The halophilic archaeon Halogranum roseipondis sp. nov. is susceptible to a virus carrying an exceptionally high number of viral tRNA genes

Abstract

Archaea constitute a diverse group of organisms, many of which inhabit extreme environments, such as haloarchaea that dominate hypersaline ecosystems, like solar salterns. Although sampling of solar salterns and other hypersaline environments have resulted in numerous haloarchaeal isolates, including 3 classified and 25 unclassified Halogranum species, no complete genome has been reported for any member of this genus. Here we present the first comprehensive study of Halogranum sp. SS5-1 isolated from a solar saltern in Samut Sakhon, Thailand. Hgn. SS5-1 is a pleomorphic, aerobic heterotroph that thrives in high salinity and moderate temperature and is capable of hydrolysing starch. Its genome consists of a 3.6 Mbp chromosome and seven additional plasmids. Based on our phylogenetic analyses, which establish Hgn. SS5-1 as a distinct species, we propose that it will be classified as the novel species Halogranum roseipondis sp. nov. SS5-1T. Additionally, we report that Hgn. roseipondis sp.nov. SS5-1T is infected by Hagravirus capitaneum (HGTV-1), the only virus known to infect a Halogranum host. HGTV-1 exhibits a unique head-tailed morphology and encodes the largest archaeal virus dsDNA genome known to date, including 34 tRNA encoding genes. Codon usage analysis of the viral genome suggests partial alignment with host preferences, yet the abundance of viral tRNA genes hints to broader roles, potentially including translation modulation. This study establishes Hgn. roseipondis and HGTV-1 as a novel virus-host system, opening avenues to explore infection dynamics and the roles of virus-encoded tRNA in archaea. ImportanceArchaea that thrive in high-salinity environments are key players in geochemical cycles and the primary producers in their habitat. Despite their ecological significance and importance for the development of novel applications in synthetic biology, haloarchaea remain poorly studied. For example, exploration of haloarchaea is required to understand the evolution of cellular complexity and the molecular mechanisms that allow cells to thrive in harsh environmental conditions. In this study, we characterize a novel archaeon, Halogranum roseipondis sp. SS5-1T, alongside the infection cycle of its associated virus, Hagravirus capitaneum. This tailed myovirus carries an extraordinary set of 34 viral tRNA genes, a feature that opens intriguing questions about virus-host interactions and translational control. Our findings lay the groundwork for future investigations into the expression and function of viral tRNAs in an archaeal model system, thereby enabling the study of archaeal translation and virus-driven modulation of host cellular processes.