Genomic potential and evolution of Dissimilatory Nitrate Reduction to Ammonium in Cyanobacteria

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Abstract Cyanobacteria play an important role in primary production and nitrogen fixation. Although Cyanobacteria are well-known diazotrophic organisms, their role in other steps Nitrogen Cycle is obscure. Screening of Cyanobacterial genomes from cultured and unculturable species can help identify potentially novel functions. In this study, we assembled Cyanobacterial genomes from metagenomic data generated from environmental DNA isolated from a brackish water lagoon (Chilika, India). We annotated these Cyanobacterial metagenome-assembled genomes (MAG) for all the encoded functions using KEGG Orthology. We found two high-quality Cyanobacterial MAGs containing the nirBD gene and nifH and nifD genes involved in the nitrogen cycle. nirBD encodes for the Dissimilatory Nitrate Reduction to Ammonium (DNRA) activity, a function previously not ascribed to Cyanobacteria. We validated the presence of NirBD in publicly available isolate genomes of Cyanobacteria and examined its evolution in the phylum by phylogenetic reconciliation of species and gene trees. Our analysis revealed that both horizontal gene transfers and speciation events contributed to the dispersal of the nirBD gene in Cyanobacteria. We observed that mostly filamentous Cyanobacteria served as ancestral donors in horizontal gene transfer events. Further, we found that the nirBD gene is under a purifying selection pressure in Cyanobacteria. This study demonstrates the genomic potential and evolution of DNRA activity in Cyanobacteria for the utilisation of nitrate in the ecosystem which can help these organisms to cope with extreme environmental conditions. It expands our overall comprehension of the contribution of Cyanobacteria in the biogeochemical cycling in aquatic ecosystems.

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