Abstract
Virus–host interactions evolve along a symbiosis continuum from antagonism to mutualism. Long-term associations between virus and host, such as those in chronic infection, will select for traits that drive the interaction towards mutualism, especially when susceptible hosts are rare in the population. Virus–host mutualism has been demonstrated in thermophilic archaeal populations where Sulfolobus spindle-shaped viruses (SSVs) provide a competitive advantage to their host Sulfolobus islandicus by producing a toxin that kills uninfected strains. Here, we determine the genetic basis of this killing phenotype by identifying highly transcribed genes in cells that are chronically infected with a diversity of SSVs. We demonstrate that these genes alone confer growth inhibition by being expressed in uninfected cells via a Sulfolobus expression plasmid. Challenge of chronically infected strains with vector-expressed toxins revealed a nested network of cross-toxicity among divergent SSVs, with both broad and specific toxin efficacies. This suggests that competition between viruses and/or their hosts could maintain toxin diversity. We propose that competitive interactions among chronic viruses to promote their host fitness form the basis of virus–host mutualism.This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
Highlights
Viruses of microbes play key roles in shaping the population dynamics of their host
We used transcriptomics to identify highly expressed genes in several divergent spindle-shaped viruses (SSVs), and by expressing these genes ectopically in uninfected strains we have shown spindle-shaped virus 9 (SSV9) B310 and SSV11 p29 are the toxins responsible for the competitive phenotype of SSV-infected cells
For SSV9 B310, the toxic effect is dependent on an N-terminal portion of the gene product, absence of which abolishes the phenotype
Summary
This can be due to antagonistic interactions, such as those with lytic viruses, or more mutualistic interactions, in which the host is benefited [1,2] Such benefits can include growth advantages, for example by viruses that encode auxiliary metabolic genes [3,4,5], or competitive advantages in which the infected hosts are able to outcompete their uninfected counterparts such as through the production of intraspecific toxins [6]. Infection with viruses has been shown to induce host toxin–antitoxin systems [13,14,15,16] In their carrier (non-induced) state, very few viral genes are expressed, the majority of which are predicted to encode structural proteins [16]. The competitive advantage associated with SSV9 infection is due to the ability of chronically infected hosts to kill uninfected hosts, even when initially rare in the population [17]. Challenge of chronically infected strains with different toxins suggests there may be competition among hosts mediated by their mutualistic viral infections
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