CARBON FIXATION Cyanobacteria use the reducing power and energy derived from photochemistry to fix carbon

The origin of oxygenic photosynthesis was the most important metabolic innovation in Earth history. It allowed life to generate energy and reducing power directly from sunlight and water, freeing it from the limited resources of geochemically derived reductants. This greatly increased global primary productivity and restructured ecosystems. The release of O2 as an end product of water oxidation led to the rise of oxygen, which dramatically altered the redox state of Earth’s atmosphere and oceans and permanently changed all major biogeochemical cycles. Furthermore, the biological availability of O2 allowed for the evolution of aerobic respiration and novel biosynthetic pathways, facilitating much of the richness we associate with modern biology, including complex multicellularity. Here we critically review and synthesize information from the geological and biological records for the origin and evolution of oxygenic photosynthesis. Data from both of these archives illustrate that this metabolism first appeared in early Paleoproterozoic time and, despite its biogeochemical prominence, is a relatively late invention in the context of our planet’s history. 647 Click here to view this article's online features: • Download figures as PPT slides • Navigate linked references • Download citations • Explore related articles • Search keywords ANNUAL REVIEWS Further A nn u. R ev . E ar th P la ne t. Sc i. 20 16 . 4 4: 64 768 3. D ow nl oa de d fr om w w w . a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y C al if or ni a In st itu te o f T ec hn ol og y on 0 7/ 14 /1 6. F or p er so na l u se o nl y. EA44CH24-Fischer ARI 17 May 2016 19:44 Chlorophyll: chlorin pigments found in all oxygenic and some anoxygenic phototrophs that absorb photons to provide the energy needed for photochemistry Anoxygenic phototroph: a phototrophic organism that uses electron donors other than water INTRODUCTION Oxygenic photosynthesis is an evolutionary singularity—it evolved once in the ancestors of modern Cyanobacteria. Understanding its origin and evolution is a grand-challenge problem in geobiology that requires integrating insights from multiple disparate scientific fields, including comparative biology, genomics, biochemistry, ecology, geology, geochemistry, and paleontology. Each of these approaches views the problem through a different lens, providing perspectives that have individual strengths and weaknesses. Biological studies, on the one hand, allow access to molecular diversity, illuminate mechanistic details, and enable rigorous hypothesis testing. However, they can ordinate evolutionary events only in relative time, and they are blind to extinction because they rely on extant organisms. Geology and geochemistry, on the other hand, provide an empirical historical record of phototrophic and photosynthetic processes, enabling absolute timing of key events. However, these approaches are limited by challenges associated with accurately reading ancient chemistry from sedimentary rocks and can paint metabolic and ecological processes only in broad and coarse brushstrokes. Because the geological and biological records present different perspectives of the same history, their integration should provide a consistent view. This logic frames our pedagogy here. We begin with an overview of the mechanisms and diversity of chlorophyll-based phototrophy. We then discuss insights into the origin and evolution of oxygenic photosynthesis gained from the geological and biological records, focusing on geological evidence for O2 and the discovery of deep-branching nonphototrophic Cyanobacteria. We end by discussing an emerging testable hypothesis consistent with available data: Oxygenic photosynthesis may have evolved via an Mn-oxidizing intermediate in ancestral Cyanobacteria, near in time to the rise of oxygen. PHOTOTROPHY’S MOLECULAR MECHANICS Phototrophy is the process by which organisms convert the energy carried in photons into electrochemical energy useful to cells (Blankenship 2014, Overmann & Garcia-Pichel 2013). There are two types of phototrophy known: chlorophyll-based chlorophototrophy and rhodopsin-based phototrophy (Bryant & Frigaard 2006). Here we focus exclusively on chlorophototrophy because it was single-handedly responsible for the greatest environmental transition in Earth history—the rise of oxygen. In addition to generating energy from sunlight, photosynthetic organisms fix either CO2 or bicarbonate into biomass. Anoxygenic phototrophs derive the electrons needed for energy generation from reduced inorganic and organic compounds, such as Fe2+, H2, S0, HS−, S2O32−, NO2−, AsO33−, and various organic central metabolism intermediates. In contrast, oxygenic photosynthesis uses electrons originating from water, generating O2 as product: nCO2 + H2O + light→ (CH2O)n + O2. This reaction conceals substantial biochemical complexity. It is useful to decompose the net reaction into separate components consisting of those directly involved in photochemistry and those involved in carbon fixation, given that not all phototrophs fix inorganic carbon and, moreover, that these distinct processes have different evolutionary histories. Here we focus on the light reactions because they are the key components that perform photochemistry coupled to water oxidation. A brief discussion of the carbon fixation reactions can be found in the sidebar Carbon Fixation. Photochemical Reactions Phototrophy is powered by reaction centers (called photosystems in Cyanobacteria), molecular machines that transduce light energy into chemical energy. When a reaction center absorbs a photon of light, or receives an exciton of energy from neighboring light-gathering antennae, it undergoes a charge separation event (Blankenship 2014) (Figure 1). This allows the reaction 648 Fischer · Hemp · Johnson A nn u. R ev . E ar th P la ne t. Sc i. 20 16 . 4 4: 64 768 3. D ow nl oa de d fr om w w w . a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y C al if or ni a In st itu te o f T ec hn ol og y on 0 7/ 14 /1 6. F or p er so na l u se o nl y. EA44CH24-Fischer ARI 17 May 2016 19:44