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Trajectories for the evolution of bacterial CO₂-concentrating mechanisms

Flamholz, Avi I. and Dugan, Eli and Panich, Justin and Desmarais, John J. and Oltrogge, Luke M. and Fischer, Woodward W. and Singer, Steven W. and Savage, David F. (2022) Trajectories for the evolution of bacterial CO₂-concentrating mechanisms. Proceedings of the National Academy of Sciences of the United States of America, 119 (49). Art. No. e2210539119. ISSN 0027-8424. PMCID PMC9894237. doi:10.1073/pnas.2210539119.

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Cyanobacteria rely on CO₂-concentrating mechanisms (CCMs) to grow in today’s atmosphere (0.04% CO₂). These complex physiological adaptations require ≈15 genes to produce two types of protein complexes: inorganic carbon (Ci) transporters and 100+ nm carboxysome compartments that encapsulate rubisco with a carbonic anhydrase (CA) enzyme. Mutations disrupting any of these genes prohibit growth in ambient air. If any plausible ancestral form—i.e., lacking a single gene—cannot grow, how did the CCM evolve? Here, we test the hypothesis that evolution of the bacterial CCM was “catalyzed” by historically high CO₂ levels that decreased over geologic time. Using an E. coli reconstitution of a bacterial CCM, we constructed strains lacking one or more CCM components and evaluated their growth across CO₂ concentrations. We expected these experiments to demonstrate the importance of the carboxysome. Instead, we found that partial CCMs expressing CA or Ci uptake genes grew better than controls in intermediate CO₂ levels (≈1%) and observed similar phenotypes in two autotrophic bacteria, Halothiobacillus neapolitanus and Cupriavidus necator. To understand how CA and Ci uptake improve growth, we model autotrophy as colimited by CO₂ and HCO₃⁻, as both are required to produce biomass. Our experiments and model delineated a viable trajectory for CCM evolution where decreasing atmospheric CO₂ induces an HCO₃⁻ deficiency that is alleviated by acquisition of CA or Ci uptake, thereby enabling the emergence of a modern CCM. This work underscores the importance of considering physiology and environmental context when studying the evolution of biological complexity.

Item Type:Article
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URLURL TypeDescription CentralArticle ItemDiscussion Paper InCaltech News
Flamholz, Avi I.0000-0002-9278-5479
Dugan, Eli0000-0003-2400-5511
Panich, Justin0000-0003-1283-4910
Desmarais, John J.0000-0002-7739-2079
Oltrogge, Luke M.0000-0001-5716-9980
Fischer, Woodward W.0000-0002-8836-3054
Singer, Steven W.0000-0002-4229-8314
Savage, David F.0000-0003-0042-2257
Alternate Title:Trajectories for the evolution of bacterial CO2-concentrating mechanisms
Additional Information:© 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY). We dedicate this paper to the memory of Danny Salah Tawfik (z”l), a luminary to the scientific community and a dear friend and mentor to A.I.F. Danny’s many studies of enzyme evolution taught us that evolutionary timescales are accessible in carefully designed lab-scale experiments and his active cultivation of relationships that transcend generational, professional, and cultural divides continues to inspire. We are also indebted to Arren Bar-Even (z”l) for formative conversations guiding this work. Many thanks to Darcy McRose, Elad Noor, and Renee Wang for extensive comments on the manuscript and to Cecilia Blikstad, Julia Borden, Vahe Galstyan, Josh Goldford, Ron Milo, Robert Nichols, Naiya Phillips, Noam Prywes, and Gabe Salmon for helpful input. This research was supported in part by an NSF Graduate Research Fellowship (to A.I.F), NSF Grant No. PHY-1748958, the Gordon and Betty Moore Foundation Grant No. 2919.02, and the Kavli Foundation (to A.I.F), Schwartz/Reisman Collaborative Science Program (to W.W.F.), the US Department of Energy (DE-SC00016240 to D.F.S.), and Royal Dutch Shell (Energy and Biosciences Institute project CW163755 to D.F.S. and S.W.S.). Author contributions. A.I.F., E.D., W.W.F., and D.F.S. designed research; A.I.F., E.D., J.P., J.J.D., and L.M.O. performed research; S.W.S. contributed new reagents/analytic tools; A.I.F., E.D., J.P., J.J.D., L.M.O., W.W.F., and D.F.S. analyzed data; and A.I.F. and E.D. wrote the paper. The authors declare no competing interest.
Group:Division of Geological and Planetary Sciences, Resnick Sustainability Institute
Funding AgencyGrant Number
NSF Graduate Research FellowshipUNSPECIFIED
Gordon and Betty Moore Foundation2919.02
Kavli FoundationUNSPECIFIED
Schwartz/Reisman Collaborative Science ProgramUNSPECIFIED
Department of Energy (DOE)DE-SC00016240
Royal Dutch ShellCW163755
Issue or Number:49
PubMed Central ID:PMC9894237
Record Number:CaltechAUTHORS:20230106-62570000.2
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:118752
Deposited By: George Porter
Deposited On:06 Jan 2023 22:41
Last Modified:27 Feb 2023 18:37

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