Deep-branching evolutionary intermediates reveal structural origins of form I rubisco

Albert K Liu; Benjamin Kaeser; LinXing Chen; Jacob West-Roberts; Leah J Taylor-Kearney; Adi Lavy; Damian Günzing; Wen-Jun Li; Michal Hammel; Eva Nogales; Jillian F Banfield; Patrick M Shih

doi:10.1016/j.cub.2023.10.053

Deep-branching evolutionary intermediates reveal structural origins of form I rubisco

Curr Biol. 2023 Dec 18;33(24):5316-5325.e3. doi: 10.1016/j.cub.2023.10.053. Epub 2023 Nov 17.

Authors

Affiliations

¹ Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA; Biochemistry, Molecular, Cellular and Developmental Biology Graduate Group, University of California, Davis, Davis, CA 95616, USA.
² Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
³ Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA 94720, USA; Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA 94720, USA.
⁴ Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA 94720, USA.
⁵ Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA.
⁶ Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA 94720, USA.
⁷ Department of Physics, University of Duisburg-Essen, 47057 Duisburg, Germany.
⁸ State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, P.R. China; State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, P.R. China.
⁹ Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
¹⁰ Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; California Institute for Quantitative Biosciences (QB3), University of California, Berkeley, Berkeley, CA 94720, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA.
¹¹ Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA 94720, USA; School of Geography, Earth and Atmospheric Sciences, University of Melbourne, Melbourne, VIC 3053, Australia; Chan Zuckerberg Biohub, San Francisco, CA 94158, USA.
¹² Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA; Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: pmshih@berkeley.edu.

PMID: 37979578
DOI: 10.1016/j.cub.2023.10.053

Abstract

The enzyme rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyzes the majority of biological carbon fixation on Earth. Although the vast majority of rubiscos across the tree of life assemble as homo-oligomers, the globally predominant form I enzyme-found in plants, algae, and cyanobacteria-forms a unique hetero-oligomeric complex. The recent discovery of a homo-oligomeric sister group to form I rubisco (named form I') has filled a key gap in our understanding of the enigmatic origins of the form I clade. However, to elucidate the series of molecular events leading to the evolution of form I rubisco, we must examine more distantly related sibling clades to contextualize the molecular features distinguishing form I and form I' rubiscos. Here, we present a comparative structural study retracing the evolutionary history of rubisco that reveals a complex structural trajectory leading to the ultimate hetero-oligomerization of the form I clade. We structurally characterize the oligomeric states of deep-branching form Iα and I'' rubiscos recently discovered from metagenomes, which represent key evolutionary intermediates preceding the form I clade. We further solve the structure of form I'' rubisco, revealing the molecular determinants that likely primed the enzyme core for the transition from a homo-oligomer to a hetero-oligomer. Our findings yield new insight into the evolutionary trajectory underpinning the adoption and entrenchment of the prevalent assembly of form I rubisco, providing additional context when viewing the enzyme family through the broader lens of protein evolution.

Keywords: evolutionary biology; protein oligomerization; rubisco; structural biology.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Ribulose-Bisphosphate Carboxylase* / chemistry
Ribulose-Bisphosphate Carboxylase* / genetics
Ribulose-Bisphosphate Carboxylase* / metabolism

Substances

Ribulose-Bisphosphate Carboxylase

Abstract

Publication types

MeSH terms

Substances

Grants and funding