Cellular organisms from all three domains of life, from the simple prokaryotes to highly-organized multicellular eukaryotes, are infected with viruses that have coevolved with their hosts for millions of years. As a result of this perennial arms race, viruses are efficient nanomachines that have adapted to function in any environment where their hosts are found. Viruses infecting extremophilic archaea, which thrive in extremely hot and acidic environments, are of particular interest both from fundamental and biotechnological perspectives. One such virus, Sulfolobus monocaudavirus 1 (SMV1), a member of the Bicaudaviridae family, has large lemon-shaped virions and infects hyperthermophilic acidophile Sulfolobus islandicus. Due to its polyextremophilic nature, SMV1 has recently emerged as a promising model system to study the mechanic properties of extremophilic viruses but also as an oral nanocage candidate because of its ability to cross the gastrointestinal barrier. Currently, principles underlying the robustness of SMV1 virions in the extremely harsh conditions of its natural habitats (76ºC, pH~3) remain unknown nor is it understood how the lemon-shaped virion is constructed. To gain insights into these questions, in this work we analyzed the SMV1 virions using the atomic force microscopy (AFM) in liquid milieu. This technique provides information about the structural changes in real time due to material fatigue when applying external forces. Furthermore, we can also determine the physical properties of the viral particle, such as the stiffness or the viral resilience in hydrated and dehydrated conditions, both of which are physiologically relevant for environmental viruses. Unlike other studied viruses, under forces of few nN, SMV1 behaves in a wavy, plastic fashion without presenting fragile fracture or evident cracks. This absence of brittleness seems adequate for the virus to surpass the stringent environmental conditions and its extreme deformation during the binding to the host.

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