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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’.
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Surface resistance to SSVs and SIRVs in pilin deletions of Sulfolobus islandicus
Abstract Characterizing the molecular interactions of viruses in natural microbial populations offers insights into virus–host dynamics in complex ecosystems. We identify the resistance ofSulfolobus islandicustoSulfolobusspindle‐shaped virus (SSV9) conferred by chromosomal deletions of pilin genes,pilA1andpilA2that are individually able to complement resistance. Mutants with deletions of bothpilA1andpilA2or the prepilin peptidase, PibD, show the reduction in the number of pilins observed in TEM and reduced surface adherence but still adsorb SSV9. The proteinaceous outer S‐layer proteins, SlaA and SlaB, are not required for adsorption nor infection demonstrating that the S‐layer is not the primary receptor for SSV9 surface binding. Strains lacking both pilins are resistant to a broad panel of SSVs as well as a panel of unrelatedS. islandicusrod‐shaped viruses (SIRVs). Unlike SSV9, we show thatpilA1orpilA2is required for SIRV8 adsorption. In sequencedSulfolobusstrains from around the globe, one copy of eachpilA1andpilA2is maintained and show codon‐level diversification, demonstrating their importance in nature. By characterizing the molecular interactions at the initiation of infection betweenS. islandicusand two different types of viruses we hope to increase the understanding of virus–host interactions in the archaeal domain.
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- Award ID(s):
- 1656869
- PAR ID:
- 10375189
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Microbiology
- Volume:
- 113
- Issue:
- 4
- ISSN:
- 0950-382X
- Page Range / eLocation ID:
- p. 718-727
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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