Ecology, ecosystem services and evolution of freshwater ammonia oxidizing archaea

Large planktonic population of ammonia oxidizing archaea (AOA) inhabit deep oligotrophic lakes, resembling the situation in the open ocean. They are thought to be the key ammonia oxidizers in these freshwater reservoirs and as such responsible for the rate-limiting step in nitrification. We followed this archaeal population in one of Europe"s largest lakes, Lake Constance, using metagenomics and metatranscriptomics combined with stable isotope-based activity measurements. An abundant (8–39% of picoplankton) and transcriptionally active archaeal ecotype dominated the nitrifying community. It represented a freshwater-specific species: "Candidatus Nitrosopumilus limneticus". Its biomass corresponded to 12% of carbon stored in phytoplankton over the year´s cycle. Ca. N. limneticus populations were driving potential ammonia oxidation rates of 6.0 ± 0.9 nmol l^‒1 d^‒1. At the ecosystem level, this translates to a maximum capacity of archaea-driven nitrification of 1760 metric tons of N-ammonia per year or 11% of N-biomass produced annually by phytoplankton¹. We extended this analysis by a global assessment of lacustrine AOA diversity. Using continental-scale metagenomics, we show that AOA species diversity in freshwater systems is remarkably low compared to marine environments. We further show that Ca. Nitrosopumilus limneticus is ubiquitous and genotypically static in various large European lakes where it evolved 13 million years ago. We find that extensive proteome remodeling was a key innovation for freshwater colonization of AOA². These findings reveal the genetic diversity and adaptive mechanisms of a keystone species that has survived clonally in lakes for millennia.

¹Klotz et al., 2022. ISME J. 16:1647-1656
²Ngugi et al., 2023. Science Advances. 9: eadc9392