Totivirus–satellite coinfection prevalence and host genotype associations in wild <i>Saccharomyces cerevisiae</i>

Saccharomyces cerevisiae is occasionally infected by dsRNA totiviruses and their toxin-encoding dsRNA satellite nucleic acids. The autonomous totivirus and its satellite can coexist but with an asymmetric dependence of the satellite on the totivirus for replication and maintenance inside the host cell. Satellites provide their yeast hosts with inhibitory toxins and the necessary self-immunity; loss of the satellite equates to loss of toxin immunity. Because these viral elements lack known extracellular stages, and sex is suspected to be rare, they are assumed to be transmitted vertically, implying that infection states should correlate with host genotypes. However, totivirus-satellite coinfections are rarely examined in natural populations, leaving their associations with host genotypes poorly understood. We screened a multiyear, vineyard-associated population of S. cerevisiae isolates from New Zealand to examine the stability of host-virus associations over time, both within and across genotypes. Over half of the wild isolates harbored infections (55%), but less than half of these (37% of infected) had toxin-encoding satellites. Genotypes that persisted across years typically maintained consistent infection states. However, we also observed stepwise transitions from coinfection through infection to an infection-free state, as well as acquisition of totiviruses and satellites. Genotypes clustered strongly by infection state, and population heterozygosity was significantly lower than expected, supporting vertical transmission while suggesting that outcrossing is not responsible for the acquisition of higher infection states. Despite occasional intragenotypic transitions, genotype clustering by infection state remained intact, suggesting that such transitions are transient and that host genotypes may have optimal infection states with regard to totiviruses and their satellites.