Trophic status and local conditions affect microbial potential for denitrification versus internal nitrogen cycling in lake sediments

Abstract

The nitrogen (N) cycle is of global importance as N is an essential element and a limiting nutrient in terrestrial and aquatic ecosystems. Excessive anthropogenic N fertilizer usage threatens sensitive downstream aquatic ecosystems. Although freshwater lake sediments remove N through various microbial transformation processes, few studies have investigated the microbial communities involved. In an integrated biogeochemical and microbiological study on a eutrophic and oligotrophic lake, we estimated N removal rates in the sediments from porewater concentration gradients. Simultaneously, the abundance of different microbial N transformation genes was investigated using metagenomics on a seasonal and spatial scale. We observed that contrasting nutrient concentrations in the sediments were reflected in distinct microbial community compositions and significant differences in the abundance of various N transformation genes. Within each lake, we observed a more pronounced spatial than seasonal variability. The eutrophic Lake Baldegg showed a higher denitrification potential with higher nosZ gene (N2O reductase) abundance and higher nirS:nirK (nitrite reductase) ratio, indicating a greater capacity for complete denitrification. Correspondingly, this lake had a higher N removal efficiency. The oligotrophic Lake Sarnen, in contrast, had a higher potential for DNRA and nitrification, and specifically a high abundance of Nitrospirae, including some capable of comammox. In general, the oligotrophic lake ecosystems had a higher microbial diversity, thus acting as an important habitat for oligotrophic microbes. Our results demonstrate that knowledge of the genomic N transformation potential is important for interpreting N process rates and understanding the limitations of the N cycle response to environmental drivers. Importance{paragraph}Anthropogenic nitrogen (N) inputs can lead to eutrophication in aquatic systems, specifically in N limited coastal ecosystems. Lakes act as N sinks by transforming reactive N to N2 through denitrification or anammox. The N cycle in lake sediments is mediated by microbial processes and affected by environmental drivers such as the amount and quality of settling organic material or nitrate concentration. However, the microbial communities mediating the different N transformation processes and their impact on N removal in freshwater lake sediments remain largely unknown. We provide the first seasonally and spatially resolved metagenomic analysis of the N cycle in the sediments of two lakes with different trophic states. We show that the trophic state of lakes provokes other microbial communities with characteristic key players and functional potential for N transformation.