Abstract
CRISPR-Cas adaptive immune systems are found in bacteria and archaea and provide defence against phage by inserting phage-derived sequences into CRISPR loci on the host genome to provide sequence specific immunological memory against re-infection. Under laboratory conditions the bacterium Pseudomonas aeruginosa readily evolves the high levels of CRISPR-based immunity against clonal populations of its phage DMS3vir, which in turn causes rapid extinction of the phage. However, in nature phage populations are likely to be more genetically diverse, which could theoretically impact the frequency at which CRISPR-based immunity evolves which in turn can alter phage persistence over time. Here we experimentally test these ideas and found that a smaller proportion of infected bacterial populations evolved CRISPR-based immunity against more genetically diverse phage populations, with the majority of the population evolving a sm preventing phage adsorption and providing generalised defence against a broader range of phage genotypes. However, those cells that do evolve CRISPR-based immunity in response to infection with more genetically diverse phage acquire greater numbers of CRISPR memory sequences in order to resist a wider range of phage genotypes. Despite differences in bacterial resistance evolution, the rates of phage extinction were similar in the context of clonal and diverse phage infections suggesting selection for CRISPR-based immunity or sm-based resistance plays a relatively minor role in the ecological dynamics in this study. Collectively, these data help to understand the drivers of CRISPR-based immunity and their consequences for bacteria-phage coexistence, and, more broadly, when generalised defences will be favoured over more specific defences.
Highlights
Bacterial and archaeal viruses can influence microbial communities both through direct interactions with their hosts as well as indirect effects on non-host populations [1,2,3,4]
We find that infecting P. aeruginosa with experimentally evolved populations of phage DMS3vir that have elevated levels of standing genetic diversity results in, first, higher frequencies of smbased resistance compared with CRISPR-based immunity and that, second, cells with CRISPR-based immunity are more likely to acquire multiple spacers
While the elevated genetic variation of phage DMS3vir is presumably more reflective of natural environments compared with the clonal phage populations that are typically used in experimental evolution studies, it should be noted that our experiments do not capture the complexity of natural environments where different phages with overlapping host ranges tend to coexist, which can further impact the evolution of CRISPR-based immunity [31]
Summary
Bacterial and archaeal viruses can influence microbial communities both through direct interactions with their hosts as well as indirect effects on non-host populations [1,2,3,4]. The selective pressure of viral predation has resulted in the evolution of a range of archaeal and bacterial defence mechanisms, which includes CRISPR-Cas (clustered regularly interspaced short palindromic repeats; CRISPRassociated) systems, prokaryotic argonautes, restriction– modification (R–M) systems, surface modification (sm), toxin–antitoxin and abortive infection systems [5]. These defences differ in multiple ways including the range of phage to which they provide resistance (generalist versus specialist) and in their fitness costs [6]. Phage can in turn overcome CRISPR-based immunity by acquiring a point mutation in the target sequence on their genome [14], the emergence and spread of such phage “escape” mutants is constrained by both the diversity of CRISPR immunity alleles in the bacterial population and the fitness costs associated with the phage mutations [15,16,17,18]
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