Abstract
SummaryCRISPR-Cas are adaptive immune systems that protect their hosts against viruses and other parasitic mobile genetic elements.1 Although widely distributed among prokaryotic taxa, CRISPR-Cas systems are not ubiquitous.2, 3, 4 Like most defense-system genes, CRISPR-Cas are frequently lost and gained, suggesting advantages are specific to particular environmental conditions.5 Selection from viruses is assumed to drive the acquisition and maintenance of these immune systems in nature, and both theory6, 7, 8 and experiments have identified phage density and diversity as key fitness determinants.9,10 However, these approaches lack the biological complexity inherent in nature. Here, we exploit metagenomic data from 324 samples across diverse ecosystems to analyze CRISPR abundance in natural environments. For each metagenome, we quantified viral abundance and diversity to test whether these contribute to CRISPR-Cas abundance across ecosystems. We find a strong positive association between CRISPR-Cas abundance and viral abundance. In addition, when controlling for differences in viral abundance, CRISPR-Cas systems are more abundant when viral diversity is low, suggesting that such adaptive immune systems may offer limited protection when required to target a diverse viral community. CRISPR-Cas abundance also differed among environments, with environmental classification explaining roughly a quarter of the variation in CRISPR-Cas relative abundance. The relationships between CRISPR-Cas abundance, viral abundance, and viral diversity are broadly consistent across environments, providing robust evidence from natural ecosystems that supports predictions of when CRISPR is beneficial. These results indicate that viral abundance and diversity are major ecological factors that drive the selection and maintenance of CRISPR-Cas in microbial ecosystems.
Highlights
Variation in CRISPR-Cas abundance is partially explained by viral abundance While it is well established that CRISPR-Cas immune systems can protect bacteria and archaea against viral infections under in vitro laboratory conditions, it remains unclear how important viruses are as a selective force for the maintenance of CRISPR-Cas systems in nature, as CRISPR-Cas targets other genetic parasites, such as plasmids.[11]
Our analyses use all contigs classified as viral, and while the vast majority of these are of bacteriophage and prophage origin, we refer to these as viral for consistency. These metagenomes vary in both CRISPRCas and viral abundance and provided a suitable dataset to test the hypothesis that viral abundance drives selection for CRISPR-Cas (Figure 1)
We found a positive correlation between viral abundance and the abundance of CRISPR-Cas systems, with viral abundance explaining around 20% of the observed variation in CRISPR-Cas abundance (R2 = 0.209)
Summary
CRISPR-Cas are adaptive immune systems that protect their hosts against viruses and other parasitic mobile genetic elements.[1]. We quantified viral abundance and diversity to test whether these contribute to CRISPR-Cas abundance across ecosystems. When controlling for differences in viral abundance, CRISPR-Cas systems are more abundant when viral diversity is low, suggesting that such adaptive immune systems may offer limited protection when required to target a diverse viral community. The relationships between CRISPR-Cas abundance, viral abundance, and viral diversity are broadly consistent across environments, providing robust evidence from natural ecosystems that supports predictions of when CRISPR is beneficial. These results indicate that viral abundance and diversity are major ecological factors that drive the selection and maintenance of CRISPR-Cas in microbial ecosystems
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