Ecological and Metabolic Strategies of Nitrifying Lineages Across Freshwater Inland Seas

Nitrifiers represent a phylogenetically and metabolically diverse group whose activity has consequences for nitrogen remineralization and carbon fixation. Contributions of nitrifiers to carbon fixation may be especially significant in deep, well-oxygenated water columns like those found in the Laurentian Great Lakes, Earth’s largest freshwater ecosystem. Using genome reconstructions and quantitative population genomics, we characterized the phylogenetic and metabolic diversity of nitrifiers across the five Laurentian Great Lakes, which encompass strong gradients of nutrient availability, productivity, and water clarity. Nitrifiers were restricted to aphotic waters in deep basins during summer stratification. The ammonia oxidizing bacterial family Nitrosomonadaceae was well-represented across all lakes, while ammonia oxidizing archaea in Nitrosoarchaeum were restricted to a few of the deepest basins. Metabolic and genome features differed across Nitrosomonadaceae subtypes; one subtype found predominantly in the low-productivity upper lakes was characterized by a very small genome, low GC content, and the presence of proteorhodopsin. Newly discovered Ca. Nitrotoga were the only nitrite oxidizing bacteria detected in Lake Erie while Nitrospira were the only nitrite oxidizing bacteria detected in Lake Superior. While nitrite oxidizers exhibited low phylogenetic diversity, frequency of certain genes within a population, including Nitrospira urease genes, varied across lakes, suggesting environmental selection at the gene level. Our findings have implications for predicting how carbon flux and nitrogen cycling within the Laurentian Great Lakes will respond to environmental changes (e.g., increased water clarity) and explaining niche differentiation among phylogenetically diverse nitrifier lineages.