Abstract
BackgroundRh50 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.ResultsHere, 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.ConclusionsThe 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.
Highlights
Rh50 proteins belong to the family of ammonia permeases together with their ammonium transporters (Amt)/MEP homologs
The analyses suggest that (i) branch 103, leading to two euryarchaeal methanogens (M. intestinalis, M. luminyensis) is found to be the preferential donor in the Horizontal gene transfer (HGT) involving T. vaginalis in 0.74 of the gene trees
No documented evidence was available for the presence of RH50 genes in archaea, and only the Rh50 protein from the ammonia-oxidizing bacterium N. europaea (NeRh50) has been characterized as an ammonium permease [17]
Summary
Rh50 proteins belong to the family of ammonia permeases together with their Amt/MEP homologs. Horizontal gene transfer (HGT), the process whereby genetic material is exchanged between unrelated species, has challenged our perception of evolution and the metaphors used to describe it; the interplay between tree-shaped and reticulate-shaped processes provides a more realistic account of evolution, especially in prokaryotes [1, 2]. The protein family denoted Amt/MEP/Rh comprises ammonium transporters, methylamine permeases, and Rh permeases. The biochemical function of Amt proteins as NH3/NH4+ permeases is fairly well established in Matassi BMC Evolutionary Biology (2017) 17:2 bacteria, fungi and plants [12], yet the substrate specificity of Rh50 permeases, be it NH3/NH4+, CO2 or both, is still debated [13, 14]. Along the same reasoning, depending on the cellular and/or external environmental pressures, or on the tissue/organ/species involved, the Rh50 permease would be recruited to facilitate the transport of different gaseous substrates
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