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Condensed Matter Physics

Contrasting packing modes for tubular assemblies in chlorosomes

Profile image of Yuliya MiloslavinaYuliya Miloslavina

2024, Contrasting packing modes for tubular assemblies in chlorosomes

https://doi.org/10.1007/S11120-024-01089-3
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Abstract

The largest light-harvesting antenna in nature, the chlorosome, is a heterogeneous helical BChl self-assembly that has evolved in green bacteria to harvest light for performing photosynthesis in low-light environments. Guided by NMR chemical shifts and distance constraints for Chlorobaculum tepidum wild-type chlorosomes, the two contrasting packing modes for syn-anti parallel stacks of BChl c to form polar 2D arrays, with dipole moments adding up, are explored. Layered assemblies were optimized using local orbital density functional and plane wave pseudopotential methods. The packing mode with the low- est energy contains syn-anti and anti-syn H-bonding between stacks. It can accommodate R and S epimers, and side chain variability. For this packing, a match with the available EM data on the subunit axial repeat and optical data is obtained with multiple concentric cylinders for a rolling vector with the stacks running at an angle of 21° to the cylinder axis and with the BChl dipole moments running at an angle ß ∼ 55° to the tube axis, in accordance with optical data. A packing mode involving alternating syn and anti parallel stacks that is at variance with EM appears higher in energy. A weak cross-peak at -6 ppm in the MAS NMR with 50 kHz spinning, assigned to C-181, matches the shift of antiparallel dimers, which possibly reflects a minor impurity-type fraction in the self-assembled BChl c.

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  61. Author Contributions
  62. Yuliya A. Miloslavina: writing, figures, tables, references, MAS NMR measurements and data analysis in Leiden and in Göttingen, construction and analysis of repeat units and packing modes in the Materials Studio, theoretical calculations and analysis, EM data modeling, construction of the tubes in Crystal Maker. Brijith Thomas: support with Castep calculations Michael Reus: sample preparation Karthick Babu Sai Sankar Gupta: MAS NMR measurements setup help in Leiden Gert T. Oostergetel: provided original EM spectra and explain how to do EM modeling. Loren Andreas: supervised MAS NMR measurements in Göttingen, writing-editing
  63. Alfred R. Holzwarth: discussions about optical spectroscopy, modeling was first started by modifications of Alfred's model Huub J.M. de Groot: coordination of the project, writing, editing

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A Refined Model of the Chlorosomal Antennae of the Green Bacterium <i>Chlorobium tepidum</i> from Proton Chemical Shift Constraints Obtained with High-Field 2-D and 3-D MAS NMR Dipolar Correlation Spectroscopy
Alfred Holzwarth

Biochemistry, 2001

Heteronuclear 2-D and 3-D magic-angle spinning NMR dipolar correlation spectroscopy was applied to determine solid-state 1 H shifts for aggregated bacteriochlorophyll c (BChl c) in uniformly 13 Cenriched light harvesting chlorosomes of the green photosynthetic bacterium Chlorobium tepidum. A complete assignment of 29 different observable resonances of the 61 protons of the aggregated BChl c in the intact chlorosomes is obtained. Aggregation shifts relative to monomeric BChl c in solution are detected for protons attached to rings I, II, and III/V and to their side chains. The 2 1-H 3 , 3 2-H 3 , and 3 1-H resonances are shifted upfield by-2.2,-1, and-3.3 ppm, respectively, relative to monomeric BChl c in solution. Although the resonances are inhomogeneously broadened and reveal considerable global structural heterogeneity, the 5-CH and the 7-Me responses are doubled, which provides evidence for the existence of at least two relatively well-defined structurally different arrangements. Ab initio quantum chemical modeling studies were performed to refine a model for the self-assembled BChl c with two different types of BChl stacks. The BChl in the stacks can adopt either anti-or syn-configuration of the coordinative bond, where anti and syn designate the relative orientation of the Mg-OH bond relative to the direction of the 17-17 1 bond. The analogy between aggregation shifts for BChl c in the chlorosome and for selfassembled chlorophyll a/H 2 O is explored, and a bilayer model for the tubular supra-structure of sheets of BChl c is proposed, from a homology modeling approach.

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Structural Variations in Chlorosomes from Wild-Type and a bchQR Mutant of Chlorobaculum tepidum Revealed by Single-Molecule Spectroscopy
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The journal of physical chemistry. B, 2018

Green sulfur bacteria can grow photosynthetically by absorbing only a few photons per bacteriochlorophyll molecule per day. They contain chlorosomes, perhaps the most efficient light-harvesting antenna system found in photosynthetic organisms. Chlorosomes contain supramolecular structures comprising hundreds of thousands of bacteriochlorophyll molecules, which are properly positioned with respect to one another solely by self-assembly and not by using a protein scaffold as a template for directing the mutual arrangement of the monomers. These two features-high efficiency and self-assembly-have attracted considerable attention for developing light-harvesting systems for artificial photosynthesis. However, reflecting the heterogeneity of the natural system, detailed structural information at atomic resolution of the molecular aggregates is not yet available. Here, we compare the results for chlorosomes from the wild type and two mutants of Chlorobaculum tepidum obtained by polarizatio...

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In situ high-resolution structure of the baseplate antenna complex in Chlorobaculum tepidum
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Nature Communications, 2016

Photosynthetic antenna systems enable organisms harvesting light and transfer the energy to the photosynthetic reaction centre, where the conversion to chemical energy takes place. One of the most complex antenna systems, the chlorosome, found in the photosynthetic green sulfur bacterium Chlorobaculum (Cba.) tepidum contains a baseplate, which is a scaffolding superstructure , formed by the protein CsmA and bacteriochlorophyll a. Here we present the first high-resolution structure of the CsmA baseplate using intact fully functional, light-harvesting organelles from Cba. tepidum, following a hybrid approach combining five complementary methods: solid-state NMR spectroscopy, cryo-electron microscopy, isotropic and anisotropic circular dichroism and linear dichroism. The structure calculation was facilitated through development of new software, GASyCS for efficient geometry optimization of highly symmetric oligomeric structures. We show that the baseplate is composed of rods of repeated dimers of the strongly amphipathic CsmA with pigments sandwiched within the dimer at the hydrophobic side of the helix.

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wPMLG-5 Spectroscopy of Self-Aggregated BChlein Natural Chlorosomes ofChlorobaculum Limnaeum
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CP-MAS 13C-NMR dipolar correlation spectroscopy of 13C-enriched chlorosomes and isolated bacteriochlorophyll c aggregates of Chlorobium tepidum: the self-organization of pigments is the main structural feature of chlorosomes
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Magic angle spinning (MAS) NMR dipolar correlation spectroscopy was applied for the first time to a biologically intact system, the light-harvesting chlorosomes of the green photosynthetic bacterium Chlorobium tepidum. The MAS spectra provide evidence that the self-organization of many thousands of bacteriochlorophyll c (BChl c ) molecules is the predominant structural feature of the chlorosome. 13C-Enriched chlorosomes were prepared from nonuniformly labeled cultures grown with NaH13C03 as the main carbon source and from a uniformly 13C-labeled culture grown with NaH13C03 as the sole carbon source. For the nonuniformly labeled samples, the positions of the chlorin macrocycle originating from C-4 and C-5 of 5-aminolevulinic acid contained '95% 13C while the remaining positions, which could have originated also from unlabeled acetate, were labeled to -60% with I3C. The 1-D and 2-D MAS data of the labeled chlorosomes, when compared with data on the isolated labeled BChl c aggregated in n-hexane, show that the major component of the MAS signals in the chlorosomes is from BChl c, and only minor signal contributions arise from lipids and proteins. The 13C MAS signals of the BChl c aggregates were fully assigned by MAS 2-D dipolar correlation spectroscopy, using data on monomeric BChl c in CDC13ICD30D as reference. The 2l-, 3-, 3*-, 5, 12l-, 13-, and 13l-carbons are shifted by 2.5 ppm or more upfield with respect to the solution data. The 2-D response of the BChl c in intact chlorosomes is virtually indistinguishable from that of the in vitro aggregate with respect to chemical shifts, line widths, and relative intensities of the cross-peaks. This corroborates previous evidence that self-assembly of BChl c, without the interaction with protein, provides the structural basis for the BChl c organization in vivo.

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Related topics

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