Global, single-cell-resolution of antiviral defenses in marine prokaryoplankton

Abstract

Background Growing evidence suggests that variation in resistance to viral infections by marine prokaryoplankton enables the coexistence of both viral and host populations. Recent experimental work on model organisms has revealed dozens of novel antiviral defense mechanisms. This diversity has prompted the hypothesis of the pan-immunity model, in which diverse defenses are a shared resource among closely related individuals to broaden the population's resistance and minimize an individual's burden. The composition and abundance of such defense pools in natural microbial communities, however, remain largely unknown. Here, we begin to parameterize resistance in marine prokaryotes and define their defense repertoire by quantifying antiviral defenses across thousands of randomized single-amplified genomes (SAGs) from a global collection of seawater samples. Results Prokaryoplankton SAGs contained an average of 1.1 defenses, with dark ocean (200 m - 11 km) prokaryotes having a slightly higher genomic load of defenses as compared to the sunlit, surface ocean. The number of defenses per cell was taxon-specific, with little or no relationship to depth, taxon abundance, estimated maximal growth rate, or viral infection rate. The most numerous and taxonomically widespread defenses were restriction modification systems, followed by dGTPase (mostly in Pelagibacterales) in the sunlit ocean and AbiU (mostly in Nitrososphaerales) in the dark ocean. Most other defense types were rare (< 0.1% SAGs) yet distributed across distant taxa (> 3 phyla). We found evidence for the cross-domain exchange of the most common defense system, RM II, between archaea and bacteria, which improves our understanding of the biology of this prevalent defense and could be consequential in predicting target motifs for connecting viruses with potential hosts in epigenetic studies. Conclusions Collectively, these results suggest lineages restrict genomic real estate for defenses yet enable extensive lateral transfer, potentially for the maintenance of defense variation at the community level rather than only among closely related individuals. This study provides a quantitative atlas of prokaryoplankton immunity toward grounding our understanding of virus-microbe interactions in the Earth's largest biome, the open ocean.