Welcome to the new version of CaltechAUTHORS. Login is currently restricted to library staff. If you notice any issues, please email coda@library.caltech.edu
Published May 16, 2023 | Published + Supplemental Material
Journal Article Open

Carbon isotope fractionation by an ancestral rubisco suggests that biological proxies for CO₂ through geologic time should be reevaluated

Abstract

The history of Earth's carbon cycle reflects trends in atmospheric composition convolved with the evolution of photosynthesis. Fortunately, key parts of the carbon cycle have been recorded in the carbon isotope ratios of sedimentary rocks. The dominant model used to interpret this record as a proxy for ancient atmospheric CO₂ is based on carbon isotope fractionations of modern photoautotrophs, and longstanding questions remain about how their evolution might have impacted the record. Therefore, we measured both biomass (ε_p) and enzymatic (ε_(Rubisco) carbon isotope fractionations of a cyanobacterial strain (Synechococcus elongatus PCC 7942) solely expressing a putative ancestral Form 1B rubisco dating to ≫1 Ga. This strain, nicknamed ANC, grows in ambient pCO₂ and displays larger ε_p values than WT, despite having a much smaller ε_(Rubisco) (17.23 ± 0.61‰ vs. 25.18 ± 0.31‰, respectively). Surprisingly, ANC ε_p exceeded ANC ε_(Rubisco) in all conditions tested, contradicting prevailing models of cyanobacterial carbon isotope fractionation. Such models can be rectified by introducing additional isotopic fractionation associated with powered inorganic carbon uptake mechanisms present in Cyanobacteria, but this amendment hinders the ability to accurately estimate historical pCO₂ from geological data. Understanding the evolution of rubisco and the CO₂ concentrating mechanism is therefore critical for interpreting the carbon isotope record, and fluctuations in the record may reflect the evolving efficiency of carbon fixing metabolisms in addition to changes in atmospheric CO₂.

Additional Information

© 2023 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). We thank Newton Nguyen for valuable guidance in the MCMC model used to calculate doubling times from growth curve data. We thank Victoria Orphan and Alex Sessions for access to lab space and analytical instruments, as well as lab managers Stephanie A. Connon, Fenfang Wu, and Nami Kitchen for assistance. This research was supported by the David and Lucille Packard Foundation (12540178), Simons Foundation (554187), NASA Exobiology (00010652), and the Schwartz-Reisman Collaborative Science Program (12520057). R.Z.W. was supported by a NSF Graduate Research Fellowship. Work in the lab of D.F.S. was supported by the US Department of Energy (DE-SC00016240). Work in the lab of P.M.S. was supported by a Society in Science-Branco Weiss fellowship from ETH Zürich and a Packard Fellowship from the David Lucile Packard Foundation. We thank Danielle Jorgens and Reena Zalpuri at the University of California Berkeley Electron Microscope Laboratory for advice and assistance in electron microscopy sample preparation and data collection. Author contributionsR.Z.W., R.J.N., A.K.L., D.F.S., J.M.E., P.M.S., and W.W.F. designed research; R.Z.W., R.J.N., A.K.L., J.A., and D.M.B. performed research; R.Z.W., R.J.N., A.K.L., A.I.F., and J.A. analyzed data; D.F.S., J.M.E., P.M.S., and W.W.F. advised on project; and R.Z.W. and A.I.F. wrote the paper. Data, Materials, and Software Availability. All study data are included in the article and/or SI Appendix. The authors declare no competing interest.

Attached Files

Published - pnas.202300466.pdf

Supplemental Material - pnas.2300466120.sapp.pdf

Files

pnas.202300466.pdf
Files (7.6 MB)
Name Size Download all
md5:db5a7194e4420f26c11a0b25dca8bf4f
6.4 MB Preview Download
md5:150a5508bbf895908409ae0b5550a1d8
1.2 MB Preview Download

Additional details

Created:
August 22, 2023
Modified:
October 20, 2023