Timescales of Oxygenation Following the Evolution of Oxygenic Photosynthesis

Abstract

Among the most important bioenergetic innovations in the history of life was the invention of oxygenic photosynthesis-autotrophic growth by splitting water with sunlight-by Cyanobacteria. It is widely accepted that the invention of oxygenic photosynthesis ultimately resulted in the rise of oxygen by ca. 2.35 Gya, but it is debated whether this occurred more or less immediately as a proximal result of the evolution of oxygenic Cyanobacteria or whether they originated several hundred million to more than one billion years earlier in Earth history. The latter hypothesis involves a prolonged period during which oxygen production rates were insufficient to oxidize the atmosphere, potentially due to redox buffering by reduced species such as higher concentrations of ferrous iron in seawater. To examine the characteristic timescales for environmental oxygenation following the evolution of oxygenic photosynthesis, we applied a simple mathematical approach that captures many of the salient features of the major biogeochemical fluxes and reservoirs present in Archean and early Paleoproterozoic surface environments. Calculations illustrate that oxygenation would have overwhelmed redox buffers within ~100 kyr following the emergence of oxygenic photosynthesis, a geologically short amount of time unless rates of primary production were far lower than commonly expected. Fundamentally, this result arises because of the multiscale nature of the carbon and oxygen cycles: rates of gross primary production are orders of magnitude too fast for oxygen to be masked by Earth's geological buffers, and can only be effectively matched by respiration at non-negligible O2 concentrations. These results suggest that oxygenic photosynthesis arose shortly before the rise of oxygen, not hundreds of millions of years before it.

Early Archean origin of Photosystem II

“…For example, Ward et al. () calculated that the planet could have become oxygenated within just one hundred thousand years from the origin of oxygenic photosynthesis. Thus, in a hypothetical scenario in which a non‐photosynthetic ancestor of Cyanobacteria obtained photosynthesis via HGT from an anoxygenic phototroph, and this transferred reaction center evolved standard levels of oxygen evolution within one hundred thousand years (ΔT = 0.1 Ma), then ν max would need to be more than 400 thousand amino acid changes per site per Ga, which is orders of magnitude greater than the rate of evolution of any known protein (Table ).…”

“…We denote this span of time by ΔT. If ΔT is small, such as a few million years or less for example, then the evolution of oxygenic photosynthesis may be better described as a sudden and fast process only getting started shortly before the GOE as suggested by some recent analyses (Shih, Hemp et al., ; Ward, Kirschvink, & Fischer, ). On the other hand, if ΔT is large: Several hundred million years or more for example, then the earliest stages in the evolution of oxygenic photosynthesis could significantly predate the GOE as suggested by some geochemical (Mukhopadhyay et al., ; Planavsky et al., ; Satkoski, Beukes, Li, Beard, & Johnson, ) and phylogenetic data (Blank & Sanchez‐Baracaldo, ; Schirrmeister, de Vos, Antonelli, & Bagheri, ).…”

Microbial diversity and iron oxidation at Okuoku‐hachikurou Onsen, a Japanese hot spring analog of Precambrian iron formations

“…While substantial debate exists about the antiquity of Cyanobacteria, multiple lines of evidence suggest that oxygenic photosynthesis evolved only shortly before the GOE Johnson et al, 2013a;Shih et al, 2017;Ward, Kirschvink, & Fischer, 2016), and therefore, molecular oxygen derived from photosynthesis was unlikely to play a role in Archean BIF formation. 2.3 Ga.…”

The timetable of evolution

“…Ward et al . ( 180 ) modeled the GOE as the initial appearance of oxygenic photosynthesis but similarly concluded that the oxic transition was rapid. Our simple model of bacterial sequence evolution, introduced above, would suggest that shifting redox conditions would quickly be exploited by bacteria with novel physiologies that make use of oxygen in energy metabolism or biosynthesis.…”