Long-Term m5C Methylome Dynamics Parallel Phenotypic Adaptation in the Cyanobacterium Trichodesmium

Area of Science:

• Microbiology and Evolutionary Biology
• Environmental Science and Climate Change

Background:

• Understanding short-term biological responses and their long-term evolutionary impacts is crucial for microbes facing global change.
• Epigenetic modifications, such as methylation, influence plastic responses and long-term adaptation.
• Limited research exists on long-term methylation dynamics during environmental adaptation in ecologically important, non-model microbes.

Purpose of the Study:

• To investigate long-term epigenetic (m5C methylome) modifications during phenotypic adaptation to elevated CO2 in a marine prokaryote.
• To examine the dynamics of methylation changes over a 7-year evolution experiment.
• To correlate methylation changes with adaptive traits like growth and N2 fixation.

Main Methods:

• Conducted a 7-year evolution experiment with the marine cyanobacterium Trichodesmium under high CO2 conditions (750 µatm).
• Analyzed m5C methylome modifications over time in response to CO2 selection.
• Measured growth rates and N2 fixation rates to assess phenotypic adaptation.

Main Results:

• Identified specific m5C methylated sites that rapidly responded to high CO2 and were maintained for 4.5 years.
• Observed a return of m5C methylation levels to ancestral states after 7 years of CO2 selection.
• Demonstrated sustained higher growth and N2 fixation rates in high-CO2 adapted lines, irrespective of CO2 concentration, supporting genetic assimilation.

Conclusions:

• Methylation dynamics play a role in the initial stages of adaptation to environmental change, with rapid responses and prolonged maintenance.
• Phenotypic adaptation, driven by genetic assimilation, can persist even after epigenetic marks return to ancestral levels.
• These findings offer critical evolutionary insights into microbial adaptation to global change, particularly concerning biogeochemical cycles.