Cyanobacterial nitrogenases: phylogenetic diversity, regulation and functional predictions

Abstract

Cyanobacteria is a remarkable group of prokaryotic photosynthetic microorganisms, with several genera capable of fixing atmospheric nitrogen (N2) and presenting a wide range of morphologies. Although the nitrogenase complex is not present in all cyanobacterial taxa, it is spread across several cyanobacterial strains. The nitrogenase complex has also a high theoretical potential for biofuel production, since H2 is a by-product produced during N2 fixation. In this review we discuss the significance of a relatively wide variety of cell morphologies and metabolic strategies that allow spatial and temporal separation of N2 fixation from photosynthesis in cyanobacteria. Phylogenetic reconstructions based on 16S rRNA and nifD gene sequences shed light on the evolutionary history of the two genes. Our results demonstrated that (i) sequences of genes involved in nitrogen fixation (nifD) from several morphologically distinct strains of cyanobacteria are grouped in similarity with their morphology classification and phylogeny, and (ii) nifD genes from heterocytous strains share a common ancestor. By using this data we also discuss the evolutionary importance of processes such as horizontal gene transfer and genetic duplication for nitrogenase evolution and diversification. Finally, we discuss the importance of H2 synthesis in cyanobacteria, as well as strategies and challenges to improve cyanobacterial H2 production.

Reconstruction of Diverse Verrucomicrobial Genomes from Metagenome Datasets of Freshwater Reservoirs

“…Nitrogenase activity is commonly limited to anaerobic environments, where nitrogenase is not inhibited by oxygen, although some aerobic microorganisms like Cyanobacteria ( Esteves-Ferreira et al, 2017 ) or Azotobacter vinelandii ( Bishop et al, 1980 ) present strategies to perform nitrogen fixation under aerobic conditions. The discovery of the nitrogen fixing Verrucomicrobia-Tous-C9LFEB is remarkable since the study site (Tous reservoir) is totally oxic throughout the year.…”

Genome analysis of the freshwater planktonic Vulcanococcus limneticus sp. nov. reveals horizontal transfer of nitrogenase operon and alternative pathways of nitrogen utilization

“…It was reported that in nitrogen-fixing cyanobacteria hydrogen is synthesized as a by-product of nitrogenase activity and is further oxidized by a hydrogenase [ 7 , 8 ]. There are two types of hydrogenases in cyanobacteria: an uptake hydrogenase (HupSL) which catalyses H 2 consumption and is present in almost all nitrogen-fixing strains [ 45 ] and a bidirectional hydrogenase (HoxFUYH) which is involved in both hydrogen synthesis and oxidation but seems to be unrelated to the nitrogen-fixing process [ 46 ].…”

“…Cyanobacteria are the only oxygen producing microorganisms able to perform nitrogen fixation [ 6 ]. Typically, cyanobacterial nitrogenases are organized in different operons, nifB-fdxN-nifSU, nifHDK, nifENXW and nifVZT [ 7 ]. The nitrogenase complex is irreversibly damaged by oxygen, thus diazotrophic microorganisms have developed different strategies to ensure the success of this process.…”

An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean

“…The unicellular, non-heterocystous Chroococcidiopsis thermalis PCC7203 was isolated from a soil sample near Greifswald, Germany (Rippka, Deruelles, Waterbury, Herdman, & Stanier, 1979). While not located in the cyanobacterial basal clade of Sánchez-Baracaldo et al (2014), it is a proposed representative of an ancient cyanobacterial species, with 16S rDNA (Fewer, Friedl, & Büdel, 2002) and nifD (Esteves-Ferreira et al, 2017) gene phylogenies placing it as the nearest single-celled nitrogen fixer to the heterocyst-forming diazotrophs. It carries a nitrogen fixation gene cluster that permits nitrogen fixation only under anoxic conditions (Thiel & Pratte, 2014), is cryptoendolithic (Büdel et al, 2004), with a high UV tolerance (Billi et al, 2011), and is able to withstand harsh desiccation conditions by virtue of the production of copious amounts of EPS and thick cell walls (Caiola, Billi, & Imre Friedmann, 1996).…”