The age of Rubisco: the evolution of oxygenic photosynthesis

Abstract

The evolutionary history of oxygenesis is controversial. Form I of ribulose 1,5‐bisphosphate carboxylase/oxygenase (Rubisco) in oxygen‐tolerant organisms both enables them to carry out oxygenic extraction of carbon from air and enables the competitive process of photorespiration. Carbon isotopic evidence is presented from ~2.9 Ga stromatolites from Steep Rock, Ontario, Canada, ~2.9 Ga stromatolites from Mushandike, Zimbabwe, and ~2.7 Ga stromatolites in the Belingwe belt, Zimbabwe. The data imply that in all three localities the reef‐building autotrophs included organisms using Form I Rubisco. This inference, though not conclusive, is supported by other geochemical evidence that these stromatolites formed in oxic conditions. Collectively, the implication is that oxygenic photosynthesizers first appeared ~2.9 Ga ago, and were abundant 2.7–2.65 Ga ago. Rubisco specificity (its preference for CO2 over O2) and compensation constraints (the limits on carbon fixation) may explain the paradox that despite the inferred evolution of oxygenesis 2.9 Ga ago, the Late Archaean air was anoxic. The atmospheric CO2:O2 ratio, and hence greenhouse warming, may reflect Form I Rubisco's specificity for CO2 over O2. The system may be bistable under the warming Sun, with liquid oceans occurring in either anoxic (H2O with abundant CH4 plus CO2) or oxic (H2O with more abundant CO2, but little CH4) greenhouse states. Transition between the two states would involve catastrophic remaking of the biosphere. Build‐up of a very high atmospheric inventory of CO2 in the 2.3 Ga glaciation may have allowed the atmosphere to move up the CO2 compensation line to reach stability in an oxygen‐rich system. Since then, Form I Rubisco specificity and consequent compensation limits may have maintained the long‐term atmospheric disproportion between O2 and CO2, which is now close to both CO2 and O2 compensation barriers.

Cyanobacterial evolution during the Precambrian

“…For example, oxygenic phototrophs today show organic carbon isotope values (δ 13 C) between −30 and −25‰, a signature of the RuBisCO I enzyme operating during carbon fixation, whereas δ 13 C values for methanogens range from −45 to −35‰ due to the activity of RuBisCO III in those organisms (Fig. 5) (Schidlowski 2001;Nisbet et al 2007). Unfortunately, cyanobacteria do not possess a unique range of carbon isotope values, so these data alone cannot be used to pinpoint their presence in the rock record.…”

“…Cyanobacteria are the only organism where oxygenic photosynthesis has evolved. There is strong support for the presence of appreciable amounts (*3 × 10 −4 present atmospheric levels (PAL)) of free oxygen around 3.0-3.2 Ga from chromium, iron, molybdenum (Mo) and carbon isotopes (Nisbet et al 2007;Crowe et al 2013;Lyons et al 2014;Planavsky et al 2014;Satkoski et al 2015). Morphological analysis of stromatolites and other microbially induced sedimentary structures (MISS) support an origin of cyanobacteria by 3.2-2.7 Ga (Flannery & Walter 2012;Homann et al 2015) and perhaps even by 3.4-3.5 Ga (Hofmann et al 1999;Van Kranendonk 2006).…”

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

“…Central to this process is the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). When Rubisco evolved approximately 3 billion years ago, the enzyme operated at high CO 2 concentrations whereas oxygen (O 2 ) concentrations were negligible (Nisbet et al, 2007). Once the O 2 concentration in the cell, and later in the air, increased as a consequence of oxygenic photosynthesis, the oxygenation side reaction of Rubisco produced the dead-end metabolite 2-phosphoglycolate (2PG), sequestering a significant fraction of phosphate and carbon from the Calvin-Benson-Bassham (CBB) cycle metabolite pool.…”

Stranger in a strange land: an optimal-environments account of evolutionary mismatch

“…When the concentration of CO 2 drops too low, RubisCO can no longer fix carbon for the organism. (Nisbet et al (2007)) Thus, Lloyd et al contend, in any oxygenrich environment RubisCO will result in a mismatch. In cyanobacteria, for example, this (putative) mismatch is ameliorated by pathways which transport CO 2 to the carboxysome, "a microcompartment containing RubisCO in 8 See, e.g., Buller (2006).…”

“…(Nisbet et al (2007)) Lloyd et al say that in some cases, like RubisCO, mismatches "can become permanent features of life" which are compensated for rather than eliminated by further evolution.…”