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 July 8, 2022 | Supplemental Material + Submitted
Report Open

Trajectories for the evolution of bacterial CO₂-concentrating mechanisms

Abstract

Cyanobacteria rely on CO₂ concentrating mechanisms (CCMs) that depend on ≈15 genes to produce two protein complexes: an inorganic carbon (Ci) transporter and a 100+ nm carboxysome compartment that encapsulates rubisco with a carbonic anhydrase (CA) enzyme. Mutations disrupting CCM components prohibit growth in today's atmosphere (0.04% CO₂), indicating that CCMs evolved to cope with declining environmental CO₂. Indeed, geochemical data and models indicate that atmospheric CO₂ has been generally decreasing from high concentrations over the last ≈3.5 billion years. We used a synthetic reconstitution of a bacterial CCM in E. coli to study the co-evolution of CCMs with atmospheric CO₂. We constructed strains expressing putative ancestors of modern CCMs — strains lacking one or more CCM components — and evaluated their growth in a variety of CO₂ concentrations. Partial forms expressing CA or Ci uptake genes grew better than controls in intermediate CO₂ levels (≈1%); we observed similar phenotypes in genetic studies of two autotrophic bacteria, H. neapolitanus and C. necator. To explain how partial CCMs improve growth, we advance a model of co-limitation of autotrophic growth by CO₂ and HCO₃⁻, as both are required to produce biomass. Our model and results delineated a viable trajectory for bacterial CCM evolution where decreasing atmospheric CO₂ induces an HCO₃⁻ deficiency that is alleviated by acquisition of CAs or Ci uptake genes, 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.

Additional Information

The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. 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 AIF. 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), 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.S.). Competing Interest Statement. D.F.S. is a co-founder of Scribe Therapeutics and a scientific advisory board member of Scribe Therapeutics and Mammoth Biosciences. These companies were not involved in this work in any way.

Attached Files

Submitted - 2022.06.21.497102v2.full.pdf

Supplemental Material - media-1.pdf

Supplemental Material - media-2.xlsx

Files

media-1.pdf
Files (4.4 MB)
Name Size Download all
md5:4434b0e1063637c3c466758d546f9465
2.7 MB Preview Download
md5:6e77d7b6f78837505f3c2a4e4ee5bd99
1.7 MB Preview Download
md5:2ea39a8d1a5956cf8fd87a15a5d3d235
46.0 kB Download

Additional details

Created:
August 20, 2023
Modified:
October 23, 2023