Unravelling the Role of the F55 Regulator in the Transition from Lysogeny to UV Induction of Sulfolobus Spindle-Shaped Virus 1

Abstract

Sulfolobus spindle-shaped virus 1 represents a model for studying virus-host interaction in harsh environments, and it is so far the only member of the family Fuselloviridae that shows a UV-inducible life cycle. Although the virus has been extensively studied, mechanisms underpinning the maintenance of lysogeny as well as those regulating the UV induction have received little attention. Recently, a novel SSV1 transcription factor, F55, was identified. This factor was able to bind in vitro to several sequences derived from the early and UV-inducible promoters of the SSV1 genome. The location of these binding sites together with the differential affinity of F55 for these sequences led to the hypothesis that this protein might be involved in the maintenance of the SSV1 lysogeny. Here, we report an in vivo survey of the molecular events occurring at the UV-inducible region of the SSV1 genome, with a focus on the binding profile of F55 before and after the UV irradiation. The binding of F55 to the target promoters correlates with transcription repression, whereas its dissociation is paralleled by transcription activation. Therefore, we propose that F55 acts as a molecular switch for the transcriptional regulation of the early viral genes. IMPORTANCEFunctional genomic studies of SSV1 proteins have been hindered by the lack of similarity with other characterized proteins. As a result, few insights into their in vivo roles have been gained throughout the last 3 decades. Here, we report the first in vivo investigation of an SSV1 transcription regulator, F55, that plays a key role in the transition from the lysogenic to the induced state of SSV1. We show that F55 regulates the expression of the UV-inducible as well as the early genes. Moreover, the differential affinity of this transcription factor for these targets allows a fine-tuned and temporal coordinated regulation of transcription of viral genes.T he majority of viruses isolated from Crenarchaea shows virion morphotypes that have not been observed for viruses infecting Bacteria and Eukarya. Consequently, eight novel viral families have been introduced in order to classify these novel viruses (Fuselloviridae, Lipothrixviridae, Rudiviridae, Guttaviridae, Globuloviridae, Bicaudaviridae, Ampullaviridae, and Clavaviridae), but so far, there are still several unique archaeal viruses that remain to be classified (1-3). Many analyses of environmental samples have shown that spindle-shaped viruses are abundant and occupy several niches, including deep sea hydrothermal vents (4, 5), hypersaline environments (6, 7), anoxic freshwaters (8), cold Antarctic lakes (9), terrestrial hot springs (10-12), and acidic mines (13, 14), where they frequently outnumber head-tailed viruses. Notably, this unique virion morphotype seems to be a hallmark of viruses infecting Archaea, since it has never been observed for bacteriophages or eukaryal viruses (15). To date, the family Fuselloviridae comprises nine members (SSV1, SSV2, SSV4, SSV5, SSV6, SSV7, SSV8, SSV9, and ASV1) isolated f...

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“…SSV1 encodes a second monocistronic transcript in this region, T lys , that apparently is expressed constitutively (25,26). T lys encodes a 55-amino-acid protein (F55) that is hypothesized to repress transcription from early viral promoters, maintaining low virus expression in the absence of UV irradiation (25).…”

“…The protein product of ORF f55 is predicted to possess an RHH DNA binding domain and was shown to bind weakly to a number of viral promoters in vitro that presumably control the expression of early gene products. Based on these data, SSV1-F55 is hypothesized to maintain lysogeny by repressing early viral promoters (25,26).…”