Title: Photoactivation mechanism of a carotenoid-based photoreceptor

Abstract

Photoprotection is essential for efficient photosynthesis. Cyanobacteria have evolved a unique photoprotective mechanism mediated by a water-soluble carotenoid-based photoreceptor known as orange carotenoid protein (OCP). OCP undergoes large conformational changes in response to intense blue light, and the photoactivated OCP facilitates dissipation of excess energy via direct interaction with allophycocyanins at the phycobilisome core. However, the structural events leading up to the OCP photoactivation remain elusive at the molecular level. Here we present direct observations of light-induced structural changes in OCP captured by dynamic crystallography. Difference electron densities between the dark and illuminated states reveal widespread and concerted atomic motions that lead to altered protein–pigment interactions, displacement of secondary structures, and domain separation. Based on these crystallographic observations together with site-directed mutagenesis, we propose a molecular mechanism for OCP light perception, in which the photochemical property of a conjugated carbonyl group is exploited. We hypothesize that the OCP photoactivation starts with keto–enol tautomerization of the essential 4-keto group in the carotenoid, which disrupts the strong hydrogen bonds between the bent chromophore and the protein moiety. Subsequent structural changes trapped in the crystal lattice offer a high-resolution glimpse of the initial molecular events as OCP begins to transition from the orange-absorbingmore » state to the active red-absorbing state.« less

Authors:

Bandara, Sepalika ^[1]; Ren, Zhong ^[1]; Lu, Lu ^[2]; Zeng, Xiaoli ^[1]; Shin, Heewhan ^[1]; Zhao, Kai-Hong ^[2]; Yang, Xiaojing ^[1]

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+ Show Author Affiliations

1. Univ. of Illinois, Chicago, IL (United States)
2. Huazhong Agricultural Univ., Wuhan (China). State Key Lab. of Agricultural Microbiology

Publication Date:

Tue May 30 00:00:00 EDT 2017

Research Org.:

Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:

National Institutes of Health (NIH); USDOE

OSTI Identifier:

1438873

Grant/Contract Number:  

AC02-06CH11357

Resource Type:

Accepted Manuscript

Journal Name:

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

Additional Journal Information:

Journal Volume: 114; Journal Issue: 24; Journal ID: ISSN 0027-8424

Publisher:

National Academy of Sciences

Country of Publication:

United States

Language:

ENGLISH

Subject:

59 BASIC BIOLOGICAL SCIENCES; photoreceptor; light perception; photoprotection; carotenoid-binding protein; dynamic crystallography