Effect of Molybdenum on The Activity of Molybdoenzymes

Main Article Content


N.N. Iksat

Department of Biotechnology and Microbiology, L.N. Gumilyov Eurasian National University, 13, Kazhymukan street, Nur-Sultan, 010000, Kazakhstan

S.B. Zhangazin

Department of Biotechnology and Microbiology, L.N. Gumilyov Eurasian National University, 13, Kazhymukan street, Nur-Sultan, 010000, Kazakhstan

A.A. Madirov

Department of Biotechnology and Microbiology, L.N. Gumilyov Eurasian National University, 13, Kazhymukan street, Nur-Sultan, 010000, Kazakhstan

R.T. Omarov

Department of Biotechnology and Microbiology, L.N. Gumilyov Eurasian National University, 13, Kazhymukan street, Nur-Sultan, 010000, Kazakhstan


The soil is a reservoir of various contaminants with heavy metals and has a strong cation exchange property. Among these heavy metals, molybdenum is an essential element that is required in small quantities for optimal plant growth and development. This useful heavy metal performs several biochemical and physiological tasks in plants and is also considered as an important component of various cellular enzymes and is actively involved in redox reactions. Mononuclear molybdenum-containing enzymes, as a rule, have a certain conserved metal center, coordinated by one or two pyranopterins. The pyranopterin fragment plays a key role in the properties of the metal site in the group of mononuclear enzymes of molybdenum with various functions: coordination; stabilization and modulation of the redox transitions of the center, acting as a redox buffer; and for redox regulation/compliance in a variety of catalytic reactions. The coordination sphere of the metal is equipped with oxygen and/or sulfur, selenium atoms in various forms. Tungsten is an antagonist of molybdenum and inhibits molybdoenzymes. In the current review we elaborately reviewed various studies regarding heavy metals - molybdenum and tungsten, their uptake mechanism, essential transporters, and also discuss about the destructive properties of heavy metals in response to their concentration.


molybdenum, molybdoenzyme, molybdenum cofactor, tungsten, xanthine dehydrogenase, aldehyde oxidase

Article Details


Maupin-Furlow J. A. [et al.]. Genetic analysis of the modABCD (molybdate transport) operon of Escherichia coli. Journal of bacteriology, 1995, vol. 177, no. 17, pp. 4851–4856.

Tejada-Jimenez M. [et al.]. A high-affinity molybdate transporter in eukaryotes Proceedings of the National Academy of Sciences, 2007, vol. 104, no. 50, pp. 20126–20130.

Tejada-Jimenez M., Galvan A., Fernandez E. Algae and humans share a molybdate transporter. Proceedings of the National Academy of Sciences, 2011, vol. 108, no. 16, pp. 6420–6425.

Wichard T. [et al.]. Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nature Geoscience, 2009, vol.2, no. 9, pp. 625–629.

Arnon D. I. Molybdenum as an essential element for higher plants. Plant physiology, 1939 , vol.14, no. 3, pp. 599–602. Crossref

Walker R.B. Molybdenum Deficiency in Serpentine Barren Soils. Science, New Series, 1948, vol. 108, no. 2809, pp. 473-475.

Schwarz G., Mendel R. R. Molybdenum cofactor biosynthesis and molybdenum enzymes. Annual Review of Plant Biology, 2006. vol.57, no. 1, pp. 623–647.

Rothery R. A. [et al.]. Pyranopterin conformation defines the function of molybdenum and tungsten enzymes. Proceedings of the National Academy of Sciences of the United States of America, 2012, vol.109, no. 37, pp. 14773–14778.

Rajagopalan K. V., Johnson Jean L. The Pterin Molybdenum Cofactors. The Journal of Biological Chemistry, 1992, vol. 267, no.15, pp.10199-10202.

Chan M. K. [et al.]. Structure of a Hyperthermophilic Tungstopterin Enzyme, Aldehyde Ferredoxin Oxidoreductase. Science, New Series, 1995, vol. 267, no. 5203, pp. 1463–1469.

Fischer B. [et al.]. Models for the Active Center of Pterin-Containing Molybdenum Enzymes: Crystal structure of a molybdenum complex with sulfur and pterin ligands. Helvetica Chimica Acta, 1997, vol.80, no. 1, pp. 103–110.

Schwarz G., Mendel R. R., Ribbe M. W. Molybdenum cofactors, enzymes and pathways. Nature, 2009, vol. 460, no. 7257, pp. 839–847.

Havemeyer A., Bittner F., Wollers S., Mendel R., Kunze T., Clement B. Identification of the Missing Component in the Mitochondrial Benzamidoxime Prodrug-converting System as a Novel Molybdenum Enzyme. The journal of biological chemistry, 2006, vol. 281, no. 46, pp. 34796–34802.

Teschner J., Lachmann N., Schulze J., Geisler M., Selbach K., Santamaria-Araujo J., Balk J., Mendel R.R., Bittner F. A Novel Role for Arabidopsis Mitochondrial ABC Transporter ATM3 in Molybdenum Cofactor Biosynthesis. The Plant Cell, 2010, vol. 22, pp. 468–480.

Matthies A., Rajagopalan K. V., Mendel Ralf R. and Leimkuhler S. Evidence for the physiological role of a rhodanese-like protein for the biosynthesis of the molybdenum cofactor in humans. PNAS, 2004, vol. 101, no. 16, pp. 5946–5951. doi/10.1073/pnas.0308191101.

Kuper J. [et al.]. The active site of the molybdenum cofactor biosynthetic

protein domain Cnx1G. Archives of Biochemistry and Biophysics, 2003, pp. 36–46, doi:10.1016/S0003-9861(02)00714-2.

Angel Llamas, Tanja Otte, Gerd Multhaup, Ralf R. Mendel and Guenter Schwarz. The Mechanism of Nucleotide-assisted Molybdenum Insertion into Molybdopterin: A novel route toward metal cofactor assembly. J. Biol. Chem. 2006, 281, pp. 18343-18350, doi: 10.1074/jbc.M601415200.

Gasber A. [et al.]. Identification of an Arabidopsis solute carrier critical for

intracellular transport and inter-organ allocation of molybdate. Plant Biology, 2011, pp. 710–718, doi:10.1111/j.1438-8677.2011.00448.x.

Mendel R. R. Molybdoenzymes and molybdenum cofactor in plants. Journal of Experimental Botany, 2002, vol.53, no. 375, pp. 1689–1698.

Mendel R. R. Biology of the molybdenum cofactor. Journal of Experimental Botany, 2007, vol. 58, no. 9, pp. 2289–2296.

Turner N. A., Bray R. C., Diakun G. P. Information from e.x.a.f.s. spectroscopy on the structures of different forms of molybdenum in xanthine oxidase and the catalytic mechanism of the enzyme. Biochemical Journal, 1989, vol.260, no. 2, pp. 563–571.

Vorbach C., Harrison R., Capecchi M. R. Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends in Immunology, 2003, vol.24, no. 9, pp. 512–517.

Nishino T. [et al]. Mammalian xanthine oxidoreductase - mechanism of transition from xanthine dehydrogenase to xanthine oxidase: Mammalian xanthine oxidoreductase. FEBS Journal, 2008, vol. 275, no. 13, pp. 3278–3289.

Yesbergenova Z. [et al]. The plant Mo-hydroxylases aldehyde oxidase and xanthine dehydrogenase have distinct reactive oxygen species signatures and are induced by drought and abscisic acid: ROS production by plant Mo-hydroxylases. The Plant Journal, 2005, vol. 42, no. 6, pp. 862–876.

Montalbini P., Della Torre G. Evidence of a two-fold mechanism responsible for the inhibition by allopurinol of the hypersensitive response induced in tobacco by tobacco necrosis virus. Physiological and Molecular Plant Pathology, 1996, vol.48, no. 4, pp. 273–287.

Pastori G. M., Rio L. A. del Natural Senescence of Pea Leaves (An Activated Oxygen-Mediated Function for Peroxisomes). Plant Physiology, 1997, vol.113, no. 2, pp. 411–418.

Rodriguez-Trelles F., Tarrio R., Ayala F. J. Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene. Proceedings of the National Academy of Sciences, 2003, vol.100, no. 23, pp. 13413–13417.

Seo M. [et al.]. Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. The Plant Journal, 2000, vol. 23, no. 4, pp. 481–488.

Sagi M., Scazzocchio C., Fluhr R. The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants: MoCo sulfurase in flacca tomato mutant. The Plant Journal, 2002, vol. 31, no. 3, pp. 305–317.

Drechsel G., Raab S., Hoth S. Arabidopsis zinc-finger protein 2 is a negative regulator of ABA signaling during seed germination. Journal of Plant Physiology, 2010, vol. 167, no. 16, pp. 1418–1421.

Bittner F. Molybdenum metabolism in plants and crosstalk to iron. Frontiers in Plant Science, 2014, vol. 5, no. 28. doi: 10.3389/fpls.2014.00028.

Batyrshina Z. [et al.]. Differential influence of molybdenum and tungsten on the growth of barley seedlings and the activity of aldehyde oxidase under salinity. Journal of Plant Physiology, 2018, no. 228, pp. 189-196.

W.R. Hagen and A.E Arendsen. The Bio-lnorganic Chemistry of Tungsten. Structure and Bonding, vol. 90, 1998, pp. 162-191.

Lee H.-S., Milborrow B. V. Endogenous Biosynthetic Precursors of (+)-Abscisic Acid. V. Inhibition by Tungstate and its Removal by Cinchonine shows that Xanthoxal is Oxidised by a Molybdo-Aldehyde Oxidase. Functional Plant Biology, 1997, vol. 24, no.6, p. 727.

Hauke Hansen and Klaus Grossmann. Auxin-Induced Ethylene Triggers Abscisic Acid Biosynthesis and Growth Inhibition. Plant Physiol., vol. 124, 2000, pp. 1437-1448.

Zeller M., Hunter A.D. Crystal structure of molybdenum and tungsten trans-bis(dinitrogen)-bis{di(p-ethylbenzene)phosphino)ethane} toluene solvate, M(C34H40P2)2(N2)2*C7H8(M=Mo,W). Kristallogr. NCS, 2004, 219, pp. 249-254.

Maurya A. K., Rani A. Nitric Oxide (NO) and Physio-biochemical Adaptation in Plants Against Stress. Springer Singapore, 2017, pp. 347–386.

Preiner J. [et al.]. Molecular Mechanisms of Tungsten Toxicity Differ for Glycine max Depending on Nitrogen Regime. Frontiers in Plant Science, 2019, vol. 10, p. 367.

Vega J. M. Nitrogen and Sulfur Metabolism in Microalgae and Plants: 50 Years of Research Progress in Botany. Springer International Publishing, 2018, pp. 1–40.

Habib U., Hoffman M. Effect of molybdenum and tungsten on the reduction of nitrate in nitrate reductase, a DFT study. Chemistry Central Journal, 2017, vol.11, no. 1, p. 35.

Nancy Klein Amy, Reginald H. Garrett. Immunoelectrophoretic Determination of Nitrate Reductase in Neurospora crassa I. Analytical biochemistry, 1979, pp. 97-107

Jones H.P. [et al.]. In vitro reconstitution of demolybdosulfite oxidase by molybdate. The Journal of Biological Chemistry, 1977, no.14, pp. 4988-4993.

Kumar A., Aery N. C. Effect of tungsten on growth, biochemical constituents, molybdenum and tungsten contents in wheat. Plant, Soil and Environment, 2011, vol. 57, no. 11, pp. 519–525.

Chamizo-Ampudia A. [et al.]. Nitrate Reductase Regulates Plant Nitric Oxide Homeostasis. Trends in Plant Science, 2017, vol. 22, no. 2, pp. 163–174.

Hochheimer A. [et al.]. The Molybdenum Formylmethanofuran Dehydrogenase Operon and the Tungsten Formylmethanofuran Dehydrogenase Operon from Methanobacterium Thermoautotrophicum. Structures and Transcriptional Regulation. European Journal of Biochemistry, 1996, vol. 242, no. 1, pp. 156–162.

Cho S. [et al.]. Stimulation of cell growth by addition of tungsten in batch culture of a methanotrophic bacterium, Methylomicrobium alcaliphilum 20Z on methane and methanol. Journal of Biotechnology, 2020, vol. 309, pp. 81–84.

Jie Xiong, Guanfu Fu, Yongjie Yang, Cheng Zhu and Longxing Tao. Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? Journal of Experimental Botany, 2011, pp. 1-9, doi:10.1093/jxb/err268.

James E. Harper and Joseph C. Nicholas. Nitrogen Metabolism of Soybeans. Plant Physiol., 1978, pp. 662-664.

Nikolay Strigul, Agamemnon Koutsospyros, Christos Christodoulatos. Tungsten speciation and toxicity: Acute toxicity of mono- and poly-tungstates to fish. Ecotoxicology and Environmental Safety, 2010, pp. 164–171.

Loes E. Bevers, Peter-Leon Hagedoorn, Wilfred R. Hagen. The bioinorganic chemistry of tungsten. Coordination Chemistry Reviews, 2009, pp. 269–290.