Marine cyanobacteria tune energy transfer efficiency in their light-harvesting antennae by modifying pigment coupling

FEBS J. 2021 Feb;288(3):980-994. doi: 10.1111/febs.15371. Epub 2020 Jun 4.

Abstract

Photosynthetic light harvesting is the first step in harnessing sunlight toward biological productivity. To operate efficiently under a broad and dynamic range of environmental conditions, organisms must tune the harvesting process according to the available irradiance. The marine cyanobacteria Synechococcus WH8102 species is well-adapted to vertical mixing of the water column. By studying its responses to different light regimes, we identify a new photo-acclimation strategy. Under low light, the phycobilisome (PBS) is bigger, with extended rods, increasing the absorption cross-section. In contrast to what was reported in vascular plants and predicted by Forster resonance energy transfer (FRET) calculations, these longer rods transfer energy faster than in the phycobilisomes of cells acclimated to a higher light intensity. Comparison of cultures grown under different blue light intensities, using fluorescence lifetime and emission spectra dependence on temperature at the range of 4-200 K in vivo, indicates that the improved transfer arises from enhanced energetic coupling between the antenna rods' pigments. We suggest two physical models according to which the enhanced coupling strength results either from additional coupled pathways formed by rearranging rod packing or from the coupling becoming non-classical. In both cases, the energy transfer would be more efficient than standard one-dimensional FRET process. These findings suggest that coupling control can be a major factor in photosynthetic antenna acclimation to different light conditions.

Keywords: energy transfer; photosynthesis; phycobilisome; quantum biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chlorophyll / metabolism
  • Dose-Response Relationship, Radiation
  • Light
  • Light-Harvesting Protein Complexes / metabolism*
  • Microscopy, Electron, Transmission
  • Photosynthesis / physiology*
  • Photosynthesis / radiation effects
  • Phycobilisomes / metabolism*
  • Phycobilisomes / radiation effects
  • Phycobilisomes / ultrastructure
  • Seawater / microbiology
  • Spectrometry, Fluorescence
  • Synechococcus / metabolism*
  • Synechococcus / radiation effects
  • Synechococcus / ultrastructure
  • Temperature

Substances

  • Light-Harvesting Protein Complexes
  • Phycobilisomes
  • Chlorophyll