Horizontal gene transfer drives the evolution of Rh50 permeases in prokaryotes

Giorgio Matassi

Rh50 proteins belong to the family of ammonia permeases together with their Amt/MEP homologs. Ammonia permeases increase the permeability of NH3/NH4(+) across cell membranes and are believed to be involved in excretion of toxic ammonia and in the maintenance of pH homeostasis. RH50 genes are widespread in eukaryotes but absent in land plants and fungi, and remarkably rare in prokaryotes. The evolutionary history of RH50 genes in prokaryotes is just beginning to be unveiled. Here, a molecular phylogenetic approach suggests horizontal gene transfer (HGT) as a primary force driving the evolution and spread of RH50 among prokaryotes. In addition, the taxonomic distribution of the RH50 gene among prokaryotes turned out to be very narrow; a single-copy RH50 is present in the genome of only a small proportion of Bacteria, and, first evidence to date, in only three methanogens among Euryarchaea. The coexistence of RH50 and AMT in prokaryotes seems also a rare event. Finally, phylogenetic analyses were used to reconstruct the HGT network along which prokaryotic RH50 evolution has taken place. The eukaryotic or bacterial "origin" of the RH50 gene remains unsolved. The RH50 prokaryotic HGT network suggests a preferential directionality of transfer from aerobic to anaerobic organisms. The observed HGT events between archaeal methanogens, anaerobic and aerobic ammonia-oxidizing bacteria suggest that syntrophic relationships play a major role in the structuring of the network, and point to oxygen minimum zones as an ecological niche that might be of crucial importance for HGT-driven evolution.