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Elucidating chirality transfer in liquid crystals of viruses

Nature Materials (2024)Cite this article

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Abstract

Chirality is ubiquitous in nature across all length scales, with major implications spanning fields from biology, chemistry and physics to materials science. How chirality propagates from nanoscale building blocks to meso- and macroscopic helical structures remains an open issue. Here, working with a canonical system of filamentous viruses, we demonstrate that their self-assembly into chiral liquid crystal phases quantitatively results from the interplay between two main mechanisms of chirality transfer: electrostatic interactions from the helical charge patterns on the virus surface, and fluctuation-based helical deformations leading to viral backbone helicity. Our experimental and theoretical approach provides a comprehensive framework for deciphering how chirality is hierarchically and quantitatively propagated across spatial scales. Our work highlights the ways in which supramolecular helicity may arise from subtle chiral contributions of opposite handedness that act either cooperatively or competitively, thus accounting for the multiplicity of chiral behaviours observed for nearly identical molecular systems.

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Fig. 1: Structural chirality of filamentous viruses at various hierarchical scales, ranging from the asymmetry of Cα atoms of the amino acids of the major coat proteins p8, to the α-helical structure of these proteins and their helical arrangement on the virion surface.
Fig. 2: Atomistic representation of the semi-flexible M13 and stiff Y21M virions and pH dependence of their charge distribution calculated using Adaptive Poisson-Boltzmann Solver (APBS).
Fig. 3: Cholesteric to nematic crossover by decreasing charge fully accounted for by the electrostatic model in Y21M virus suspensions.
Fig. 4: Cholesteric ordering in sterically stabilized semi-flexible viruses and suprahelix model.
Fig. 5: Master curve of the cholesteric pitch P for semi-flexible viruses accounted for by the suprahelix model.

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Data availability

All the data supporting the findings of this study are included in the article and its Supplementary Information file. Source data are provided with this paper.

Code availability

The numerical codes used for molecular structure preparation and density functional calculations can be accessed via GitHub at https://github.com/mtortora/chiralDFT.

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Acknowledgements

We thank H. Anop for the data of Extended Data Fig. 5 and A. Pope for help with Y21M sample preparation. We also acknowledge access to computing resources provided by the Pôle Scientifique de Modélisation Numérique of the ENS de Lyon.

Author information

Author notes

  1. Maxime M. C. Tortora

    Present address: Department of Quantitative and Computational Biology, University of Southern California, Los Angeles, CA, USA

Authors and Affiliations

  1. Centre de Recherche Paul Pascal (CRPP, UMR 5031), Univ. Bordeaux, CNRS, Pessac, France

    Eric Grelet

  2. Laboratoire de Biologie et Modélisation de la Cellule (LBMC, UMR 5239, Inserm 1293), Univ. Claude Bernard Lyon 1, ENS de Lyon, CNRS, Lyon, France

    Maxime M. C. Tortora

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Contributions

E.G. conceptualized the study, instigated the project, performed the experiments and wrote the paper with contributions from M.M.C.T.; M.M.C.T. implemented the numerical methods and carried out the calculations. Both authors developed the models, analysed the results, wrote the Supplementary Information and revised and edited the paper. Correspondence and requests for materials and data should be addressed to E.G. Queries regarding numerical details and computational data should be directed to M.M.C.T.

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Correspondence to Eric Grelet or Maxime M. C. Tortora.

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Nature Materials thanks Torsten Hegmann, Jan Lagerwall and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Opposite handedness of the cholesteric helix for M13 and Y21M strains.

Determined by fluorescence microscopy in (a) PEGylated M13 suspension (pH 8.2, IS=110 mM) and (b) Y21M suspension (pH 8.2, IS=60 mM). A small fraction (1:105) of viruses are labelled with red or green fluorescent tags to indicate the orientation of the nematic director in each focal plane, as shown by arrows. Their rotation through the sample thickness Z reveals the handedness of the cholesteric helicity, which is found to be left-handed for M13 and M13-PEG and right-handed for Y21M strain. The periodicity of the cholesteric helix, or cholesteric pitch P, is also indicated for both virion strains, and its value is positive (negative) for right (left) handedness. Each image has a size of 50 μm x 50 μm.

Extended Data Fig. 2 Electrostatic dependence of the cholesteric pitch, P.

Measurements for Y21M (open symbols) and M13 (full symbols) for different ionic strengths IS at fixed pH 8 as a function of the respective virus concentration. The data of Y21M phages at pH 8 and IS = 110 mM are taken from Ref. 37. For both virions, ∣P∣ increases with increasing ionic strength, that is, with increasing the screening of electrostatic interactions. For each data set, the binodal concentrations of the isotropic-to-cholesteric transition corresponding to the stability limit of the isotropic phase, Ciso, are shown by a dotted line whose colour corresponds to the associated colour of the symbols. For error bar determination, see Methods.

Source data

Extended Data Fig. 3 Inversion of the twist handedness between right-handed screws of varying thread angle, φ.

The helical twist resulting from the close packing of two right-handed (that is 0 < φ < + 90o) screws leads (a) to a right-handed twist (and therefore a right-handed cholesteric pitch P > 0) of angle 2φ > 0 when φ < 45o and (b) to a left-handed twist (P < 0) of angle − (180o − 2φ) < 0 for φ > 45o.

Extended Data Fig. 4 Phase behaviour of semi-flexible M13 (a)-(c) and PEGylated M13-PEG (d)-(f) virus suspensions at pH close to the isoelectric point, pIE.

(a) and (d): Schematic representation of the filamentous viruses, whose colloidal stability stems from either (a) electrostatic or (d) steric repulsion. (b) and (e): Macroscopic observation under white light of the virion suspensions: while aggregates are observed in raw M13 virus dispersions at pH ≃ pIE, the colloidal stability is preserved in the M13-PEG system. Scale bar: 2 mm. (c) and (f): Polarized optical microscopy images displaying a nematic-like birefingent texture with fibrillar moieties for raw M13 viruses (c) and the characteristic fingerprint texture of the cholesteric phase for PEGylated particles (f). Scale bar: 200 μm.

Extended Data Fig. 5 Helical supramolecular structures.

They are formed by condensation of filamentous viruses initially organized in a cholesteric mesophase, induced by depletion interaction using poly(ethylene glycol) polymer (molecular weight Mw=2000 g mol-1; Sigma-Aldrich) and observed by (a) polarizing and (b) differential interference contrast (DIC) microscopy. Scale bar: 2 μm.

Supplementary information

Supplementary Information

Supplementary Sections I–VII and Figs. 1–7.

Source data

Source Data Fig. 3

Numerical source data for Fig. 3.

Source Data Fig. 4

Numerical source data for Fig. 4.

Source Data Fig. 5

Numerical source data for Fig. 5.

Source Data Extended Data Fig. 2

Numerical source data for Extended Data Fig. 2.

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Grelet, E., Tortora, M.M.C. Elucidating chirality transfer in liquid crystals of viruses. Nat. Mater. (2024). https://doi.org/10.1038/s41563-024-01897-x

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