Biochemical characterization of predicted Precambrian RuBisCO (original) (raw)
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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.
Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide
Philosophical Transactions of the Royal Society B: Biological Sciences, 2012
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 .
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2014
The deep dichotomy of archaea and bacteria is evident in many basic traits including ribosomal protein composition, membrane lipid synthesis, cell wall constituents, and flagellar composition. Here we explore that deep dichotomy further by examining the distribution of genes for the synthesis of the central carriers of one carbon units, tetrahydrofolate (H 4 F) and tetrahydromethanopterin (H 4 MPT), in bacteria and archaea. The enzymes underlying those distinct biosynthetic routes are broadly unrelated across the bacterial-archaeal divide, indicating that the corresponding pathways arose independently. That deep divergence in one carbon metabolism is mirrored in the structurally unrelated enzymes and different organic cofactors that methanogens (archaea) and acetogens (bacteria) use to perform methyl synthesis in their H 4 F-and H 4 MPT-dependent versions, respectively, of the acetyl-CoA pathway. By contrast, acetyl synthesis in the acetyl-CoA pathwayfrom a methyl group, CO 2 and reduced ferredoxinis simpler, uniform and conserved across acetogens and methanogens, and involves only transition metals as catalysts. The data suggest that the acetyl-CoA pathway, while being the most ancient of known CO 2 assimilation pathways, reflects two phases in early evolution: an ancient phase in a geochemically confined and non-free-living universal common ancestor, in which acetyl thioester synthesis proceeded spontaneously with the help of geochemically supplied methyl groups, and a later phase that reflects the primordial divergence of the bacterial and archaeal stem groups, which independently invented genetically-encoded means to synthesize methyl groups via enzymatic reactions. This article is part of a Special Issue entitled: 18th European Bioenergetic Conference.
Temperature response of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalytic properties directly determines the CO 2 assimilation capacity of photosynthetic organisms as well as their survival in environments with different thermal conditions. Despite unquestionable importance of Rubisco, the comprehensive analysis summarizing temperature responses of Rubisco traits across lineages of carbon-fixing organisms is lacking. Here, we present a review of the temperature responses of Rubisco carboxylase specific activity (k c cat ) within and across domains of life. In particular, we consider the variability of temperature responses, and their ecological, physiological, and evolutionary controls. We observed over two-fold differences in the energy of activation (DH a ) among different groups of photosynthetic organisms, and found significant differences between C 3 plants from cool habitats, C 3 plants from warm habitats and C 4 plants. According to phylogenetically independent contrast analysis, DH a was not related to the species optimum growth temperature (T growth ), but was positively correlated with Rubisco specificity factor (S c/o ) across all organisms. However, when only land plants were analyzed, DH a was positively correlated with both T growth and S c/o , indicating different trends for these traits in plants versus unicellular aquatic organisms, such as algae and bacteria. The optimum temperature (T opt ) for k c cat correlated with S c/o for land plants and for all organisms pooled, but the effect of T growth on T opt was driven by species phylogeny. The overall phylogenetic signal was significant for all analyzed parameters, stressing the importance of considering the evolutionary framework and accounting for shared ancestry when deciphering relationships between Rubisco kinetic parameters. We argue that these findings have important implications for improving global photosynthesis models.
A Novel Evolutionary Lineage of Carbonic Anhydrase ( Class) Is a Component of the Carboxysome Shell
Journal of Bacteriology, 2004
A significant portion of the total carbon fixed in the biosphere is attributed to the autotrophic metabolism of prokaryotes. In cyanobacteria and many chemolithoautotrophic bacteria, CO 2 fixation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), most if not all of which is packaged in protein microcompartments called carboxysomes. These structures play an integral role in a cellular CO 2 -concentrating mechanism and are essential components for autotrophic growth. Here we report that the carboxysomal shell protein, CsoS3, from Halothiobacillus neapolitanus is a novel carbonic anhydrase (-class CA) that has an evolutionary lineage distinct from those previously recognized in animals, plants, and other prokaryotes. Functional CAs encoded by csoS3 homologues were also identified in the cyanobacteria Prochlorococcus sp. and Synechococcus sp., which dominate the oligotrophic oceans and are major contributors to primary productivity. The location of the carboxysomal CA in the shell suggests that it could supply the active sites of RuBisCO in the carboxysome with the high concentrations of CO 2 necessary for optimal RuBisCO activity and efficient carbon fixation in these prokaryotes, which are important contributors to the global carbon cycle.
Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree
Ribulose 1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO, or Rubisco) cata-lyzes a key reaction by which inorganic carbon is converted into organic carbon in the metabolism of many aerobic and anaerobic organisms. Across the broader Rubisco protein family, homologs exhibit diverse biochemical characteristics and metabolic functions, but the evolutionary origins of this diversity are unclear. Evidence of the timing of Rubisco family emergence and diversification of its different forms has been obscured by a meager paleontological record of early Earth biota, their subcellular physiology and metabolic components. Here, we use computational models to reconstruct a Rubisco family phylogenetic tree, ancestral amino acid sequences at branching points on the tree, and protein structures for several key ancestors. Analysis of historic substitutions with respect to their structural locations shows that there were distinct periods of amino acid substitution enrichment above background levels near and within its oxygen-sensitive active site and subunit interfaces over the divergence between Form III (associated with anoxia) and Form I (associated with oxia) groups in its evolutionary history. One possible interpretation is that these periods of substitutional enrichment are coincident with oxidative stress exerted by the rise of oxygenic photo-synthesis in the Precambrian era. Our interpretation implies that the periods of Rubisco substitutional enrichment inferred near the transition from anaerobic Form III to aero-bic Form I ancestral sequences predate the acquisition of Rubisco by fully derived cy-anobacterial (i.e., dual photosystem-bearing, oxygen-evolving) clades. The partitioning of extant lineages at high clade levels within our Rubisco phylogeny indicates that horizontal transfer of Rubisco is a relatively infrequent event. Therefore, it is possible that the mutational enrichment periods between the Form III and Form I common ancestral sequences correspond to the adaptation of key oxygen-sensitive components of Rubisco prior to, or coincident with, the Great Oxidation Event.
Philosophical Transactions of the Royal Society B: Biological Sciences, 2008
Two major geological problems regarding the origin of oxygenic photosynthesis are: (1) identifying a source of oxygen predating biological oxygen production and capable of driving the evolution of oxygen tolerance, and (2) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically-produced H2O2 at the surface of glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H2O2, which interacts with seawater to produce O2 in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H2O2. Answers to the second problem are controversial and range from 3.8 to 2.2 Ga. A skeptical view, based on metals that have redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the late Archaean atmosphere (< 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date ≥2.7 Ga but could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two.
Molecular Biology and Evolution, 2008
Understanding the origin and evolution of cellular processes is fundamental to understand how biological activity has shaped the history of our planet. Among these, aerobic respiration is probably one of the most debated. We have applied a phylogenomics approach to investigate the origin and evolution of dioxygen reductases (O 2 Red), the key enzymes of aerobic respiratory chains. The distribution and phylogenetic analysis of the four types of O 2 Red (Cyt-bd and the A, B, and C families of heme-copper O 2 Red) from 673 complete bacterial and archaeal genomes show that these enzymes have very different evolutionary histories: Cyt-bd are of bacterial origin and were transferred to a few archaea; CO 2 Red are of proteobacterial origin and were transferred to a few other bacteria; B-O 2 Red are of archaeal origin and were transferred to a few bacteria; and A-O 2 Red are the most ancient O 2 Red and were already present prior to the divergence of major present-day bacterial and archaeal phyla, thus before the emergence of Cyanobacteria and oxygenic photosynthesis. Implications for the origin and the evolution of aerobic respiration are discussed.