Geological constraints on the origin of oxygenic photosynthesis

Abstract

This article examines the geological evidence for the rise of atmospheric oxygen and the origin of oxygenic photosynthesis. The evidence for the rise of atmospheric oxygen places a minimum time constraint before which oxygenic photosynthesis must have developed, and was subsequently established as the primary control on the atmospheric oxygen level. The geological evidence places the global rise of atmospheric oxygen, termed the Great Oxidation Event (GOE), between ~2.45 and ~2.32 Ga, and it is captured within the Duitschland Formation, which shows a transition from mass-independent to mass-dependent sulfur isotope fractionation. The rise of atmospheric oxygen during this interval is closely associated with a number of environmental changes, such as glaciations and intense continental weathering, and led to dramatic changes in the oxidation state of the ocean and the seawater inventory of transition elements. There are other features of the geologic record predating the GOE by as much as 200-300 million years, perhaps extending as far back as the Mesoarchean-Neoarchean boundary at 2.8 Ga, that suggest the presence of low level, transient or local, oxygenation. If verified, these features would not only imply an earlier origin for oxygenic photosynthesis, but also require a mechanism to decouple oxygen production from oxidation of Earth's surface environments. Most hypotheses for the GOE suggest that oxygen production by oxygenic photosynthesis is a precondition for the rise of oxygen, but that a synchronous change in atmospheric oxygen level is not required by the onset of this oxygen source. The potential lag-time in the response of Earth surface environments is related to the way that oxygen sinks, such as reduced Fe and sulfur compounds, respond to oxygen production. Changes in oxygen level imply an imbalance in the sources and sinks for oxygen. Changes in the cycling of oxygen have occurred at various times before and after the GOE, and do not appear to require corresponding changes in the intensity of oxygenic photosynthesis. The available geological constraints for these changes do not, however, disallow a direct role for this metabolism. The geological evidence for early oxygen and hypotheses for the controls on oxygen level are the basis for the interpretation of photosynthetic oxygen production as examined in this review.

Iron formations: A global record of Neoarchaean to Palaeoproterozoic environmental history

“…The GOE represents a transition from an atmosphere that was essentially devoid of free oxygen (O 2 << 10 -5 PAL) to one with O 2 concentrations >10 -5 PAL, where estimates of oxygen levels are based on modelling massindependent S isotope (S-MIF) variations (Pavlov and Kasting, 2002). In the rock record, this event is manifested by a number of changes (see Farquhar et al, 2011Farquhar et al, , 2014, for reviews), including (1) loss of easily oxidisable detrital uraninite, pyrite, and siderite from fluvial siliciclastic sediments at ca. 2.4 Ga (e.g., Rasmussen and Buick, 1999;England et al, 2002;Hofmann et al, 2009;Johnson et al, 2014); (2) loss of iron from ancient soil horizons (paleosols) older than ca.…”

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

“…The Precambrian evolution of the oxygenated atmosphere was strongly coupled to the evolution of oxygenic photosynthesis (Farquhar, Zerkle, & Bekker, 2011). There are numerous pathways for the uptake of carbon from the environment (Boyle and Morgan, 2011), but the Rubisco protein catalyzes the addition of CO 2 and H 2 O to 1,5‐ribulose bisphosphate (RuBP) in the first major step of carbon fixation through photosynthesis.…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…The deposition of sedimentary organic matter also can also be correlated with changes in the nitrogen cycle (Farquhar et al 2010 and references therein) that would likely have involved the cyanobacteria as significant contributors. However, the general assumption is that much of the fixed carbon in sediments is from anoxic photosynthetic bacteria, the presumed independent progenitors of the photosynthetic reaction centers (RCI, RCII).…”

“…The co-editors of this volume (Gantt and Falkowski) have invited specialists from a broad range of disciplines to benefit those readers interested in a comprehensive understanding of oxygenic photosynthesis. Major topics being addressed in the accompanying series of articles relate to the evidence and time-lines of oxygenic photosynthesis on the earth (Farquhar et al 2010), the resultant gains of an aerobic atmosphere and the increase in organismal size and diversity, as well as multicellularity (Payne et al 2010). At the organismal level, some of the biggest questions are: what were the original key characteristics from which the photosynthetic reaction centers were derived (Allen and Williams 2010), what essential changes were required for electron production by the water splitting complex (Williamson et al 2010), and what is the evidence for the timeline of how long cyanobacteria have been around (Schopf 2010)?…”

“…Among geologists and geochemists, it is generally agreed that the atmosphere and oceans were devoid of oxygen until ca. 2.45 BYa, the time of the great oxidation event (Canfield 2005;Farquhar et al 2010). Yet considerable allowances have to be made for a lag in time, differences in local environments before the notable O 2 rise resulted in a transition from anoxia to the estimated ca.…”