遺伝子工学が古代の進化の謎に迫る(Genetic Engineering Sheds Light on Ancient Evolutionary Questions)


2023-01-31 カリフォルニア工科大学(Caltech)



バクテリアのCO2濃縮機構の進化に伴う軌跡 Trajectories for the evolution of bacterial CO2-concentrating mechanisms

Avi I. Flamholz ,Eli Dugan,Justin Panich,John J. Desmarais,Luke M. Oltrogge,Woodward W. Fischer,Steven W. Singer,David F. Savage
Proceedings of the National Academy of Sciences  Published:December 1, 2022


The emergence of biological novelty is often coupled to the evolution of Earth’s chemical environment. Here, we studied how the evolution of a bacterial CO2-concentrating mechanism (CCM)—a complex, multicomponent system that enables modern CO2-fixing bacteria to grow robustly in environments with low CO2—depends on environmental CO2 levels. Using a “synthetic biological” approach to assay the growth of the present-day bacteria engineered to resemble ancient ones, we show that it is possible to explain the emergence of bacterial CCMs if atmospheric CO2 was once much higher than today, consistent with geochemical proxies. Taken together, our results delineated an unexpected “CO2-catalyzed” pathway for the evolution of bacterial CCMs, whose multiple emergence has been challenging to understand.


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.