Laboratory evolution of synthetic electron transport system variants reveals a larger metabolic respiratory system and its plasticity

Amitesh Anand (), Arjun Patel, Ke Chen, Connor A. Olson, Patrick V. Phaneuf, Cameron Lamoureux, Ying Hefner, Richard Szubin, Adam M. Feist and Bernhard O. Palsson ()
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Amitesh Anand: University of California, San Diego
Arjun Patel: University of California, San Diego
Ke Chen: University of California, San Diego
Connor A. Olson: University of California, San Diego
Patrick V. Phaneuf: University of California, San Diego
Cameron Lamoureux: University of California, San Diego
Ying Hefner: University of California, San Diego
Richard Szubin: University of California, San Diego
Adam M. Feist: University of California, San Diego
Bernhard O. Palsson: University of California, San Diego

Nature Communications, 2022, vol. 13, issue 1, 1-9

Abstract: Abstract The bacterial respiratory electron transport system (ETS) is branched to allow condition-specific modulation of energy metabolism. There is a detailed understanding of the structural and biochemical features of respiratory enzymes; however, a holistic examination of the system and its plasticity is lacking. Here we generate four strains of Escherichia coli harboring unbranched ETS that pump 1, 2, 3, or 4 proton(s) per electron and characterized them using a combination of synergistic methods (adaptive laboratory evolution, multi-omic analyses, and computation of proteome allocation). We report that: (a) all four ETS variants evolve to a similar optimized growth rate, and (b) the laboratory evolutions generate specific rewiring of major energy-generating pathways, coupled to the ETS, to optimize ATP production capability. We thus define an Aero-Type System (ATS), which is a generalization of the aerobic bioenergetics and is a metabolic systems biology description of respiration and its inherent plasticity.

Date: 2022
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DOI: 10.1038/s41467-022-30877-5

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