Algal evolution in relation to atmospheric CO ₂ : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

Abstract

Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco) -photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO 2 assimilation. The high CO 2 and (initially) O 2 -free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO 2 decreased and O 2 increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO 2 affinity and CO 2 /O 2 selectivity correlated with decreased CO 2 -saturated catalytic capacity and/or for CO 2 -concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco -PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO 2 episode followed by one or more lengthy high-CO 2 episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO 2 ocean. More investigations, including studies of genetic adaptation, are needed.

Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia

“…Favourable growth of N. scintillans under hypoxia is not unrealistic, given that its endosymbiont P. noctilucae evolved 1.3 Ga years ago when oceanic O 2 concentrations were much lower than in the modern world, making its carbon assimilation pathways and enzyme systems more uniquely suited to hypoxic environments 25 . Oxygen deficiency 26,27 in the northeastern Arabian Sea is a unique mid-depth (4120-1,500 m) feature formed by the combined influences of monsoon-driven high surface productivity of the semi-annual phytoplankton blooms, sub- 13 , there are no known physical mechanisms to explain the appearance of O 2 deficient waters above 40 m in the offshore region in winter.…”

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

“…The geologic record has sufficient resolution to affirm that highly derived organisms harboring Rubisco, most notably algal and plant clades that emerged toward the end of the Proterozoic eon (Butterfield, Knoll, & Swett, 1990; Raven, Giordano, Beardall, & Maberly, 2012), have greatly impacted carbon and oxygen reservoirs and played important roles in facilitating the conversion of CO 2 to reduced organic carbon over Earth's recent history (Mccourt, Delwiche, & Karol, 2004; Tabita, 1999). This is also presumed to be the case for Earth's more distant past with respect to photosynthetic bacteria, though perhaps to a lesser magnitude (Blank & Sanchez‐Baracaldo, 2010).…”

Genetic diversity of inorganic carbon uptake systems causes variation in CO2 response of the cyanobacterium Microcystis

“…Cyanobacteria have had a long evolutionary history, during which they have developed highly efficient CO 2 -concentrating mechanisms (CCMs) that enable them to grow well at a wide range of C i conditions (Kaplan and Reinhold, 1999;Giordano et al, 2005;Badger et al, 2006;Price et al, 2008;Raven et al, 2012). The CCMs of cyanobacteria are structurally and phylogenetically different from those of most eukaryotic algae (Raven, 2010;Wang et al, 2011b), and it has been argued that bloomforming cyanobacteria are particularly adept to compete at the low CO 2 and high-pH conditions typical of dense blooms (Shapiro, 1990).…”