Abstract
The population diversity and structure of CRISPR-Cas immunity provides key insights into virus–host interactions. Here, we examined two geographically and genetically distinct natural populations of the thermophilic crenarchaeon Sulfolobus islandicus and their interactions with Sulfolobus spindle-shaped viruses (SSVs) and S. islandicus rod-shaped viruses (SIRVs). We found that both virus families can be targeted with high population distributed immunity, whereby most immune strains target a virus using unique unshared CRISPR spacers. In Kamchatka, Russia, we observed high immunity to chronic SSVs that increases over time. In this context, we found that some SSVs had shortened genomes lacking genes that are highly targeted by the S. islandicus population, indicating a potential mechanism of immune evasion. By contrast, in Yellowstone National Park, we found high inter- and intra-strain immune diversity targeting lytic SIRVs and low immunity to chronic SSVs. In this population, we observed evidence of SIRVs evolving immunity through mutations concentrated in the first five bases of protospacers. These results indicate that diversity and structure of antiviral CRISPR-Cas immunity for a single microbial species can differ by both the population and virus type, and suggest that different virus families use different mechanisms to evade CRISPR-Cas immunity.This article is part of a discussion meeting issue ‘The ecology and evolution of prokaryotic CRISPR-Cas adaptive immune systems’.
Highlights
Infection by viruses is a common feature among the three domains of life
We examined their interactions with contemporary chronic, non-lytic Sulfolobus spindle-shaped viruses (SSVs) from the Fuselloviridae family and lytic S. islandicus rod-shaped viruses (SIRVs) from the Rudiviridae family
We investigated whether in silico and in vitro predictions about the distributed population structure of Clustered regularly interspaced short palindromic repeats (CRISPRs)-CRISPR-associated system (Cas) immunity are applicable in nature using two geographically distinct populations of S. islandicus [26,27]
Summary
Infection by viruses is a common feature among the three domains of life. Genetic diversity within genes associated with antiviral immunity is often high compared with the rest of an organism’s genome and is maintained by diversifying selection [1,2]. Clustered regularly interspaced short palindromic repeats (CRISPRs) are genetic loci that function with CRISPR-associated system (Cas) genes to provide bacteria and archaea with adaptive immunity against viruses and foreign nucleic acids [10] In these systems, short genome-encoded sequences called spacers. To expand our understanding of the population structure of CRISPR diversity and its impact on virus–host interactions, we present findings from our study of Sulfolobus islandicus populations isolated from hot springs in Yellowstone National Park in the United States and near Mutnovsky volcano in Kamchatka, Russia. Spacers targeting protospacers lacking PAM sequences were only considered to provide immunity if the host strain had a type III CRISPR-Cas system. Distributed immunity (DI), which describes the diversity and distribution of virus-targeting spacers, was calculated by comparing the immunity providing spacers for every pair of immune strains in a population. Statistical analysis of data was performed using either Graphpad Prism for Windows (v. 7.02) or R (v. 3.3.2)
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