The microbial community structure and nitrogen cycle of high-altitude pristine saline lakes on the Qinghai-Tibetan plateau

Abstract

The nitrogen (N) cycle is the foundation of the biogeochemistry on Earth and plays a crucial role in global climate stability. It is one of the most important nutrient cycles in high-altitude lakes. The biogeochemistry of nitrogen is almost entirely dependent on redox reactions mediated by microorganisms. However, the nitrogen cycling of microbial communities in the high-altitude saline lakes of the Qinghai-Tibet Plateau (QTP), the world's "third pole" has not been investigated extensively. In this study, we used a metagenomic approach to investigate the microbial communities in four high-altitude pristine saline lakes in the Altun mountain on the QTP. We observed that Proteobacteria, Bacteroidota, and Actinobacteriota were dominant in these lakes. We reconstructed 1,593 bacterial MAGs and 8 archaeal MAGs, 1,060 of which were found to contain nitrogen cycle related genes. Our analysis revealed that nitrite reduction, nitrogen fixation, and assimilatory nitrate reduction processes might be active in the lakes. Denitrification might be a major mechanism driving the potential nitrogen loss, while nitrification might be inactive. A wide variety of microorganisms in the lake, dominated by Proteobacteria, participate together in the nitrogen cycle. The prevalence of the dominant taxon Yoonia in these lakes may be attributed to its well-established nitrogen functions and the coupled proton dynamics. This study is the first to systematically investigate the structure and nitrogen function of the microbial community in the high-altitude pristine saline lakes in the Altun mountain on the QTP. As such, it contributes to a better comprehension of biogeochemistry of high-altitude saline lakes.

Keywords: Qinghai-Tibetan plateau; high-altitude pristine saline lakes; metagenome-assembled genomes; metagenomics; nitrogen cycle.

Figure 1

The abundance of functional genes involved in nitrogen cycling. (A) Nitrogen cycle, with the thickness of lines showing gene abundance and dashed lines showing that the genes were not found by annotation. (B) Abundance of nitrogen cycle related pathways. (C) Abundance of nitrogen cycle related genes.

Figure 2

Phylogenetic trees of metagenome-assembled genomes (MAGs). (A) The phylogenetic tree of bacterial MAGs involved in the nitrogen cycle. (B) The phylogenetic tree of archaeal MAGs. Red dots indicate MAGs. The colors of the branches show different phyla. Solid circles on the branches represent bootstrap values ≥70% from 100 replicates. The outer circles show the nitrogen cycle related pathways encoded by each MAG, arranged from the center to the outside: Ammonification, Anammox, Assimilatory nitrate reduction, Denitrification, Dissimilatory nitrate reduction, Nitrification, and Nitrogen fixation.

Figure 3

Species encoding genes with nitrogen cycle functions. (A) Number of MAGs encoding genes with nitrogen cycle functions in each phylum. (B) Abundance of Yoonia (Alphaproteobacteria) encoding nitrogenase in four high-altitude pristine lakes. (C) Number of MAGs encoding nirB, nosZ, and nirK genes in the total of 13 MAGs of Cyclobacterium (Bacteroidota). The dashed lines show that the genes were not found by annotation.

Figure 4

The proposed model of nitrogen metabolism in Yoonia and Cyclobacterium. Nitrogen cycle and coupled carbon cycle, oxidative phosphorylation and transmembrane transporters. A gene was considered to be present in the taxon if it appeared in more than 25% of the MAGs or in high-quality MAGs with greater than 90% completeness. (A) Yoonia. (B) Cyclobacterium.