Glutamine versus Ammonia Utilization in the NAD Synthetase Family
Publication Date
June 15, 2012
Journal
PLOS ONE
Authors
Jessica De Ingeniis, Marat D. Kazanov, Konstantin Shatalin, Mikhail S. Gelfand, et al
Volume
7
Issue
6
Pages
e39115
DOI
https://dx.plos.org/10.1371/journal.pone.0039115
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0039115
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22720044
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3376133
Europe PMC
http://europepmc.org/abstract/MED/22720044
Web of Science
000305350000040
Scopus
84862492833
Mendeley
http://www.mendeley.com/research/glutamine-versus-ammonia-utilization-nad-synthetase-family
Events
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Mendeley | Further Information

{"title"=>"Glutamine versus ammonia utilization in the NAD synthetase family", "type"=>"journal", "authors"=>[{"first_name"=>"Jessica", "last_name"=>"de Ingeniis", "scopus_author_id"=>"23995086400"}, {"first_name"=>"Marat D.", "last_name"=>"Kazanov", "scopus_author_id"=>"6506765203"}, {"first_name"=>"Konstantin", "last_name"=>"Shatalin", "scopus_author_id"=>"8786911600"}, {"first_name"=>"Mikhail S.", "last_name"=>"Gelfand", "scopus_author_id"=>"7201803297"}, {"first_name"=>"Andrei L.", "last_name"=>"Osterman", "scopus_author_id"=>"24352765400"}, {"first_name"=>"Leonardo", "last_name"=>"Sorci", "scopus_author_id"=>"7801524464"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"22720044", "sgr"=>"84862492833", "doi"=>"10.1371/journal.pone.0039115", "scopus"=>"2-s2.0-84862492833", "pui"=>"365023666", "isbn"=>"10.1371/journal.pone.0039115", "issn"=>"19326203"}, "id"=>"27546069-b073-3536-9237-c2699b8a57d9", "abstract"=>"NAD is a ubiquitous and essential metabolic redox cofactor which also functions as a substrate in certain regulatory pathways. The last step of NAD synthesis is the ATP-dependent amidation of deamido-NAD by NAD synthetase (NADS). Members of the NADS family are present in nearly all species across the three kingdoms of Life. In eukaryotic NADS, the core synthetase domain is fused with a nitrilase-like glutaminase domain supplying ammonia for the reaction. This two-domain NADS arrangement enabling the utilization of glutamine as nitrogen donor is also present in various bacterial lineages. However, many other bacterial members of NADS family do not contain a glutaminase domain, and they can utilize only ammonia (but not glutamine) in vitro. A single-domain NADS is also characteristic for nearly all Archaea, and its dependence on ammonia was demonstrated here for the representative enzyme from Methanocaldococcus jannaschi. However, a question about the actual in vivo nitrogen donor for single-domain members of the NADS family remained open: Is it glutamine hydrolyzed by a committed (but yet unknown) glutaminase subunit, as in most ATP-dependent amidotransferases, or free ammonia as in glutamine synthetase? Here we addressed this dilemma by combining evolutionary analysis of the NADS family with experimental characterization of two representative bacterial systems: a two-subunit NADS from Thermus thermophilus and a single-domain NADS from Salmonella typhimurium providing evidence that ammonia (and not glutamine) is the physiological substrate of a typical single-domain NADS. The latter represents the most likely ancestral form of NADS. The ability to utilize glutamine appears to have evolved via recruitment of a glutaminase subunit followed by domain fusion in an early branch of Bacteria. Further evolution of the NADS family included lineage-specific loss of one of the two alternative forms and horizontal gene transfer events. Lastly, we identified NADS structural elements associated with glutamine-utilizing capabilities.", "link"=>"http://www.mendeley.com/research/glutamine-versus-ammonia-utilization-nad-synthetase-family", "reader_count"=>25, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>14, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Brazil"=>1, "United Kingdom"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/623484"], "description"=>"<p>Distribution of two-component glutamine-utilizing NADS signature elements across phylogenetic branches.</p>", "links"=>[], "tags"=>["two-component", "glutamine-utilizing", "nads", "elements", "phylogenetic"], "article_id"=>293971, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.t002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_two_component_glutamine_utilizing_NADS_signature_elements_across_phylogenetic_branches_/293971", "title"=>"Distribution of two-component glutamine-utilizing NADS signature elements across phylogenetic branches.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-06-15 01:06:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/623153"], "description"=>"<p>(A) Schematic of <i>S. typhimurium nadE</i> mutant strains. Nit11 mutant features a missense mutation at nucleotide 143 yielding the amino acid substitution AN. SK51 mutant features a single nucleotide deletion (G at position – 51 considering as +1 the first base of the start codon) that is just upstream of the -35 box regulatory region of the promoter. Predicted regulatory sequences are indicated in the bottom line. (B) Relative expression level of <i>nadE</i> in the wild type and in the two classes of mutants <i>nit11</i> (S48N) and SK51 in four different growth conditions: rich medium (1), minimal medium supplemented with 20 mM NH<sub>3</sub> (2), MM supplemented with 5 mM (3) or 20 mM (4) glutamine. (C) Kinetic characterization of wild type and S48N <i>S. typhimurium</i> NAD synthetase. Initial rates were measured by spectrophotometrical coupled (SPEC) assays. The kinetic parameters <i>K</i><sub>m</sub> and <i>k</i><sub>cat</sub> are apparent values determined at fixed (saturating) concentrations of co-substrates. For fixed substrates, concentrations were: 2 mM ATP, 2 mM NaAD, and 40 mM NH<sub>3</sub>. Errors represent standard deviation.</p>", "links"=>[], "tags"=>["nit11", "sk51", "mutant"], "article_id"=>293641, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_Nit11_and_SK51_S_typhimurium_mutant_strains_/293641", "title"=>"Analysis of Nit11 and SK51 <i>S. typhimurium</i> mutant strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 01:00:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/623443"], "description"=>"1<p>Gene names are as in <i>E. coli</i> except <i>gatABC</i> and <i>yaaDE</i> that are as in <i>B. subtilis</i> (not present in <i>E. coli</i>). <sup>2</sup> A current classification of glutaminase domains (subunits) of amidotransferases includes four classes of nonhomologous enzymes: Class I (contains a catalytic triad in the active site); Class II (contains a catalytic Cys at the N-terminus); Class III (a relatively poorly explored glutaminase subunit of GatABC complex); and Class IV (nitrilase-like glutaminase component of NADS). <sup>3</sup> Percentage (%) of total number of arrangements within analyzed genomes.</p>", "links"=>[], "tags"=>["synthetase", "glutaminase", "components", "nad", "atp-dependent"], "article_id"=>293926, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_arrangement_of_the_synthetase_and_glutaminase_components_in_NAD_synthetase_and_other_families_of_ATP_dependent_amidotransferases_/293926", "title"=>"Genomic arrangement of the synthetase and glutaminase components in NAD synthetase and other families of ATP-dependent amidotransferases.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-06-15 01:05:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/622890"], "description"=>"<p>Scheme of the two-step reaction catalyzed by NAD synthetase.</p>", "links"=>[], "tags"=>["two-step", "catalyzed", "nad"], "article_id"=>293379, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scheme_of_the_two_step_reaction_catalyzed_by_NAD_synthetase_/293379", "title"=>"Scheme of the two-step reaction catalyzed by NAD synthetase.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 00:56:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/623373"], "description"=>"<p>Tentative evolutionary scenario of one- and two-domain form of NAD synthetase enzyme family.</p>", "links"=>[], "tags"=>["evolutionary", "one-", "two-domain", "nad", "synthetase", "enzyme"], "article_id"=>293858, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tentative_evolutionary_scenario_of_one_and_two_domain_form_of_NAD_synthetase_enzyme_family_/293858", "title"=>"Tentative evolutionary scenario of one- and two-domain form of NAD synthetase enzyme family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 01:04:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/323971", "https://ndownloader.figshare.com/files/324098", "https://ndownloader.figshare.com/files/324174", "https://ndownloader.figshare.com/files/324231", "https://ndownloader.figshare.com/files/324330", "https://ndownloader.figshare.com/files/324415", "https://ndownloader.figshare.com/files/324491", "https://ndownloader.figshare.com/files/324529", "https://ndownloader.figshare.com/files/324585", "https://ndownloader.figshare.com/files/324627", "https://ndownloader.figshare.com/files/324655", "https://ndownloader.figshare.com/files/324795", "https://ndownloader.figshare.com/files/324835"], "description"=>"<div><p>NAD is a ubiquitous and essential metabolic redox cofactor which also functions as a substrate in certain regulatory pathways. The last step of NAD synthesis is the ATP-dependent amidation of deamido-NAD by NAD synthetase (NADS). Members of the NADS family are present in nearly all species across the three kingdoms of Life. In eukaryotic NADS, the core synthetase domain is fused with a nitrilase-like glutaminase domain supplying ammonia for the reaction. This two-domain NADS arrangement enabling the utilization of glutamine as nitrogen donor is also present in various bacterial lineages. However, many other bacterial members of NADS family do not contain a glutaminase domain, and they can utilize only ammonia (but not glutamine) in vitro. A single-domain NADS is also characteristic for nearly all Archaea, and its dependence on ammonia was demonstrated here for the representative enzyme from <em>Methanocaldococcus jannaschi</em>. However, a question about the actual <em>in vivo</em> nitrogen donor for single-domain members of the NADS family remained open: Is it glutamine hydrolyzed by a committed (but yet unknown) glutaminase subunit, as in most ATP-dependent amidotransferases, or free ammonia as in glutamine synthetase? Here we addressed this dilemma by combining evolutionary analysis of the NADS family with experimental characterization of two representative bacterial systems: a two-subunit NADS from <em>Thermus thermophilus</em> and a single-domain NADS from <em>Salmonella typhimurium</em> providing evidence that ammonia (and not glutamine) is the physiological substrate of a typical single-domain NADS. The latter represents the most likely ancestral form of NADS. The ability to utilize glutamine appears to have evolved via recruitment of a glutaminase subunit followed by domain fusion in an early branch of Bacteria. Further evolution of the NADS family included lineage-specific loss of one of the two alternative forms and horizontal gene transfer events. Lastly, we identified NADS structural elements associated with glutamine-utilizing capabilities.</p> </div>", "links"=>[], "tags"=>["glutamine", "ammonia", "utilization", "nad", "synthetase"], "article_id"=>123947, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0039115.s001", "https://dx.doi.org/10.1371/journal.pone.0039115.s002", "https://dx.doi.org/10.1371/journal.pone.0039115.s003", "https://dx.doi.org/10.1371/journal.pone.0039115.s004", "https://dx.doi.org/10.1371/journal.pone.0039115.s005", "https://dx.doi.org/10.1371/journal.pone.0039115.s006", "https://dx.doi.org/10.1371/journal.pone.0039115.s007", "https://dx.doi.org/10.1371/journal.pone.0039115.s008", "https://dx.doi.org/10.1371/journal.pone.0039115.s009", "https://dx.doi.org/10.1371/journal.pone.0039115.s010", "https://dx.doi.org/10.1371/journal.pone.0039115.s011", "https://dx.doi.org/10.1371/journal.pone.0039115.s012", "https://dx.doi.org/10.1371/journal.pone.0039115.s013"], "stats"=>{"downloads"=>30, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Glutamine_versus_Ammonia_Utilization_in_the_NAD_Synthetase_Family/123947", "title"=>"Glutamine versus Ammonia Utilization in the NAD Synthetase Family", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-06-15 01:05:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/622973"], "description"=>"<p>Comparative genome analysis revealed 4 different genomic arrangements of GAT and NADS components: a) two domain organization (fusion); b) physical clustering; c) remote occurrence; d) absence of glutaminase. Their relative distribution across Archaea, Bacteria, and Eukaryotes is also shown (left side).</p>", "links"=>[], "tags"=>["arrangements", "functionally", "coupled", "glutaminase", "synthetase"], "article_id"=>293463, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_arrangements_of_functionally_coupled_glutaminase_GAT_and_synthetase_NADS_components_/293463", "title"=>"Genomic arrangements of functionally coupled glutaminase (GAT) and synthetase (NADS) components.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 00:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/623039"], "description"=>"<p>SDS-page analysis of Ni-NTA affinity column (A) and gel filtration chromatography (B) elution fractions show that His-tagged recombinant <i>T. thermophilus</i> NADS and untagged GAT tend to co-purify. (C) Kinetic characterization of <i>T. thermophilus</i> S-subunit and G/S complex.</p>", "links"=>[], "tags"=>["characterization", "glutaminase", "nad", "synthetase"], "article_id"=>293528, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Biochemical_characterization_of_T_thermophilus_glutaminase_and_NAD_synthetase_subunits_/293528", "title"=>"Biochemical characterization of <i>T. thermophilus</i> glutaminase and NAD synthetase subunits.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 00:58:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/623294"], "description"=>"<p>The majority of interacting residues were found in following structural regions-the α9, α18 helices and the extended C-terminal loop, which are highlighted by pink, green and yellow colors, respectively.</p>", "links"=>[], "tags"=>["regions", "synthetase", "glutaminase", "domains", "nads"], "article_id"=>293782, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g006", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Contact_regions_between_synthetase_blue_and_glutaminase_cyan_domains_in_NADS_from_Mycobacterium_tuberculosis_/293782", "title"=>"Contact regions between synthetase (blue) and glutaminase (cyan) domains in NADS from <i>Mycobacterium tuberculosis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 01:03:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/623226"], "description"=>"<p>(A) Schematic representation of NAD synthetase phylogenetic tree (full version is in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0039115#pone.0039115.s001\" target=\"_blank\">Figure S1</a>) constructed based on synthetase domain. Defined types of NAD synthetase genes – “Fused” (<i>type F</i>), “Clustered” (<i>type C</i>), “Remote” (<i>type R</i>) and “None” (<i>type N</i>) are highlighted by red, green, cyan and magenta colors, respectively. The whole tree is partitioned by topology into clusters, which are designated as I–VII branches. (B) Schematic representation of species tree with mapping of NAD synthetase gene types (full version is in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0039115#pone.0039115.s002\" target=\"_blank\">Figure S2</a>). Genomes containing single NAD synthetase gene of F, N, C, and R types are depicted by red, green, cyan and magenta colors, respectively. Genomes that possess more than one NAD synthetase gene are divided into “multiple F”, “multiple N”, “single F – single N” and “all others” genome groups, which are highlighted by dark red, dark green, orange and yellow colors, respectively.</p>", "links"=>[], "tags"=>["nad", "synthetase", "enzyme"], "article_id"=>293715, "categories"=>["Biological Sciences", "Biochemistry", "Evolutionary Biology"], "users"=>["Jessica De Ingeniis", "Marat D. Kazanov", "Konstantin Shatalin", "Mikhail S. Gelfand", "Andrei L. Osterman", "Leonardo Sorci"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039115.g005", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_analysis_of_NAD_synthetase_enzyme_family_/293715", "title"=>"Phylogenetic analysis of NAD synthetase enzyme family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-15 01:01:55"}

PMC Usage Stats | Further Information

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