The Evolution of Molybdenum Dependent Nitrogenase in Cyanobacteria

Abstract

Nitrogen fixation plays a crucial role in the nitrogen cycle by helping to convert nitrogen into a form usable by other organisms. Bacteria capable of fixing nitrogen are found in six phyla including Cyanobacteria. Molybdenum dependent nitrogenase (nif) genes are thought to share a single origin as they have homologs in various phyla. However, diazotrophic bacteria have a mosaic distribution within the cyanobacterial lineage. Therefore, the aim of this study was to determine the cause of this mosaic distribution. We identified nif gene operon structures in the genomes of 85 of the 179 cyanobacterial strains for which whole genome sequences were available. Four nif operons were conserved in each diazotroph Cyanobacterium, although there were some gene translocations and insertions. Phylogenetic inference of these genes did not reveal horizontal gene transfer from outside the phylum Cyanobacteria. These results support the hypothesis that the mosaic distribution of diazotrophic bacteria in the cyanobacterial lineage is the result of the independent loss of nif genes inherited from common cyanobacterial ancestors in each lineage.

Keywords: cyanobacteria; evolution; horizontal gene transfer; nitrogen fixation; nitrogen fixation-related genes.

Figure 1

Phylogenetic tree of 179 Cyanobacteria species. The phylogenetic tree was inferred using the concatenated sequences. Some of the phylogenetic relationships among species are compressed in Figure 1, but the complete phylogenetic tree is shown in Figure S1. Black squares indicate diazotrophic Cyanobacteria. Diazotrophic Cyanobacteria belonging to groups I–V are shown in brackets. Diazotrophic cyanobacteria with no closely related species were not included in the groups. Bootstrap values are shown at the internal branches (<100).

Figure 2

Operon structures of Cyanobacteria nif genes. The nif operon structures of Leptolyngbya boryana dg5, Aulosira laxa NIES-50, and Anabaena sp. YBS01 are shown. Blue, red, green, and orange arrows indicate the nifVZT, nifHDK, nifBSU, and nifENXW operons, respectively. White arrows indicate the genes unrelated to nitrogen fixation.