Comparative genomics of molybdenum utilization in prokaryotes and eukaryotes

Abstract

BackgroundMolybdenum (Mo) is an essential micronutrient for almost all biological systems, which holds key positions in several enzymes involved in carbon, nitrogen and sulfur metabolism. In general, this transition metal needs to be coordinated to a unique pterin, thus forming a prosthetic group named molybdenum cofactor (Moco) at the catalytic sites of molybdoenzymes. The biochemical functions of many molybdoenzymes have been characterized; however, comprehensive analyses of the evolution of Mo metabolism and molybdoproteomes are quite limited.ResultsIn this study, we analyzed almost 5900 sequenced organisms to examine the occurrence of the Mo utilization trait at the levels of Mo transport system, Moco biosynthetic pathway and molybdoproteins in all three domains of life. A global map of Moco biosynthesis and molybdoproteins has been generated, which shows the most detailed understanding of Mo utilization in prokaryotes and eukaryotes so far. Our results revealed that most prokaryotes and all higher eukaryotes utilize Mo whereas many unicellular eukaryotes such as parasites and most yeasts lost the ability to use this metal. By characterizing the molybdoproteomes of all organisms, we found many new molybdoprotein-rich species, especially in bacteria. A variety of new domain fusions were detected for different molybdoprotein families, suggesting the presence of novel proteins that are functionally linked to molybdoproteins or Moco biosynthesis. Moreover, horizontal gene transfer event involving both the Moco biosynthetic pathway and molybdoproteins was identified. Finally, analysis of the relationship between environmental factors and Mo utilization showed new evolutionary trends of the Mo utilization trait.ConclusionsOur data provide new insights into the evolutionary history of Mo utilization in nature.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5068-0) contains supplementary material, which is available to authorized users.

Coordinated regulation of nitrogen fixation and molybdate transport by molybdenum

“…To cope with Mo limitation, 89% of Mo‐utilizing bacteria, regardless of whether diazotrophic or not, are predicted to synthesize highly efficient ModABC transporters (Peng et al , ). They import molybdate (MoO 4 2– ), the only bioavailable form of molybdenum, to sustain activity of their molybdoenzymes at nanomolar molybdate concentrations in the environment (Zhang and Gladyshev, ).…”

“…Many globally important enzymes in sulfur, carbon and nitrogen metabolism depend on molybdenum (Iobbi-Nivol and Leimkühler, 2013). Molybdoenzymes like sulfite oxidase, formate dehydrogenase, xanthine dehydrogenase, nitrate reductase and nitrogenase are widespread in bacteria, archaea and eukaryotes as indicated by comparative genomics (Zhang and Gladyshev, 2008;Zhang et al, 2011;Peng et al 2018). Apparently, some parasitic protozoa and unicellular fungi including Saccharomyces cerevisiae have lost the ability to utilize Mo during evolution.…”

“…To cope with Mo limitation, 89% of Mo-utilizing bacteria, regardless of whether diazotrophic or not, are predicted to synthesize highly efficient ModABC transporters (Peng et al, 2018). They import molybdate (MoO 4 2-), the only (Hu and Ribbe, 2011;Curatti and Rubio, 2014;Yang et al, 2014;Mendel and Leimkühler, 2015;Hu and Ribbe, 2016;Leimkühler, 2017).…”

Molybdenum Metabolism in Azotobacter vinelandii and its Biotechnological Applications

“…Mo is not biologically active by itself, but it is rather found coordinated by organic pterin molecules in the so-called molybdenum cofactors (Mo-co), which play key roles in the catalytic centers of a wide range of molybdoenzymes relevant to global carbon, sulfur and nitrogen cycles (Zhang et al, 2011;Peng et al, 2018). Hitherto more than 50…”

“…(Tejada-Jiménez et al, 2007), while reduced expression of MOT2 gene resulted in diminished molybdate uptake (Tejada-Jiménez et al, 2011). (Peng et al, 2018).…”