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ABSTRACT The mechanisms driving cyanobacterial harmful algal blooms (HABs) like those caused by Microcystis aeruginosa remain elusive, but improved defense against viral predation has been implicated for success in eutrophic environments. Our genus-level analyses of 139,023 genomes revealed that HAB-forming cyanobacteria carry vastly more restriction modification systems per genome (RMPG) than nearly all other prokaryotic genera, suggesting that viral defense is a cornerstone of their ecological success. In contrast, picocyanobacteria that numerically dominate nutrient-poor systems have the fewest RMPG within the phylum Cyanobacteria . We used classic resource competition models to explore the hypothesis that nutrient enrichments drive ecological selection for high RMPG due to increased host-phage contact rate. These classic models, agnostic to the mechanism of defense, explain how nutrient loading can select for increased RMPG but, importantly, fail to explain the extreme accumulation of these defense systems. However, extreme accumulation of RMPG can be achieved in a novel “memory” model that accounts for a unique activity of restriction modification systems: the accidental methylation of viral DNA by the methyltransferase. The methylated virus “remembers” the RM defenses of its former host and can evade these defenses if they are present in the next host. This viral memory leads to continual RM system devaluation; RMs accumulate extensively because the benefit of each addition is diminished. Our modeling leads to the hypothesis that nutrient loading and virion methylation drive the extreme accumulation of RMPG in HAB-forming cyanobacteria. Finally, our models suggest that hosts with different RMPG values can coexist when hosts have unique sets of RM systems. IMPORTANCE Harmful algal blooms (HABs), caused by cyanobacteria like Microcystis aeruginosa , are a global threat to water quality and use across the planet. Researchers have agreed that nutrient loading is a major contributor to HAB persistence. While we may understand the environmental conditions that cause HABs, we still struggle in identifying the mechanisms that explain why these organisms have a competitive edge against other, less ecologically hazardous organisms. Our interdisciplinary approach in microbiology, mathematical population modeling, and genomics allows us to use nearly 70 years of research in restriction modification systems to show that HAB-forming cyanobacteria are exceptional in their ability to defend against viruses, and this capacity is intimately tied to nutrient loading. Our hypothesis suggests that defense against viral predation is a fundamental pillar of cyanobacterial ecological strategy and an important contributor to HAB dynamics. 

ABSTRACT The genomes of Asgard Archaea , a novel archaeal proposed superphylum, share an enriched repertoire of eukaryotic signature genes and thus promise to provide insights into early eukaryote evolution. However, the distribution, metabolisms, cellular structures, and ecology of the members within this superphylum are not well understood. Here we provide a meta-analysis of the environmental distribution of the Asgard archaea, based on available 16S rRNA gene sequences. Metagenome sequencing of samples from a salt-crusted lagoon on the Baja California Peninsula of Mexico allowed the assembly of a new Thorarchaeota and three Lokiarchaeota genomes. Comparative analyses of all known Lokiarchaeota and Thorarchaeota genomes revealed overlapping genome content, including central carbon metabolism. Members of both groups contained putative reductive dehalogenase genes, suggesting that these organisms might be able to metabolize halogenated organic compounds. Unlike the first report on Lokiarchaeota , we identified genes encoding glycerol-1-phosphate dehydrogenase in all Loki - and Thorarchaeota genomes, suggesting that these organisms are able to synthesize bona fide archaeal lipids with their characteristic glycerol stereochemistry. IMPORTANCE Microorganisms of the superphylum Asgard Archaea are considered to be the closest living prokaryotic relatives of eukaryotes (including plants and animals) and thus promise to give insights into the early evolution of more complex life forms. However, very little is known about their biology as none of the organisms has yet been cultivated in the laboratory. Here we report on the ecological distribution of Asgard Archaea and on four newly sequenced genomes of the Lokiarchaeota and Thorarchaeota lineages that give insight into possible metabolic features that might eventually help to identify these enigmatic groups of archaea in the environment and to culture them.