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

Abstract

Rubisco, the most abundant enzyme on the Earth and responsible for all photosynthetic carbon fixation, is often thought of as a highly conserved and sluggish enzyme. Yet, different algal Rubiscos demonstrate a range of kinetic properties hinting at a history of evolution and adaptation. Here, we show that algal Rubisco has indeed evolved adaptively during ancient and distinct geological periods. Using DNA sequences of extant marine algae of the red and Chromista lineage, we define positive selection within the large subunit of Rubisco, encoded by rbcL, to occur basal to the radiation of modern marine groups. This signal of positive selection appears to be responding to changing intracellular concentrations of carbon dioxide (CO 2 ) triggered by physiological adaptations to declining atmospheric CO 2 . Within the ecologically important Haptophyta (including coccolithophores) and Bacillariophyta (diatoms), positive selection occurred consistently during periods of falling Phanerozoic CO 2 and suggests emergence of carbon-concentrating mechanisms. During the Proterozoic, a strong signal of positive selection after secondary endosymbiosis occurs at the origin of the Chromista lineage (approx. 1.1 Ga), with further positive selection events until 0.41 Ga, implying a significant and continuous decrease in atmospheric CO 2 encompassing the Cryogenian Snowball Earth events. We surmise that positive selection in Rubisco has been caused by declines in atmospheric CO 2 and hence acts as a proxy for ancient atmospheric CO 2 .

Paleobiological Perspectives on Early Eukaryotic Evolution

“…Increased microfossil diversity immediately preceded an interval of global glaciations, popularly known as the Snowball Earth (Hoffman et al 1998). Changes in both export fluxes and mean Redfield ratios of an increasingly eukaryotic phytoplankton have been implicated in the CO 2 drawdown that initiated glaciation (Tziperman et al 2011), and decreasing pCO 2 has, in turn, been postulated to drive adaptive evolution in Rubsico, the key enzyme in CO 2 fixation by algae and cyanobacteria (Young et al 2012). Tectonic changes also characterized the later Neoproterozoic Earth, and these also influenced atmospheric chemistry and climate.…”

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

“…A Rubisco with a high CO 2 -saturated catalytic capacity, and a correspondingly low CO 2 affinity and CO 2 /O 2 selectivity, such as occurs in the form IA and form IB Rubiscos of extant cyanobacteria, would be expected to present a stronger evolutionary case for a CCM at a given CO 2 concentration and CO 2 /O 2 ratio than would eukaryotic form IB and form ID Rubisco with higher CO 2 affinity and CO 2 /O 2 selectivity but a lower CO 2 -saturated maximum catalytic rate [65]. Young et al [107] have used molecular phylogenetic evidence to show that there was positive selection of the form ID Rubiscos in some eukaryotes that correspond to low-CO 2 and low-CO 2 /O 2 episodes in the geological record, and that these episodes of positive selection could have corresponded to the time of evolution of CCMs. To be effective, the CCM must maintain a higher CO 2 concentration at the site of Rubisco than would be possible by CO 2 diffusion alone [10].…”

Evolution of C 4 plants: a new hypothesis for an interaction of CO 2 and water relations mediated by plant hydraulics

“…The pigments and proteins involved in C 3 photosynthesis are highly conserved across photosynthetic organisms, and this pathway operates unmodified in the majority of species, termed 'C 3 plants'. However, the basic C 3 pathway has also been augmented by carbon-concentrating mechanisms (CCMs) in multiple lineages, many of which evolved during the Early Neogene following a massive depletion of atmospheric CO 2 [2][3][4][5]. 'C 4 photosynthesis' is a collective term for CCMs which initially fix carbon into four-carbon organic acids via the enzyme phosphoenolpyruvate carboxylase (PEPC) [6], and then liberate CO 2 from these C 4 acids to feed the C 3 pathway within a compartment of the cell or leaf [7,8] (figure 1a).…”