Mutations in the circadian cycle drive adaptive plasticity in cyanobacteria

• 成果类型: Article
• 署名作者: Mendana, Alfonso; Santos-Merino, Maria; Gutierrez-Lanza, Raquel; Dominguez-Quintero, Marina; Medina-Mendez, Juan Manuel; Gonzalez-Guerra, Ana; Campa, Victor; Baez, Miguel; Ducos-Galand, Magaly; Lopez-Igual, Rocio; Volke, Daniel C.; Gugger, Muriel; Nikel, Pablo I.; Mazel, Didier; de la Cruz, Fernando; Fernandez-Lopez, Raul
• 署名单位: Michigan State University; University of Sevilla; Consejo Superior de Investigaciones Cientificas (CSIC); CSIC - Instituto de Bioquimica Vegetal y Fotosintesis (IBVF); Consejo Superior de Investigaciones Cientificas (CSIC); Universidad de Cantabria; CSIC - Instituto de Biomedicina y Biotecnologia de Cantabria (IBBTEC); Universite Paris Cite; Pasteur Network; Centre National de la Recherche Scientifique (CNRS); Institut Pasteur Paris; CNRS - National Institute for Biology (INSB); Technical University of Denmark; Universite Paris Cite; Pasteur Network; Institut Pasteur Paris
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2506928122
• 发表日期: 2025-09-09
• 页码: e2506928122
• 关键词: Cyanobacteria; circadian rhythm; experimental evolution; gene-expression; laboratory evolution; biochemical-evidence; clock; TRANSFORMATION; oscillation; mechanism; rhythms; fitness; SYSTEM

摘要

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 CO2 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 aroKled 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 CO2 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.