Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide (original) (raw)
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Evolution, 2006
Selective history is thought to constrain the extent and direction of future adaptation by limiting access to genotypes that are advantageous in a novel environment. Populations of Chlamydomonas previously selected at high CO 2 were either backselected at ambient levels of CO 2 , or selected at levels of CO 2 that last occurred during glaciation in the Pleistocene. There was no effect of selective history on adaptation to either level of CO 2 , and the high CO 2 phenotypes were evolutionarily reversible such that fitness in ambient CO 2 returned to values seen in controls. CO 2 uptake affinity improved relative to the ancestor in both ambient and glacial CO 2 , although wild-type regulation of CO 2 uptake, which deteriorated during previous selection at high CO 2 , was not restored by selection at lower levels of CO 2 . Trade-offs in both CO 2 uptake affinity and growth were seen after selection at any given level of CO 2 . Adaptation to ambient and glacial-era levels of CO 2 produced a range of phenotypes, suggesting that chance rather than selective history contributes to the divergence of replicate populations in this system.
The age of Rubisco: the evolution of oxygenic photosynthesis
Geobiology, 2007
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.
Algal constraints on the cenozoic history of atmospheric CO2
Geochimica et Cosmochimica Acta, 2006
An urgent question for future climate, in light of increased burning of fossil fuels, is the temperature sensitivity of the climate system to atmospheric carbon dioxide (pCO 2 ). To date, no direct proxy for past levels of pCO 2 exists beyond the reach of the polar ice core records. We propose a new methodology for placing an upper constraint on pCO 2 5 over the Cenozoic based on the living geological record. Specifically, our premise is that the contrasting calcification tolerance of various extant species of coccolithophore to raised pCO 2 reflects an "evolutionary memory" of past atmospheric composition. The different times of first emergence of each morphospecies allows an upper constraint of past pCO 2 to be placed on Cenozoic timeslices. Further, our hypothesis has 10 implications for the response of marine calcifiers to ocean acidification. Geologically "ancient" species, which have survived large changes in ocean chemistry, are likely more resilient to predicted acidification.
Biochemical characterization of predicted Precambrian RuBisCO
Nature Communications, 2016
The antiquity and global abundance of the enzyme, RuBisCO, attests to the crucial and longstanding role it has played in the biogeochemical cycles of Earth over billions of years. The counterproductive oxygenase activity of RuBisCO has persisted over billions of years of evolution, despite its competition with the carboxylase activity necessary for carbon fixation, yet hypotheses regarding the selective pressures governing RuBisCO evolution have been limited to speculation. Here we report the resurrection and biochemical characterization of ancestral RuBisCOs, dating back to over one billion years ago (Gyr ago). Our findings provide an ancient point of reference revealing divergent evolutionary paths taken by eukaryotic homologues towards improved specificity for CO 2 , versus the evolutionary emphasis on increased rates of carboxylation observed in bacterial homologues. Consistent with these distinctions, in vivo analysis reveals the propensity of ancestral RuBisCO to be encapsulated into modern-day carboxysomes, bacterial organelles central to the cyanobacterial CO 2 concentrating mechanism.
Coccolithophore cell size and the Paleogene decline in atmospheric CO2
Earth and Planetary Science Letters, 2008
Alkenone-based Cenozoic records of the partial pressure of atmospheric carbon dioxide (pCO 2 ) are founded on the carbon isotope fractionation that occurred during marine photosynthesis (ε p37:2 ). However, the magnitude of ε p37:2 is also influenced by phytoplankton cell sizea consideration lacking in previous alkenone-based CO 2 estimates. In this study, we reconstruct cell size trends in ancient alkenone-producing coccolithophores (the reticulofenestrids) to test the influence that cell size variability played in determining ε p37:2 trends and pCO 2 estimates during the middle Eocene to early Miocene. At the investigated deep-sea sites, the reticulofenestrids experienced high diversity and largest mean cell sizes during the late Eocene, followed by a long-term decrease in maximum cell size since the earliest Oligocene. Decreasing haptophyte cell sizes do not account for the long-term increase in the stable carbon isotopic composition of alkenones and associated decrease in ε p37:2 values during the Paleogene, supporting the conclusion that the secular pattern of ε p37:2 values is primarily controlled by decreasing CO 2 concentration since the earliest Oligocene. Further, given the physiology of modern alkenone producers, and considering the timings of coccolithophorid cell size change, extinctions, and changes in reconstructed pCO 2 and temperature, we speculate that the selection of smaller reticulofenestrid cells during the Oligocene primarily reflects an adaptive response to increased [CO 2(aq) ] limitation.
Highest plasticity of carbon-concentrating mechanisms in earliest evolved phytoplankton
Limnology and Oceanography Letters
Photosynthesis evolved in oceans of a distant past, when CO 2 partial pressure was high. Over time, pCO 2 dropped while O 2 levels increased. Consequently, phytoplankton required carbon-concentrating mechanisms (CCMs) to actively supply their carbon-fixing enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase with sufficient inorganic carbon. Earlier evolved phytoplankton groups were shown to possess more active CCMs, because they had to deal with decreasing pCO 2 and increasing O 2 levels. In this study, we examined whether these earlier evolved groups are also more plastic in their CCMs than later evolved groups. Our analysis shows that earlier evolved groups, i.e., cyanobacteria and dinoflagellates, exhibit a high CCM plasticity toward elevated pCO 2 , whereas the more recently evolved haptophytes and diatoms do not. These findings improve our understanding of the evolution of CCMs and support predictions of phytoplankton group responses toward elevated pCO 2 .
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 2concentrating 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.
A coccolithophore concept for constraining the Cenozoic carbon cycle
Biogeosciences, 2007
An urgent question for future climate, in light of increased burning of fossil fuels, is the temperature sensitivity of the climate system to atmospheric carbon dioxide (pCO 2 ). To date, no direct proxy for past levels of pCO 2 exists beyond the reach of the polar ice core records. We propose a new methodology for placing a constraint on pCO 2 over the Cenozoic based on the physiological plasticity of extant coccolithophores. Specifically, our premise is that the contrasting calcification tolerance 1 of various extant species of coccolithophore to raised pCO 2 reflects an "evolutionary memory" of past atmospheric composition. The different times of evolution of certain morphospecies allows an upper constraint of past pCO 2 to be placed on Cenozoic timeslices. Further, our hypothesis has implications for the response of marine calcifiers to ocean acidification. Geologically "ancient" species, which have survived large changes in ocean chemistry, are likely more resilient to predicted acidification.
Biomarker Evidence for Photosynthesis During Neoproterozoic Glaciation
Science, 2005
Laterally extensive black shales were deposited on the São Francisco craton in southeastern Brazil during low-latitude Neoproterozoic glaciation È740 to 700 million years ago. These rocks contain up to 3.0 weight % organic carbon, which we interpret as representing the preserved record of abundant marine primary productivity from glacial times. Extractable biomarkers reflect a complex and productive microbial ecosystem, including both phototrophic bacteria and eukaryotes, living in a stratified ocean with thin or absent sea ice, oxic surface waters, and euxinic conditions within the photic zone. Such an environment provides important constraints for parts of the ''Snowball Earth'' hypothesis.