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  1. Cock, M. (Ed.)
  2. Moran, Mary Ann (Ed.)
    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. 
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  3. Many biological functions are leaky, and organisms that perform them contribute some of their products to a community “marketplace” in which nonperforming individuals may compete for them. Leaky functions are partitioned unequally in microbial communities, and the evolutionary forces determining which species perform them and which become beneficiaries are poorly understood. Here, we demonstrate that the market principle of comparative advantage determines the distribution of a leaky antibiotic resistance gene in an environment occupied by two “species”—strains ofEscherichia coligrowing on mutually exclusive resources and thus occupying separate niches. Communities comprised of antibiotic-resistant cells were rapidly invaded by sensitive cells of both types. While the two phenotypes coexisted stably for 500 generations, in 15/18 replicates, antibiotic sensitivity became fixed in one species. Fixation always occurred in the same species despite both species being genetically identical except for their niche-defining mutation. In the absence of antibiotic, the fitness cost of resistance was identical in both species. However, the intrinsic resistance of the species that ultimately became the sole helper was significantly lower, and thus its reward for expressing the resistance gene was higher. Opportunity cost of resistance, not absolute cost or efficiency of antibiotic removal, determined which species became the helper, consistent with the economic theory of comparative advantage. We present a model that suggests that this market-like dynamic is a general property of Black Queen systems and, in communities dependent on multiple leaky functions, could lead to the spontaneous development of an equitable and efficient division of labor.

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