Title: Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer

Abstract

Photosynthetic species evolved to protect their light-harvesting apparatus from photoxidative damage driven by intracellular redox conditions or environmental conditions. The Fenna–Matthews–Olson (FMO) pigment–protein complex from green sulfur bacteria exhibits redox-dependent quenching behavior partially due to two internal cysteine residues. Here, we show evidence that a photosynthetic complex exploits the quantum mechanics of vibronic mixing to activate an oxidative photoprotective mechanism. We use two-dimensional electronic spectroscopy (2DES) to capture energy transfer dynamics in wild-type and cysteine-deficient FMO mutant proteins under both reducing and oxidizing conditions. Under reducing conditions, we find equal energy transfer through the exciton 4–1 and 4–2-1 pathways because the exciton 4–1 energy gap is vibronically coupled with a bacteriochlorophyll-a vibrational mode. Under oxidizing conditions, however, the resonance of the exciton 4–1 energy gap is detuned from the vibrational mode, causing excitons to preferentially steer through the indirect 4–2-1 pathway to increase the likelihood of exciton quenching. We use a Redfield model to show that the complex achieves this effect by tuning the site III energy via the redox state of its internal cysteine residues. Overall, this result shows how pigment–protein complexes exploit the quantum mechanics of vibronic coupling to steer energy transfer.

Authors:

Higgins, Jacob S.  ^[1];

• Search DOE PAGES for author "Higgins, Jacob S."
• Search DOE PAGES for ORCID "0000-0002-8496-4899"

Lloyd, Lawson T. ^[1]; Sohail, Sara H. ^[1]; Allodi, Marco A.  ^[1];

• Search DOE PAGES for author "Allodi, Marco A."
• Search DOE PAGES for ORCID "0000-0002-3289-1659"

Otto, John P. ^[1]; Saer, Rafael G. ^[2]; Wood, Ryan E. ^[1]; Massey, Sara C. ^[1]; Ting, Po-Chieh ^[1]; Blankenship, Robert E. ^[3]; Engel, Gregory S. ^[1]

---

+ Show Author Affiliations

1. Department of Chemistry, The University of Chicago, Chicago, IL 60637,, The Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL 60637,, The James Franck Institute, The University of Chicago, Chicago, IL 60637,
2. The Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130,, Department of Biology, Washington University in St. Louis, St. Louis, MO 63130,
3. The Photosynthetic Antenna Research Center, Washington University in St. Louis, St. Louis, MO 63130,, Department of Biology, Washington University in St. Louis, St. Louis, MO 63130,, Department of Chemistry, Washington University in St. Louis, St. Louis, MO 63130

Publication Date:

Tue Mar 09 00:00:00 EST 2021

Research Org.:

Washington Univ., St. Louis, MO (United States); Univ. of Chicago, IL (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Basic Energy Sciences (BES); US Air Force Office of Scientific Research (AFOSR); National Science Foundation (NSF)

OSTI Identifier:

1770009

Alternate Identifier(s):

OSTI ID: 1850697

Grant/Contract Number:  

SC 0001035; SC0001035; SC0020131; FA9550-18-1-0099; DMR-1420709

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 118 Journal Issue: 11; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics; quantum effects in biology; ultrafast spectroscopy; photosynthesis; excitonic energy transfer; vibronic coupling