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Using light for energy: examining the evolution of phototrophic metabolism through synthetic construction

Autumn Peterson, Carina Baskett, William C. Ratcliff, View ORCID ProfileAnthony Burnetti
doi: https://doi.org/10.1101/2022.12.06.519405
Autumn Peterson
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, US
2Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, US
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Carina Baskett
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, US
2Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, US
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William C. Ratcliff
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, US
2Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, US
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  • For correspondence: ratcliff@gatech.edu anthony.burnetti@biosci.gatech.edu
Anthony Burnetti
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, US
2Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, US
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  • ORCID record for Anthony Burnetti
  • For correspondence: ratcliff@gatech.edu anthony.burnetti@biosci.gatech.edu
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Abstract

The origin of phototrophy was pivotal in increasing the size and scale of the biosphere, as it allowed organisms to utilize light-driven energy transport to drive biological processes. Retinalophototrophy, one of two independently evolved phototrophic pathways, consists of a simple system of microbial rhodopsins which have spread broadly through the tree of life via horizontal gene transfer. Here, we sought to determine whether Saccharomyces cerevisiae, a heterotrophic fungus with no known evolutionary history of phototrophy, can function as a facultative artificial phototroph after acquiring a single rhodopsin gene. We transformed S. cerevisiae into a facultative phototroph by inserting a rhodopsin protein from Ustilago maydis into the yeast vacuole, allowing light to pump protons into the vacuolar compartment, a function typically driven by consuming ATP. We show that yeast with rhodopsins gain a selective advantage when grown under green light, growing more rapidly than their non-phototrophic ancestor or rhodopsin-bearing yeast cultured in the dark. These results underscore the remarkable ease with which rhodopsins may be horizontally transferred even in eukaryotes, providing novel biological function without first requiring evolutionary optimization.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Statistical analysis of results has been updated and improved. Small errors to methods and strains corrected. Discussion and results significantly edited for clarity.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 06, 2023.
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Using light for energy: examining the evolution of phototrophic metabolism through synthetic construction
Autumn Peterson, Carina Baskett, William C. Ratcliff, Anthony Burnetti
bioRxiv 2022.12.06.519405; doi: https://doi.org/10.1101/2022.12.06.519405
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Using light for energy: examining the evolution of phototrophic metabolism through synthetic construction
Autumn Peterson, Carina Baskett, William C. Ratcliff, Anthony Burnetti
bioRxiv 2022.12.06.519405; doi: https://doi.org/10.1101/2022.12.06.519405

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