Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age

Abstract

Molecular oxygen (O2) began to accumulate in the atmosphere and surface ocean ca. 2,400 million years ago (Ma), but the persistent oxygenation of water masses throughout the oceans developed much later, perhaps beginning as recently as 580 -550 Ma. For much of the intervening interval, moderately oxic surface waters lay above an oxygen minimum zone (OMZ) that tended toward euxinia (anoxic and sulfidic). Here we illustrate how contributions to primary production by anoxygenic photoautotrophs (including physiologically versatile cyanobacteria) influenced biogeochemical cycling during Earth's middle age, helping to perpetuate our planet's intermediate redox state by tempering O 2 production. Specifically, the ability to generate organic matter (OM) using sulfide as an electron donor enabled a positive biogeochemical feedback that sustained euxinia in the OMZ. On a geologic time scale, pyrite precipitation and burial governed a second feedback that moderated sulfide availability and water column oxygenation. Thus, we argue that the proportional contribution of anoxygenic photosynthesis to overall primary production would have influenced oceanic redox and the Proterozoic O 2 budget. Later Neoproterozoic collapse of widespread euxinia and a concomitant return to ferruginous (anoxic and Fe 2؉ rich) subsurface waters set in motion Earth's transition from its prokaryote-dominated middle age, removing a physiological barrier to eukaryotic diversification (sulfide) and establishing, for the first time in Earth's history, complete dominance of oxygenic photosynthesis in the oceans. This paved the way for the further oxygenation of the oceans and atmosphere and, ultimately, the evolution of complex multicellular organisms.ocean chemistry ͉ primary production ͉ Proterozoic biosphere

Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide

“…This relaxes pressure for Rubisco to have a high affinity for CO 2 and therefore allows an increase in V c , which results in increased photosynthetic efficiency as the plant requires less nitrogen to achieve a given CO 2 [4,6,20] and K c (dark blue bars) [6,21] with standard error bars and number of species measured (n) are shown. [55,56].…”

“…The advent of oxygenic photosynthesis around 2.4 Ga increased atmospheric and surface ocean O 2 levels and reduced atmospheric CO 2 . However, O 2 levels remained low for the next billion years despite declining CO 2 [1], partly attributed to anoxygenic photosynthesis preventing oxygenation of the deep ocean [2]. It was not until the Neoproterozoic when oxygenic photosynthesis became dominant, hypothesized to contribute to the second rise of O 2 which paved the way for evolution of complex multi-cellular life [1].…”

“…where V c and V o are maximal velocities of the carboxylase and oxygenase reactions and K c and K o are the Michaelis constants for CO 2 and O 2 . Thermodynamic constraints dictate a trade-off between carboxylation velocity (V c ) and affinity for CO 2 that has led to suggestions that despite being conserved and sluggish, Rubisco is optimized to its physical environment [4].…”

“…During oxygenic photosynthesis, Rubisco catalyses the two competitive reactions: CO 2 fixation for photosynthesis (carboxylation) and energy-wasting photorespiration using O 2 (oxygenation). The ability of a particular Rubisco to discriminate between non-polar, structurally similar substrates of CO 2 and O 2 is determined by the kinetic properties of Rubisco and the CO 2 and O 2 concentrations at the catalytic site of the enzyme, denoted as the specificity factor (V) [3]:…”

An early productive ocean unfit for aerobics

“…About a decade ago, Canfield (1) offered a very different possibility-that ventilation of the deep ocean lagged behind the GOE by more than a billion years, resulting in a vast, deep reservoir of hydrogen sulfide, but long-held presumptions about photosynthetic life in the surface waters remained untouched. In the first comprehensive biogeochemical model of this ''Canfield Ocean,'' Johnston et al (2) in a recent issue of PNAS present a stunningly different take on those early photosynthesizers-one in which the upper, light-containing layers indeed drove biological production but without the expected concomitant release of oxygen. And it is this feedback that may explain a troubling uncertainty about the Canfield Ocean and this time interval in generalexactly how oxygen in the biosphere remained at only a fraction of modern levels for so long after the GOE.…”