Structural puzzles in virology solved with an overarching icosahedral design principle

Reidun Twarock,Antoni Luque

doi:10.1038/s41467-019-12367-3

Reidun Twarock, Antoni Luque

Open Access

https://doi.org/10.1038/s41467-019-12367-3

Copy DOI

Abstract

Viruses have evolved protein containers with a wide spectrum of icosahedral architectures to protect their genetic material. The geometric constraints defining these container designs, and their implications for viral evolution, are open problems in virology. The principle of quasi-equivalence is currently used to predict virus architecture, but improved imaging techniques have revealed increasing numbers of viral outliers. We show that this theory is a special case of an overarching design principle for icosahedral, as well as octahedral, architectures that can be formulated in terms of the Archimedean lattices and their duals. These surface structures encompass different blueprints for capsids with the same number of structural proteins, as well as for capsid architectures formed from a combination of minor and major capsid proteins, and are recurrent within viral lineages. They also apply to other icosahedral structures in nature, and offer alternative designs for man-made materials and nanocontainers in bionanotechnology.

Highlights

Viruses have evolved protein containers with a wide spectrum of icosahedral architectures to protect their genetic material
Viruses exhibit this high degree of symmetry as a consequence of a principle that Crick and Watson termed genetic economy, namely, the limited capacity in the viral genome to code for the coat proteins (CPs) forming its surrounding capsid[9]
We are able to derive eight families of icosahedral polyhedra that explain the outliers to the current classification scheme and at the same time provide an overarching design principle that encompasses the current models of virus architecture in Caspar-Klug theory

Summary

Introduction

Viruses have evolved protein containers with a wide spectrum of icosahedral architectures to protect their genetic material. The majority of viruses adopt polyhedral designs with icosahedral symmetry[7,8], that is, their CP positions conform to polyhedral blueprints that exhibit the characteristic arrangement of the rotational symmetry axes of an icosahedron (Fig. 1a) Viruses exhibit this high degree of symmetry as a consequence of a principle that Crick and Watson termed genetic economy, namely, the limited capacity in the viral genome to code for the CPs forming its surrounding capsid[9]. Caspar and Klug extended this idea by introducing the principle of quasiequivalence[11], which explains how proteins can adopt locally equivalent, or quasiequivalent, positions in a capsid, by repeating this local configuration across the capsid surface This allows larger viruses to form, requiring even smaller relative portions of their genomic sequences to code for their capsids, generating coding capacity for other viral components that are not present in smaller viruses and enabling more complex infection scenarios. This discovery sheds new light on the many areas of science where icosahedral structures play an important role, and provides designs for applications in bionanotechnology

Methods

Results

Conclusion