Competition between ammonia-oxidizing archaea and complete ammonia oxidizers from freshwater environments.

ABSTRACT

Aerobic ammonia oxidizers (AOs) are prokaryotic microorganisms that contribute to the global nitrogen cycle by performing the first step of nitrification, the oxidation of ammonium to nitrite and nitrate. While aerobic AOs are found ubiquitously, their distribution is controlled by key environmental conditions such as substrate (ammonium) availability. Ammonia-oxidizing archaea (AOA) and complete ammonia oxidizers (comammox) are generally found in oligotrophic environments with low ammonium availability. However, whether AOA and comammox share these habitats or outcompete each other is not well understood. We assessed the competition for ammonium between an AOA and comammox enriched from the freshwater Lake Burr Oak. The AOA enrichment culture (AOA-BO1) contained Nitrosarchaeum sp. BO1 as the ammonia oxidizer and Nitrospira sp. BO1 as the nitrite oxidizer. The comammox enrichment BO4 (cmx-BO4) contained the comammox strain Nitrospira sp. BO4. The competition experiments were performed either in continuous cultivation with ammonium as a growth-limiting substrate or in batch cultivation with initial ammonium concentrations of 50 and 500 µM. Regardless of the ammonium concentration, Nitrospira sp. BO4 outcompeted Nitrosarchaeum sp. BO1 under all tested conditions. The dominance of Nitrospira sp. BO4 could be explained by the ability of comammox to generate more energy through the complete oxidation of ammonia to nitrate and their more efficient carbon fixation pathway-the reductive tricarboxylic acid cycle. Our results are supported by the higher abundance of comammox compared to AOA in the sediment of Lake Burr Oak. IMPORTANCE Nitrification is a key process in the global nitrogen cycle. Aerobic ammonia oxidizers play a central role in the nitrogen cycle by performing the first step of nitrification. Ammonia-oxidizing archaea (AOA) and complete ammonia oxidizers (comammox) are the dominant nitrifiers in environments with low ammonium availability. While AOA have been studied for almost 20 years, comammox were only discovered 8 years ago. Until now, there has been a gap in our understanding of whether AOA and comammox can co-exist or if one strain would be dominant under ammonium-limiting conditions. Here, we present the first study characterizing the competition between freshwater AOA and comammox under varying substrate concentrations. Our results will help in elucidating the niches of two key nitrifiers in freshwater lakes.