How reduced excitonic coupling enhances light harvesting in the main photosynthetic antennae of diatoms

Tjaart P. J. Kruger, Pavel Maly, Maxime T. A. Alexandre, Tomas Mancal, Claudia Buechel, Rienk van Grondelle

Research output: Contribution to JournalArticleAcademic

Abstract

Strong excitonic interactions are a key design strategy in photosynthetic light harvesting, expanding the spectral cross-section for light absorption and creating considerably faster and more robust excitation energy transfer. These molecular excitons are a direct result of exceptionally densely packed pigments in photosynthetic proteins. The main light-harvesting complexes of diatoms, known as fucoxan-thin-chlorophyll proteins (FCPs), are an exception, displaying surprisingly weak excitonic coupling between their chlorophyll (Chl) a's, despite a high pigment density. Here, we show, using single-molecule spectroscopy, that the FCP complexes of Cyclotella meneghiniana switch frequently into stable, strongly emissive states shifted 4-10 nm toward the red. A few percent of isolated FCPa complexes and similar to 20% of isolated FCPb complexes, on average, were observed to populate these previously unobserved states, percentages that agree with the steady-state fluorescence spectra of FCP ensembles. Thus, the complexes use their enhanced sensitivity to static disorder to increase their light-harvesting capability in a number of ways. A disordered exciton model based on the structure of the main plant light-harvesting complex explains the red-shifted emission by strong localization of the excitation energy on a single Chl a pigment in the terminal emitter domain due to very specific pigment orientations. We suggest that the specific construction of FCP gives the complex a unique strategy to ensure that its light-harvesting function remains robust in the fluctuating protein environment despite limited excitonic interactions.
Original languageEnglish
Pages (from-to)E11063-E11071
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number52
DOIs
Publication statusPublished - 26 Dec 2017

Keywords

  • fucoxanthin-chlorophyll protein
  • light-harvesting complex
  • photosynthetic excitons
  • protein disorder
  • single-molecule spectroscopy

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