High viral abundance and low diversity are associated with increased CRISPR-Cas prevalence across microbial ecosystems

Abstract

CRISPR-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.2-4 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 theory6-8 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.