Mutations in the circadian cycle drive adaptive plasticity in cyanobacteria
Abstract
Circadian clocks allow organisms to anticipate daily fluctuations in light and temperature, but how this anticipatory role promotes adaptation to different environments remains poorly understood. Here, we subjected the cyanobacterium Synechococcus elongatus PCC 7942 to a long-term evolution experiment under high light, high temperature, and elevated CO 2 levels. After 1,200 generations, we obtained a strain exhibiting a 600% increase in growth rate. Whole-genome sequencing revealed three mutations fixed in the evolved population, two of which were sufficient to recapitulate the fast-growing phenotype in the wild type. A mutation in the promoter of the shikimate kinase aroK led to its overexpression, while a mutation in the central circadian regulator sasA disrupted both the phase and amplitude of the circadian rhythm. Changes in circadian control led to widespread perturbations in the transcriptome and metabolome. These included major shifts in the Calvin–Benson–Bassham cycle and glycogen storage dynamics. While these changes increased fitness under the experimental conditions, they caused maladaptation when light or CO 2 levels were altered, revealing a trade-off between fitness and environmental flexibility. Our results demonstrate that mutations in circadian control can drive fast adaptation by modulating central metabolism, underscoring the circadian cycle as a cornerstone of cellular plasticity. Thus, targeting the circadian cycle could be key to engineering cyanobacterial strains optimized for carbon fixation and biomass production.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (16)
Alfonso Mendaña
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
María Santos-Merino
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Raquel Gutiérrez-Lanza
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Marina Domínguez-Quintero
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Juan Manuel Medina-Méndez
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Ana González-Guerra
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Víctor Campa
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Miguel Baez
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Magaly Ducos-Galand
Institut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien
Rocío López-Igual
Institut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien
Daniel C. Volke
The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark
Muriel Gugger
Institut Pasteur, Université Paris Cité, Collection of Cyanobacteria
Pablo I. Nikel
The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark
Didier Mazel
Institut Pasteur, Université Paris Cité, CNRS UMR3525, Unité Plasticité du Génome Bactérien
Fernando de la Cruz
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas
Raúl Fernández-López
Instituto de Biomedicina y Biotecnología de Cantabria, Universidad de Cantabria—Consejo Superior de Investigaciones Científicas