Conformational Dynamics of Bacteriochlorophyll c in Chlorosomes from the bchQ Mutant of Chlorobaculum tepidum

Dsouza, Lolita; Gupta, Karthick Babu Sai Sankar; Li, Xinmeng; Erić, Vesna; Luo, Yusen; Huijser, Annemarie; Jansen, Thomas L. C.; Buda, Francesco; Holzwarth, Alfred R.; Bryant, Donald A.; Gurinov, Andrei; Sevink, G. J. Agur; de Groot, Huub J. M.

doi:10.1021/acs.jpcb.4c04731

Title: Conformational Dynamics of Bacteriochlorophyll c in Chlorosomes from the bchQ Mutant of Chlorobaculum tepidum

Journal Article · 16 February 2025 · Journal of Physical Chemistry. B

DOI: https://doi.org/10.1021/acs.jpcb.4c04731 · OSTI ID:2519271

Dsouza, Lolita ^[1];

^[1];

^[2]; Erić, Vesna ^[3]; Luo, Yusen ^[4]; Huijser, Annemarie ^[4];

^[3]; Buda, Francesco ^[1];

^[5]; Bryant, Donald A. ^[6]; Gurinov, Andrei ^[7]; Sevink, G. J. Agur ^[1];

^[1]

Leiden University (The Netherlands)
Leiden University (The Netherlands); University of Oslo (Norway)
University of Groningen (The Netherlands)
University of Twente (The Netherlands)
Max Planck Institute for Chemical Energy Conversion, Mülheim an der Ruhr (Germany)
The Pennsylvania State University, University Park, PA (United States)
Utrecht University (The Netherlands)

In contrast to the common viewpoint that bacteriochlorophyll (BChl) motion is largely absent within the chlorosome assembly, physics-based modeling points to a crucial role of the nanoscale librational motion of the macrocycle for the transfer of excitons. To elucidate this motion experimentally, compositional uniformity and high sensitivity are required. We focused on uniformly ¹³C labeled chlorosome preparations from the bchQ mutant Chlorobaculum tepidum with significantly enhanced structural homogeneity. The librational motion is characterized using Rotational Echo DOuble Resonance (REDOR), and in addition, the impact of temperature on specific functionalities within BChl molecules is studied with 1-dimensional and 2-dimensional dipolar and scalar-based MAS NMR measurements. Results show the gradual freezing of the tails and side chains of the BChls with decreasing temperature. However, the librational motion analyzed by measuring the 5C–H dipolar coupling strength obtained from REDOR data sets persists at different temperatures. REDOR simulations show a close match to the experimental dephasing frequency of oscillation for a dipolar coupling strength of 17.5 ± 0.5 kHz which is considerably less than the dipolar coupling strength of 22.7 kHz in the rigid limit. Following a two-site jump model, we arrive at an estimate for BChl libration sampling at an angle of θ = 48 ± 4°, corroborating that the macrocycle indeed experiences significant librational motion on a time scale that is short compared to the NMR measurement time. This finding is in full quantitative support of the dominant rotational motion exhibited by the BChl macrocycle estimated from early MD simulations.

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Research Organization:: Leiden University (The Netherlands)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: FG02-94ER20137

OSTI ID:: 2519271

Journal Information:: Journal of Physical Chemistry. B, Journal Name: Journal of Physical Chemistry. B Journal Issue: 8 Vol. 129; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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