strategies for ancient biosignatures and extant life on Earth, Mars, Venus and Europa (cf. Boston et al ., 1992; Jakosky & Shock, 1998; Fisk & Giovannoni, 1999; McCollom, 1999; Zolotov & Shock, 2004; Sleep et al ., 2004; Schulte et al ., 2006). The energetics of living organisms is dependent on cycles of non-equilibrium electron transfers (Falkowski, 2006). In the pre-photosynthetic biosphere the most important redox systems providing energy for metabolic processes involve the elements Fe, S, and C together with H and O (cf. Walker, 1977), and viable niches were formed where tectonic and/or fluid movement (magma, water, air) brought together comb- inations of these elements with incompatible oxidation states (cf. Shock et al ., 1995; Nisbet & Sleep, 2001; Nisbet & Fowler, 2004; Nealson & Rye, 2004; Kharecha et al ., 2005; Canfield et al ., 2006). In this paper, we consider first-order thermodynamic and mass balance constraints on chemoautotrophic biospheres in order to identify viable bountiful niches prior to the evolution of photosynthesis. Our objective is to predict where biosign- atures might be found in Earth’s earliest geologic record and where one might find existing analog communities. As earliest