Quantification of archaea-driven freshwater nitrification from single cell to ecosystem levels

Franziska Klotz,David Kamanda Ngugi,Katharina Kitzinger,Bernhard Schink,Michael Pester,Sten Littmann,Marcel M M Kuypers,Petra Büsing

doi:10.1038/s41396-022-01216-9

Abstract

Deep oligotrophic lakes sustain large populations of the class Nitrososphaeria (Thaumarchaeota) in their hypolimnion. They are thought to be the key ammonia oxidizers in this habitat, but their impact on N-cycling in lakes has rarely been quantified. We followed this archaeal population in one of Europe’s largest lakes, Lake Constance, for two consecutive years 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 present in major inland water bodies, for which we propose the name “Candidatus Nitrosopumilus limneticus”. Its biomass corresponded to 12% of carbon stored in phytoplankton over the year´s cycle. Ca. N. limneticus populations incorporated significantly more ammonium than most other microorganisms in the hypolimnion and were driving potential ammonia oxidation rates of 6.0 ± 0.9 nmol l‒1 d‒1, corresponding to potential cell-specific rates of 0.21 ± 0.11 fmol cell–1 d–1. At the ecosystem level, this translates to a maximum capacity of archaea-driven nitrification of 1.76 × 109 g N-ammonia per year or 11% of N-biomass produced annually by phytoplankton. We show that ammonia-oxidizing archaea play an equally important role in the nitrogen cycle of deep oligotrophic lakes as their counterparts in marine ecosystems.

Highlights

Freshwater lakes are important drinking water reservoirs
As amoA is typically present as a single copy gene in ammoniaoxidizing archaea (AOA) [46], amoA copy numbers were compared to total archaeal and bacterial 16S rRNA gene copy numbers to estimate AOA relative abundance
Over the last two decades, reports have accumulated that deep oligotrophic lakes sustain large populations of Nitrososphaeria (“Thaumarchaeota”) in their hypolimnion [10, 15–20]

Summary

Introduction

Freshwater lakes are important drinking water reservoirs. To be suitable as drinking water and to prevent toxicity to fish, ammonia must not accumulate. Nitrification prevents an accumulation of ammonia and converts it to nitrate via nitrite, with ammonia oxidation generally being the rate-limiting step [1]. Nitrification does not directly change the inventory of inorganic N in freshwater ecosystems, it represents a critical link between mineralization of organic N and its eventual loss as N2 to the atmosphere through denitrification or anaerobic ammonium oxidation [1]. The process of ammonia oxidation is catalyzed by three different microbial guilds. The third guild oxidizes ammonia directly to nitrate and is referred to as complete ammonia oxidizers (comammox) [6, 7]

Methods

Results

Conclusion