A systematic exploration of bacterial form I rubisco maximal carboxylation rates

Benoit de Pins; Lior Greenspoon; Yinon M. Bar-On; Melina Shamshoum; Roee Ben-Nissan; Eliya Milshtein; Dan Davidi; Itai Sharon; Oliver Mueller-Cajar; Elad Noor; Ron Milo

doi:10.1038/s44318-024-00119-z

A systematic exploration of bacterial form I rubisco maximal carboxylation rates

Benoit de Pins, Lior Greenspoon, Yinon M. Bar-On, Melina Shamshoum, Roee Ben-Nissan, Eliya Milshtein, Dan Davidi, Itai Sharon, Oliver Mueller-Cajar, Elad Noor, Ron Milo^*

^*Corresponding author for this work

Department of Plant and Environmental Sciences

Research output: Contribution to journal › Article › peer-review

1 Citation (Scopus)

Abstract

Autotrophy is the basis for complex life on Earth. Central to this process is rubisco—the enzyme that catalyzes almost all carbon fixation on the planet. Yet, with only a small fraction of rubisco diversity kinetically characterized so far, the underlying biological factors driving the evolution of fast rubiscos in nature remain unclear. We conducted a high-throughput kinetic characterization of over 100 bacterial form I rubiscos, the most ubiquitous group of rubisco sequences in nature, to uncover the determinants of rubisco’s carboxylation velocity. We show that the presence of a carboxysome CO₂ concentrating mechanism correlates with faster rubiscos with a median fivefold higher rate. In contrast to prior studies, we find that rubiscos originating from α-cyanobacteria exhibit the highest carboxylation rates among form I enzymes (≈10 s⁻¹ median versus <7 s⁻¹ in other groups). Our study systematically reveals biological and environmental properties associated with kinetic variation across rubiscos from nature.

Original language	English
Pages (from-to)	3072-3083
Number of pages	12
Journal	EMBO Journal
Volume	43
Issue number	14
DOIs	https://doi.org/10.1038/s44318-024-00119-z
Publication status	Published Online - 28 May 2024

Funding

The authors thank Yoav Peleg, Ron Sender, Noam Prywes, Brian Ross, Dina Listov, Ralf Steuer, Avi Flamholz and David Savage for important conversations and productive feedback on this manuscript. The authors thank Michelle Gehring for additional information about unpublished data from their laboratory. This research was supported by the Mary and Tom Beck Canadian Center for Alternative Energy Research, Miel de Botton, the Schwartz Reisman Collaborative Science Program, and the Charles and Louise Gartner Professorial Chair. Publisher Copyright: © The Author(s) 2024.

All Science Journal Classification (ASJC) codes

General Neuroscience
Molecular Biology
General Biochemistry,Genetics and Molecular Biology
General Immunology and Microbiology

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title = "A systematic exploration of bacterial form I rubisco maximal carboxylation rates",

abstract = "Autotrophy is the basis for complex life on Earth. Central to this process is rubisco—the enzyme that catalyzes almost all carbon fixation on the planet. Yet, with only a small fraction of rubisco diversity kinetically characterized so far, the underlying biological factors driving the evolution of fast rubiscos in nature remain unclear. We conducted a high-throughput kinetic characterization of over 100 bacterial form I rubiscos, the most ubiquitous group of rubisco sequences in nature, to uncover the determinants of rubisco{\textquoteright}s carboxylation velocity. We show that the presence of a carboxysome CO2 concentrating mechanism correlates with faster rubiscos with a median fivefold higher rate. In contrast to prior studies, we find that rubiscos originating from α-cyanobacteria exhibit the highest carboxylation rates among form I enzymes (≈10 s−1 median versus <7 s−1 in other groups). Our study systematically reveals biological and environmental properties associated with kinetic variation across rubiscos from nature.",

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AU - Shamshoum, Melina

AU - Ben-Nissan, Roee

AU - Milshtein, Eliya

AU - Davidi, Dan

AU - Sharon, Itai

AU - Mueller-Cajar, Oliver

AU - Noor, Elad

AU - Milo, Ron

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AB - Autotrophy is the basis for complex life on Earth. Central to this process is rubisco—the enzyme that catalyzes almost all carbon fixation on the planet. Yet, with only a small fraction of rubisco diversity kinetically characterized so far, the underlying biological factors driving the evolution of fast rubiscos in nature remain unclear. We conducted a high-throughput kinetic characterization of over 100 bacterial form I rubiscos, the most ubiquitous group of rubisco sequences in nature, to uncover the determinants of rubisco’s carboxylation velocity. We show that the presence of a carboxysome CO2 concentrating mechanism correlates with faster rubiscos with a median fivefold higher rate. In contrast to prior studies, we find that rubiscos originating from α-cyanobacteria exhibit the highest carboxylation rates among form I enzymes (≈10 s−1 median versus <7 s−1 in other groups). Our study systematically reveals biological and environmental properties associated with kinetic variation across rubiscos from nature.

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A systematic exploration of bacterial form I rubisco maximal carboxylation rates

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