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Trajectories for the evolution of bacterial CO 2 -concentrating mechanisms

Trajectories for the evolution of bacterial CO 2 -concentrating mechanisms

Authors :
Avi I. Flamholz
Eli Dugan
Justin Panich
John J. Desmarais
Luke M. Oltrogge
Woodward W. Fischer
Steven W. Singer
David F. Savage
Source :
Proceedings of the National Academy of Sciences. 119
Publication Year :
2022
Publisher :
Proceedings of the National Academy of Sciences, 2022.

Abstract

Cyanobacteria rely on CO 2 -concentrating mechanisms (CCMs) to grow in today’s atmosphere (0.04% CO 2 ). 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 CO 2 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 CO 2 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 CO 2 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 CO 2 and HCO 3 − , as both are required to produce biomass. Our experiments and model delineated a viable trajectory for CCM evolution where decreasing atmospheric CO 2 induces an HCO 3 − 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.

Subjects

Subjects :
Multidisciplinary

Details

ISSN :
10916490 and 00278424
Volume :
119
Database :
OpenAIRE
Journal :
Proceedings of the National Academy of Sciences
Accession number :
edsair.doi...........b1c3d1a1cbaa56f58d0f8cba617ce2ae
Full Text :
https://doi.org/10.1073/pnas.2210539119