The tubular cavity of tobacco mosaic virus shields mechanical stress and regulates disassembly

Abstract

Here we probe Tobacco mosaic virus (TMV) particles immobilized on a solid surface under transversal mechanical stress. We use atomic force microscopy to implement punctual deformation with high force (∼nN) that induces immediate virus rupture (single indentation assay), and continuous cycles of low force (∼100 pN) that generate a gradual disassembly of the virus particle (mechanical fatigue assay). These experiments are interpreted with the help of TMV coarse-grained and finite elements simulations, which indicate that the tubular cavity screens the transmission of mechanical stress from the top to the bottom half of the virion structure. Likewise, mechanical fatigue experiments reveal how TMV disassembles following growing transversal rifts with different dynamics that depend on a combination of the applied force and the tubular geometry of the virus. Our results indicate how the cylindrical cavity of TMV cushions the lower half of the virus structure from mechanical stress and regulates mechanical disassembly.

Statement of significance

The inability of plant viruses like tobacco mosaic virus (TMV) to infect mammals makes them ideal for technological applications. While TMV is known for it's durability, it's unclear if this is due solely to its capsid proteins or its tubular structure. Using Atomic Force Microscopy, coarse-grained and finite elements models, we found that the tubular hole screens the transmission of mechanical stress from the top to the bottom half of the virion structure. This characteristic induces a stepwise disassembly process from intact to half virus, finishing in the virion disruption. Since the energies between proteins are comparable to those of other viruses, there is a protective effect of the tubular cavity that transcends the size down to the nanoscale.