Biochemical characterization of predicted Precambrian RuBisCO

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Abstract

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.

Abstract

The enzyme RuBisCO has evolved over billions of years and catalyses reactions in plants and bacteria, although why some reactions persist is unclear. Here, the authors resurrect ancestral RuBisCO to reveal aspects of the Precambrian atmosphere and the selective pressures governing RuBisCO evolution.

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Most cited references 41

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F. Abascal, R Zardoya, D Posada (2005)

Using an appropriate model of amino acid replacement is very important for the study of protein evolution and phylogenetic inference. We have built a tool for the selection of the best-fit model of evolution, among a set of candidate models, for a given protein sequence alignment. ProtTest is available under the GNU license from http://darwin.uvigo.es

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CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution.

Mario Giordano, John Beardall, John Raven (2005)

The evolution of organisms capable of oxygenic photosynthesis paralleled a long-term reduction in atmospheric CO2 and the increase in O2. Consequently, the competition between O2 and CO2 for the active sites of RUBISCO became more and more restrictive to the rate of photosynthesis. In coping with this situation, many algae and some higher plants acquired mechanisms that use energy to increase the CO2 concentrations (CO2 concentrating mechanisms, CCMs) in the proximity of RUBISCO. A number of CCM variants are now found among the different groups of algae. Modulating the CCMs may be crucial in the energetic and nutritional budgets of a cell, and a multitude of environmental factors can exert regulatory effects on the expression of the CCM components. We discuss the diversity of CCMs, their evolutionary origins, and the role of the environment in CCM modulation.

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Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

Laura Wegener Parfrey, Daniel J G Lahr, Andrew H Knoll … (2011)

Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.

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Author and article information

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group

ISSN (Electronic): 2041-1723

Publication date (Electronic): 21 January 2016

Publication date Collection: 2016

Volume: 7

Electronic Location Identifier: 10382

Affiliations

[1 ]Department of Plant and Microbial Biology, University of California , Berkeley, California 94720-3102, USA

[2 ]Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden , Herts AL5 2JQ, UK

[3 ]Lancaster Environment Centre, Lancaster University , Bailrigg, Lancaster LA1, 4YQ, UK

[4 ]Department of Biochemistry and Molecular Biology, DOE Plant Research Laboratories, Michigan State University , East Lansing, Michigan 488242, USA

[5 ]Physical Biosciences Division, Lawrence Berkeley National Laboratory , Berkeley, California 94720, USA

Author notes

[a ] pmshih@ 123456gmail.com

[b ] ckerfeld@ 123456lbl.gov

[*]

These authors contributed equally to this work.

[†]

Present address: Joint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.

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Publisher Item ID: ncomms10382

DOI: 10.1038/ncomms10382

PMC ID: 4735906

PubMed ID: 26790750

SO-VID: 62e294e0-59c9-4b53-ac9e-b47ccbd9632b

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Biochemical characterization of predicted Precambrian RuBisCO

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Journal of Biochemical and Clinical Genetics (JBCGenetics)

Most cited references 41

ProtTest: selection of best-fit models of protein evolution.

CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution.

Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

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