Abstract
Simple SummaryNitrogen fixation is the process by which nitrogen in the atmosphere is converted into ammonia and other nitrogen-containing organic compounds. It is carried out by a variety of bacteria, including Cyanobacteria. Previous studies have shown that several groups of Cyanobacteria have the ability to fix nitrogen; however, because these groups are scattered throughout the Cyanobacterial lineage, the evolutionary history of nitrogen fixation in these bacteria has not been clarified. In this study, we attempted to identify the origin of nitrogen fixation development in Cyanobacterium by focusing on molybdenum dependent nitrogenase, a major nitrogen fixing enzyme. We compared a phylogenetic tree from 179 species of Cyanobacteria to one generated from nitrogen fixation-related genes. We also compared the genomic locations of those genes. As a result, we found that nitrogen fixing genes were acquired in the Cyanobacterium common ancestor and subsequently lost in some lineages. The results demonstrate that inconsistencies between species phylogeny and organism characteristics can occur and be caused not only by horizontal gene transfer, but also by gene deletion.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.
Highlights
Nitrogen fixation is the biochemical process by which the atmospheric nitrogen is converted to nitrogen-containing compounds including assimilation into organic compounds as part of the nitrogen cycle
We identified the operon structures of the nif genes in each genome and performed a phylogenetic analysis of the proteins encoded by each operon structure to examine the reasons for the mosaic distribution of diazotrophic Cyanobacteria
This genus consists of primitive Cyanobacteria in which a portion of the genes related to the thylakoid membranes and photochemical systems I and II are not present, and it has been previously suggested to be the first branch from the common ancestor of Cyanobacteria [21]
Summary
Nitrogen fixation is the biochemical process by which the atmospheric nitrogen is converted to nitrogen-containing compounds including assimilation into organic compounds as part of the nitrogen cycle. Diazotrophic species are present in multiple phyla of bacteria and archaea [1]. Genes encoding nitrogen fixation enzymes are categorized into five groups (I–V) [2]. The genes related to nitrogen fixation such as nifH and nifD are conserved among species in different phyla of both bacteria and archaea [2,3]. Some nif operons have been lost, duplicated, or horizontally transferred [4,5], many are conserved among these phyla [2]. These results indicate that nif genes originated from a common ancestor [6]
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