Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization

BackgroundNickel (Ni) and cobalt (Co) are trace elements required for a variety of biological processes. Ni is directly coordinated by proteins, whereas Co is mainly used as a component of vitamin B12. Although a number of Ni and Co-dependent enzymes have been characterized, systematic evolutionary analyses of utilization of these metals are limited.ResultsWe carried out comparative genomic analyses to examine occurrence and evolutionary dynamics of the use of Ni and Co at the level of (i) transport systems, and (ii) metalloproteomes. Our data show that both metals are widely used in bacteria and archaea. Cbi/NikMNQO is the most common prokaryotic Ni/Co transporter, while Ni-dependent urease and Ni-Fe hydrogenase, and B12-dependent methionine synthase (MetH), ribonucleotide reductase and methylmalonyl-CoA mutase are the most widespread metalloproteins for Ni and Co, respectively. Occurrence of other metalloenzymes showed a mosaic distribution and a new B12-dependent protein family was predicted. Deltaproteobacteria and Methanosarcina generally have larger Ni- and Co-dependent proteomes. On the other hand, utilization of these two metals is limited in eukaryotes, and very few of these organisms utilize both of them. The Ni-utilizing eukaryotes are mostly fungi (except saccharomycotina) and plants, whereas most B12-utilizing organisms are animals. The NiCoT transporter family is the most widespread eukaryotic Ni transporter, and eukaryotic urease and MetH are the most common Ni- and B12-dependent enzymes, respectively. Finally, investigation of environmental and other conditions and identity of organisms that show dependence on Ni or Co revealed that host-associated organisms (particularly obligate intracellular parasites and endosymbionts) have a tendency for loss of Ni/Co utilization.ConclusionOur data provide information on the evolutionary dynamics of Ni and Co utilization and highlight widespread use of these metals in the three domains of life, yet only a limited number of user proteins.

[1]  B. Beatrix,et al.  Cloning, sequencing and expression of the gene encoding the coenzyme B12-dependent 2-methyleneglutarate mutase from Clostridium barkeri in Escherichia coli. , 1994, European journal of biochemistry.

[2]  P. C. Wensink,et al.  One Protein, Two Enzymes* , 1999, The Journal of Biological Chemistry.

[3]  M. Mandrand-Berthelot,et al.  Nickel transport systems in microorganisms , 2000, Archives of Microbiology.

[4]  K. Ito,et al.  Crystal structure of cobalt-containing nitrile hydratase. , 2001, Biochemical and biophysical research communications.

[5]  Eugene V Koonin,et al.  On the origin of genomes and cells within inorganic compartments , 2005, Trends in Genetics.

[6]  W. Doolittle,et al.  The nature of the universal ancestor and the evolution of the proteome. , 2000, Current opinion in structural biology.

[7]  J. Stubbe,et al.  Cloning, sequencing, and expression of the adenosylcobalamin-dependent ribonucleotide reductase from Lactobacillus leichmannii. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Pietro Liò,et al.  Investigating the relationship between genome structure, composition, and ecology in prokaryotes. , 2002, Molecular biology and evolution.

[9]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[10]  Qun Liu,et al.  Crystal structure of 3‐hydroxyanthranilic acid 3,4‐dioxygenase from Saccharomyces cerevisiae: A special subgroup of the type III extradiol dioxygenases , 2006, Protein science : a publication of the Protein Society.

[11]  E. Garber,et al.  The genetics and biochemistry of urease in Ustilago violacea , 1981, Biochemical Genetics.

[12]  T. Bobik,et al.  Cobalamin (coenzyme B12): synthesis and biological significance. , 1996, Annual review of microbiology.

[13]  D. Niegowski,et al.  The CorA family: Structure and function revisited , 2007, Cellular and Molecular Life Sciences.

[14]  D. Salt,et al.  Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Ruma Banerjee,et al.  The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. , 2003, Annual review of biochemistry.

[16]  Long-Fei Wu,et al.  The nik operon of Escherichia coli encodes a periplasmic binding‐protein‐dependent transport system for nickel , 1993, Molecular microbiology.

[17]  J. Robertus,et al.  Purification and properties of cobalamin-independent methionine synthase from Candida albicans and Saccharomyces cerevisiae. , 2005, Archives of biochemistry and biophysics.

[18]  S. Shimizu,et al.  Selective transport of divalent cations by transition metal permeases: the Alcaligenes eutrophus HoxN and the Rhodococcus rhodochrous NhlF , 1999, Archives of Microbiology.

[19]  S. Shima,et al.  Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. , 1997, Science.

[20]  A. Kidera,et al.  Nickel binding to NikA: an additional binding site reconciles spectroscopy, calorimetry and crystallography. , 2007, Acta crystallographica. Section D, Biological crystallography.

[21]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[22]  M. Gelfand,et al.  Comparative Genomics of the Vitamin B12 Metabolism and Regulation in Prokaryotes* , 2003, Journal of Biological Chemistry.

[23]  D. Rees,et al.  The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Johannes Söding,et al.  The HHpred interactive server for protein homology detection and structure prediction , 2005, Nucleic Acids Res..

[25]  Harvard Medical School,et al.  Characterization of the cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium , 1993, Journal of bacteriology.

[26]  M. Kobayashi,et al.  Cobalt proteins. , 1999, European journal of biochemistry.

[27]  Yan Zhang,et al.  Dynamic evolution of selenocysteine utilization in bacteria: a balance between selenoprotein loss and evolution of selenocysteine from redox active cysteine residues , 2006, Genome Biology.

[28]  T. Cooper,et al.  Urea carboxylase and allophanate hydrolase are components of a multifunctional protein in yeast. , 1982, The Journal of biological chemistry.

[29]  B. Lahner,et al.  The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. , 2004, The Plant journal : for cell and molecular biology.

[30]  Dieter Söll,et al.  The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Visser,et al.  Cloning of a prolidase gene from Aspergillusnidulans and characterisation of its product , 2002, Molecular Genetics and Genomics.

[32]  T. Eitinger,et al.  Heterologous production and characterization of bacterial nickel/cobalt permeases. , 2004, FEMS microbiology letters.

[33]  T. Bobik,et al.  Biochemistry of coenzyme B12-dependent glycerol and diol dehydratases and organization of the encoding genes. , 1998, FEMS microbiology reviews.

[34]  K. Moremen,et al.  Insect Cells Encode a Class II α-Mannosidase with Unique Properties* , 2001, The Journal of Biological Chemistry.

[35]  P. Ludden,et al.  Nickel-binding proteins , 1999, Cellular and Molecular Life Sciences CMLS.

[36]  Mathew D Heath,et al.  NikA binds heme: a new role for an Escherichia coli periplasmic nickel-binding protein. , 2007, Biochemistry.

[37]  S. Ragsdale,et al.  The metalloclusters of carbon monoxide dehydrogenase/acetyl-CoA synthase: a story in pictures , 2004, JBIC Journal of Biological Inorganic Chemistry.

[38]  U. Hellman,et al.  Euglena gracilis Ribonucleotide Reductase , 2006, Journal of Biological Chemistry.

[39]  J. M. Sequeira,et al.  The binding properties of the human receptor for the cellular uptake of vitamin B12. , 2005, Biochemical and biophysical research communications.

[40]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[41]  R. Thauer,et al.  Methanol:coenzyme M methyltransferase from Methanosarcina barkeri -- substitution of the corrinoid harbouring subunit MtaC by free cob(I)alamin. , 1999, European journal of biochemistry.

[42]  Inna Dubchak,et al.  Reconstruction of regulatory and metabolic pathways in metal-reducing δ-proteobacteria , 2004, Genome Biology.

[43]  J. A. Smith,et al.  Secondary Transporters for Nickel and Cobalt Ions: Theme and Variations , 2005, Biometals.

[44]  J. Escalante‐Semerena,et al.  The biosynthesis of adenosylcobalamin (vitamin B12). , 2002, Natural product reports.

[45]  M. Stone,et al.  Active monomeric and dimeric forms of Pseudomonas putida glyoxalase I: evidence for 3D domain swapping. , 1998, Biochemistry.

[46]  M. Gelfand,et al.  Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters , 2006, Journal of bacteriology.

[47]  B. Brito,et al.  Molecular and functional characterization of the Azorhizobium caulinodans ORS571 hydrogenase gene cluster. , 2004, FEMS microbiology letters.

[48]  B. Matthews,et al.  Structure and function of the methionine aminopeptidases. , 2000, Biochimica et biophysica acta.

[49]  G. Gottschalk,et al.  The Na(+)-translocating methyltransferase complex from methanogenic archaea. , 2001, Biochimica et biophysica acta.

[50]  R. Burne,et al.  Identification and Characterization of the Nickel Uptake System for Urease Biogenesis in Streptococcus salivarius 57.I , 2003, Journal of bacteriology.

[51]  K. Colabroy,et al.  Structural studies on 3-hydroxyanthranilate-3,4-dioxygenase: the catalytic mechanism of a complex oxidation involved in NAD biosynthesis. , 2005, Biochemistry.

[52]  Weiwen Zhang,et al.  MeaA, a Putative Coenzyme B12-Dependent Mutase, Provides Methylmalonyl Coenzyme A for Monensin Biosynthesis in Streptomyces cinnamonensis , 2001, Journal of bacteriology.

[53]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[54]  J. Palacios,et al.  Nucleotide sequence and characterization of four additional genes of the hydrogenase structural operon from Rhizobium leguminosarum bv. viciae , 1992, Journal of bacteriology.

[55]  A. Plückthun,et al.  An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif. , 1994, The Journal of biological chemistry.

[56]  B. Mannervik,et al.  Optimized heterologous expression of the human zinc enzyme glyoxalase I. , 1996, The Biochemical journal.

[57]  R. Banerjee B12 trafficking in mammals: A for coenzyme escort service. , 2006, ACS chemical biology.

[58]  W. D. de Vos,et al.  Two distinct enzyme systems are responsible for tetrachloroethene and chlorophenol reductive dehalogenation in Desulfitobacterium strain PCE1 , 2001, Archives of Microbiology.

[59]  E. Denkhaus,et al.  Nickel essentiality, toxicity, and carcinogenicity. , 2002, Critical reviews in oncology/hematology.

[60]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[61]  R. Bradshaw,et al.  Yeast methionine aminopeptidase I can utilize either Zn2+ or Co2+ as a cofactor: A case of mistaken identity? , 1998, Protein science : a publication of the Protein Society.

[62]  M. Gelfand,et al.  A Novel Class of Modular Transporters for Vitamins in Prokaryotes , 2008, Journal of bacteriology.

[63]  R. Banerjee,et al.  Radical peregrinations catalyzed by coenzyme B12-dependent enzymes. , 2001, Biochemistry.

[64]  R. Pickersgill,et al.  Anaerobic synthesis of vitamin B12: characterization of the early steps in the pathway. , 2005, Biochemical Society transactions.

[65]  Yan Zhang,et al.  Molybdoproteomes and evolution of molybdenum utilization. , 2008, Journal of molecular biology.

[66]  D. Kuntz,et al.  Comparison of kifunensine and 1-deoxymannojirimycin binding to class I and II alpha-mannosidases demonstrates different saccharide distortions in inverting and retaining catalytic mechanisms. , 2003, Biochemistry.

[67]  J. MacInnes,et al.  Novel Genes Affecting Urease Activity inActinobacillus pleuropneumoniae , 2001, Journal of bacteriology.

[68]  R. Kinach,et al.  Overproduction and characterization of a dimeric non-zinc glyoxalase I from Escherichia coli: evidence for optimal activation by nickel ions. , 1998, Biochemistry.

[69]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[70]  O. Degen,et al.  Nic1p, a Relative of Bacterial Transition Metal Permeases inSchizosaccharomyces pombe, Provides Nickel Ion for Urease Biosynthesis* , 2000, The Journal of Biological Chemistry.

[71]  R. Pejchal,et al.  Cobalamin-Independent Methionine Synthase (MetE): A Face-to-Face Double Barrel That Evolved by Gene Duplication , 2004, PLoS biology.

[72]  N. Russo,et al.  Which one among Zn(II), Co(II), Mn(II), and Fe(II) is the most efficient ion for the methionine aminopeptidase catalyzed reaction? , 2007, Journal of the American Chemical Society.

[73]  James Thomas,et al.  COMPARATIVE AND FUNCTIONAL GENOMIC ANALYSIS OF , 2007 .

[74]  R. Hausinger,et al.  Nickel uptake and utilization by microorganisms. , 2003, FEMS microbiology reviews.

[75]  W. Köster ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. , 2001, Research in microbiology.

[76]  Eduardo P C Rocha,et al.  Base composition bias might result from competition for metabolic resources. , 2002, Trends in genetics : TIG.

[77]  Seigo Shima,et al.  Methyl-coenzyme M reductase and the anaerobic oxidation of methane in methanotrophic Archaea. , 2005, Current opinion in microbiology.

[78]  A. Banerjee,et al.  The nitrile-degrading enzymes: current status and future prospects. , 2002, Applied microbiology and biotechnology.

[79]  M. Mandrand-Berthelot,et al.  Genes Encoding Specific Nickel Transport Systems Flank the Chromosomal Urease Locus of Pathogenic Yersiniae , 2002, Journal of bacteriology.

[80]  Jeffrey E. Barrick,et al.  Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. , 2004, Nucleic acids research.

[81]  B. Seetharam,et al.  Cellular import of cobalamin (Vitamin B-12). , 1999, The Journal of nutrition.

[82]  J. Honek,et al.  Distinct classes of glyoxalase I: metal specificity of the Yersinia pestis, Pseudomonas aeruginosa and Neisseria meningitidis enzymes. , 2004, The Biochemical journal.

[83]  M. Lindenmeyer,et al.  Aerobic synthesis of vitamin B12: ring contraction and cobalt chelation. , 2005, Biochemical Society transactions.

[84]  S. Michel,et al.  Microbial nickel metalloregulation: NikRs for nickel ions. , 2006, Current opinion in chemical biology.

[85]  O. Degen,et al.  Substrate Specificity of Nickel/Cobalt Permeases: Insights from Mutants Altered in Transmembrane Domains I and II , 2002, Journal of bacteriology.

[86]  Inna Dubchak,et al.  Reconstruction Of Regulatory And Metabolic Pathways In Metal-Reducing delta-Proteobacteria , 2004 .