Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens

Yuan, Yifeng; Zallot, Rémi; Grove, Tyler L.; Payan, Daniel J.; Martin-Verstraete, Isabelle; Šepić, Sara; Balamkundu, Seetharamsingh; Neelakandan, Ramesh; Gadi, Vinod K.; Liu, Chuan-Fa; Swairjo, Manal A.; Dedon, Peter C.; Almo, Steven C.; Gerlt, John A.; de Crécy-Lagard, Valérie

doi:10.1073/pnas.1909604116

Title: Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens

Abstract

Queuosine (Q) is a complex tRNA modification widespread in eukaryotes and bacteria that contributes to the efficiency and accuracy of protein synthesis. Eukaryotes are not capable of Q synthesis and rely on salvage of the queuine base (q) as a Q precursor. While many bacteria are capable of Q de novo synthesis, salvage of the prokaryotic Q precursors preQ₀and preQ₁also occurs. With the exception of Escherichia coli YhhQ, shown to transport preQ₀and preQ₁, the enzymes and transporters involved in Q salvage and recycling have not been well described. In this work, we discovered and characterized 2 Q salvage pathways present in many pathogenic and commensal bacteria. The first, found in the intracellular pathogen Chlamydia trachomatis, uses YhhQ and tRNA guanine transglycosylase (TGT) homologs that have changed substrate specificities to directly salvage q, mimicking the eukaryotic pathway. The second, found in bacteria from the gut flora such as Clostridioides difficile, salvages preQ₁from q through an unprecedented reaction catalyzed by a newly defined subgroup of the radical-SAM enzyme family. The source of q can be external through transport by members of the energy-coupling factor (ECF) family or internal through hydrolysis of Q by a dedicated nucleosidase. This work reinforces the concept thatmore »« less

Authors:

Yuan, Yifeng ^[1]; Zallot, Rémi ^[2]; Grove, Tyler L. ^[3]; Payan, Daniel J. ^[2]; Martin-Verstraete, Isabelle ^[4]; Šepić, Sara ^[1]; Balamkundu, Seetharamsingh ^[5]; Neelakandan, Ramesh ^[5]; Gadi, Vinod K. ^[5]; Liu, Chuan-Fa ^[5]; Swairjo, Manal A. ^[6]; Dedon, Peter C. ^[7]; Almo, Steven C. ^[3]; Gerlt, John A. ^[2]; de Crécy-Lagard, Valérie ^[1]

Univ. of Florida, Gainesville, FL (United States)
Univ. of Illinois at Urbana-Champaign, IL (United States)
Albert Einstein College of Medicine, Bronx, NY (United States)
Inst. Pasteur, Paris (France); Univ. de Paris (France)
Singapore-MIT Alliance for Research and Technology (Singapore). Infectious Disease Interdisciplinary Research Group
San Diego State Univ., CA (United States)
Singapore-MIT Alliance for Research and Technology (Singapore). Infectious Disease Interdisciplinary Research Group; Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Publication Date:: 2019-09-03

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: National Institutes of Health (NIH); Price Family Foundation; California Metabolic Research Foundation; USDOE Office of Science (SC); Eli Lilly Company

OSTI Identifier:: 1576001

Grant/Contract Number:: R01 GM70641; P01 GM118303; U54-GM093342; R21-AI133329; U54-GM094662; GM110588; S10 OD020068; AC02-06CH11357

Resource Type:: Accepted Manuscript

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Volume: 116; Journal Issue: 38; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; queuosine; nucleoside transport; sequence similarity network; comparative genomics; rSAM

Citation Formats


                    Yuan, Yifeng, Zallot, Rémi, Grove, Tyler L., Payan, Daniel J., Martin-Verstraete, Isabelle, Šepić, Sara, Balamkundu, Seetharamsingh, Neelakandan, Ramesh, Gadi, Vinod K., Liu, Chuan-Fa, Swairjo, Manal A., Dedon, Peter C., Almo, Steven C., Gerlt, John A., and de Crécy-Lagard, Valérie. Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens.  United States: N. p., 2019. 
Web.  doi:10.1073/pnas.1909604116.

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                    Yuan, Yifeng, Zallot, Rémi, Grove, Tyler L., Payan, Daniel J., Martin-Verstraete, Isabelle, Šepić, Sara, Balamkundu, Seetharamsingh, Neelakandan, Ramesh, Gadi, Vinod K., Liu, Chuan-Fa, Swairjo, Manal A., Dedon, Peter C., Almo, Steven C., Gerlt, John A., & de Crécy-Lagard, Valérie. Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens.  United States.  https://doi.org/10.1073/pnas.1909604116

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                    Yuan, Yifeng, Zallot, Rémi, Grove, Tyler L., Payan, Daniel J., Martin-Verstraete, Isabelle, Šepić, Sara, Balamkundu, Seetharamsingh, Neelakandan, Ramesh, Gadi, Vinod K., Liu, Chuan-Fa, Swairjo, Manal A., Dedon, Peter C., Almo, Steven C., Gerlt, John A., and de Crécy-Lagard, Valérie. Tue .  
"Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens".  United States.  https://doi.org/10.1073/pnas.1909604116.  https://www.osti.gov/servlets/purl/1576001.

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@article{osti_1576001,

  title        = {Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens},

  author       = {Yuan, Yifeng and Zallot, Rémi and Grove, Tyler L. and Payan, Daniel J. and Martin-Verstraete, Isabelle and Šepić, Sara and Balamkundu, Seetharamsingh and Neelakandan, Ramesh and Gadi, Vinod K. and Liu, Chuan-Fa and Swairjo, Manal A. and Dedon, Peter C. and Almo, Steven C. and Gerlt, John A. and de Crécy-Lagard, Valérie},

  abstractNote = {Queuosine (Q) is a complex tRNA modification widespread in eukaryotes and bacteria that contributes to the efficiency and accuracy of protein synthesis. Eukaryotes are not capable of Q synthesis and rely on salvage of the queuine base (q) as a Q precursor. While many bacteria are capable of Q de novo synthesis, salvage of the prokaryotic Q precursors preQ0and preQ1also occurs. With the exception of Escherichia coli YhhQ, shown to transport preQ0and preQ1, the enzymes and transporters involved in Q salvage and recycling have not been well described. In this work, we discovered and characterized 2 Q salvage pathways present in many pathogenic and commensal bacteria. The first, found in the intracellular pathogen Chlamydia trachomatis, uses YhhQ and tRNA guanine transglycosylase (TGT) homologs that have changed substrate specificities to directly salvage q, mimicking the eukaryotic pathway. The second, found in bacteria from the gut flora such as Clostridioides difficile, salvages preQ1from q through an unprecedented reaction catalyzed by a newly defined subgroup of the radical-SAM enzyme family. The source of q can be external through transport by members of the energy-coupling factor (ECF) family or internal through hydrolysis of Q by a dedicated nucleosidase. This work reinforces the concept that hosts and members of their associated microbiota compete for the salvage of Q precursors micronutrients.},

  doi          = {10.1073/pnas.1909604116},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 38,

  volume       = 116,

  place        = {United States},

  year         = {2019},

  month        = {9}

}

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Structural basis of Qng1-mediated salvage of the micronutrient queuine from queuosine-5′-monophosphate as the biological substrate

Journal Article Hung, Shr-Hau ; Elliott, Gregory I. ; Ramkumar, Thakku R. ; ... - Nucleic Acids Research

Abstract Eukaryotic life benefits from—and ofttimes critically relies upon—the de novo biosynthesis and supply of vitamins and micronutrients from bacteria. The micronutrient queuosine (Q), derived from diet and/or the gut microbiome, is used as a source of the nucleobase queuine, which once incorporated into the anticodon of tRNA contributes to translational efficiency and accuracy. Here, we report high-resolution, substrate-bound crystal structures of the Sphaerobacter thermophilus queuine salvage protein Qng1 (formerly DUF2419) and of its human ortholog QNG1 (C9orf64), which together with biochemical and genetic evidence demonstrate its function as the hydrolase releasing queuine from queuosine-5′-monophosphate as the biological substrate. Wemore »« less
https://doi.org/10.1093/nar/gkac1231
X-ray absorption spectroscopy of the zinc site in tRNA-guanine transglycosylase from Escherichia coli

Journal Article Garcia, G A ; Tierney, D L ; Chong, S ; ... - Biochemistry (Eaton)

A key step in the post-transcriptional modification of tRNA with queuine in Escherichia coli is the exchange of the queuine precursor, preQ{sub 1} into tRNA. This reaction is catalyzed by tRNA-guanine transglycosylase (TGT). We have previously shown that the E. coli TGT is a zinc metalloprotein. Site-directed mutagenesis studies indicated that cysteines 302, 304, 307 and histidine 317 constitute the four ligands to the zinc. The involvement of histidine 317 is somewhat confounded by the presence of histidine 316. We have examined the zinc site in TGT (wt) and TGT (H317C) by X-ray absorption spectroscopy. The TGT (wt) data aremore »« less
https://doi.org/10.1021/bi952403v
Investigating the prevalence of queuine in Escherichia coli RNA via incorporation of the tritium-labeled precursor, preQ{sub 1}

Journal Article Brooks, Allen F. ; Velez-Martinez, Carol S. ; Hollis Showalter, H. D. ; ... - Biochemical and Biophysical Research Communications

Highlights: Black-Right-Pointing-Pointer Escherichia coli cells deficient in preQ{sub 1} biosynthesis can utilize exogenous preQ{sub 1} from growth media. Black-Right-Pointing-Pointer Exogenous radiolabeled preQ{sub 1} is incorporated into cellular RNA in both wild-type and preQ{sub 1} deficient cells. Black-Right-Pointing-Pointer Radiolabeled preQ{sub 1} is incorporated into RNAs of differing sizes larger than tRNA. Black-Right-Pointing-Pointer Analysis of isolated ribosomes shows that radiolabeled preQ{sub 1} is incorporated into ribosomal RNA. Black-Right-Pointing-Pointer The conclusion of this study is that queuine is incorporated into many other RNAs in addition to the known tRNAs. -- Abstract: There are over 100 modified bases that occur in RNA with themore »« less
https://doi.org/10.1016/J.BBRC.2012.07.055
7-Deazaguanines in DNA: functional and structural elucidation of a DNA modification system

Journal Article Gedara, Samanthi Herath ; Wood, Evan ; Gustafson, Andrew ; ... - Nucleic Acids Research

Abstract The modified nucleosides 2′-deoxy-7-cyano- and 2′-deoxy-7-amido-7-deazaguanosine (dPreQ0 and dADG, respectively) recently discovered in DNA are the products of the bacterial queuosine tRNA modification pathway and the dpd gene cluster, the latter of which encodes proteins that comprise the elaborate Dpd restriction–modification system present in diverse bacteria. Recent genetic studies implicated the dpdA, dpdB and dpdC genes as encoding proteins necessary for DNA modification, with dpdD–dpdK contributing to the restriction phenotype. Here we report the in vitro reconstitution of the Dpd modification machinery from Salmonella enterica serovar Montevideo, the elucidation of the roles of each protein and the X-ray crystalmore »« less
https://doi.org/10.1093/nar/gkad141
Queuine metabolism and cadmium toxicity in Drosophila

Conference Farkas, W R ; Siard, T ; Jacobson, K B - FASEB Journal (Federation of American Societies for Experimental Biology); (United States)

Queuine is a derivative of guanine found in the first position of the anticodon of the transfer RNAs for Asp, Asn, His and Tyr. The transcripts of these tRNAs contain a guanine in this position. This guanine is enzymatically excised and replaced by queuine. The ratio of queuine-containing or (q+) tRNA to its precursor or (q{minus}) tRNA changes throughout the Drosophila life cycle. in the egg 10% of the tRNA is (q+). During the three larval stages this ratio drops to zero. In the one day old adult it is about 10%. It has previously been shown that when fliesmore »« less

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Title: Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens

Abstract

Citation Formats

Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks journal, August 2015

Nutrition and Bipartite Metabolism of Intracellular Pathogens journal, June 2019

Synthesis of the Transfer-RNA Nucleoside Queuosine by Using a Chiral Allyl Azide Intermediate. journal, July 2007

Dali server update journal, April 2016

Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ journal, March 2013

Slight sequence variations of a common fold explain the substrate specificities of tRNA-guanine transglycosylases from the three kingdoms journal, October 1997

Possible anticodon sequences of tRNAHis, tRNAAsn, and tRNAAsp from Escherichia coli. Universal presence of nucleoside O in the first position of the anticodons of these transfer ribonucleic acid journal, January 1972

Transcriptional response of Clostridium difficile to low iron conditions journal, January 2018

Increased Expression of Queuosine Synthesizing Enzyme, tRNA-Guanine Transglycosylase, and Queuosine Levels in tRNA of Leukemic Cells journal, January 2001

Database resources of the National Center for Biotechnology Information journal, November 2018

Structural Insights into Thioether Bond Formation in the Biosynthesis of Sactipeptides journal, August 2017

Reannotation of the genome sequence of Clostridium difficile strain 630 journal, February 2011

Basic Local Alignment Search Tool journal, October 1990

Worlds within worlds: evolution of the vertebrate gut microbiota journal, October 2008

Evolution of eukaryal tRNA-guanine transglycosylase: insight gained from the heterocyclic substrate recognition by the wild-type and mutant human and Escherichia coli tRNA-guanine transglycosylases journal, December 2010

Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center journal, November 2016

Novel genomic island modifies DNA with 7-deazaguanine derivatives journal, February 2016

Queuosine modification in tRNA and expression of the nitrate reductase in Escherichia coli. journal, July 1984

Deazaguanine derivatives, examples of crosstalk between RNA and DNA modification pathways journal, December 2016

Catalysis by nucleoside hydrolases journal, December 2003

The Queuine Micronutrient: Charting a Course from Microbe to Man journal, April 2015

Prolonging healthy aging: Longevity vitamins and proteins journal, October 2018

Three-dimensional structure of hyper-modified nucleoside Q located in the wobbling position of tRNA journal, November 1979

Queuosine‐modified tRNAs confer nutritional control of protein translation journal, August 2018

Queuine, a modified base incorporated posttranscriptionally into eukaryotic transfer RNA: wide distribution in nature journal, April 1982

Involvement of protein kinase C in the control of tRNA modification with queuine in HeLa cells journal, January 1995

Structural and biochemical characterization of the nucleoside hydrolase from C . elegans reveals the role of two active site cysteine residues in catalysis : Structure of the journal, March 2017

Comparative genomics of metabolic capacities of regulons controlled by cis-regulatory RNA motifs in bacteria journal, January 2013

A Nutrient-Driven tRNA Modification Alters Translational Fidelity and Genome-wide Protein Coding across an Animal Genus journal, December 2014

Characterization of the human tRNA-guanine transglycosylase: Confirmation of the heterodimeric subunit structure journal, March 2010

Mechanism and Substrate Specificity of tRNA-Guanine Transglycosylases (TGTs): tRNA-Modifying Enzymes from the Three Different Kingdoms of Life Share a Common Catalytic Mechanism journal, October 2005

The Escherichia coli COG1738 Member YhhQ Is Involved in 7-Cyanodeazaguanine (preQ0) Transport journal, February 2017

Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods journal, March 2001

Interactions Between the Gastrointestinal Microbiome and Clostridium difficile journal, October 2015

Paramagnetic Intermediates Generated by Radical S-Adenosylmethionine (SAM) Enzymes journal, July 2014

Identification of the minimal bacterial 2′-deoxy-7-amido-7-deazaguanine synthesis machinery journal, October 2018

Investigation of Specificity Determinants in Bacterial tRNA-Guanine Transglycosylase Reveals Queuine, the Substrate of Its Eucaryotic Counterpart, as Inhibitor journal, May 2013

Complex Biotransformations Catalyzed by Radical S -Adenosylmethionine Enzymes journal, July 2011

RegPrecise 3.0 – A resource for genome-scale exploration of transcriptional regulation in bacteria journal, January 2013

Affinity electrophoresis for monitoring terminal phosphorylation and the presence of queuosine in RNA. Application of polyacrylamide containing a covalently bound boronic acid journal, January 1985

Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme journal, October 2008

Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats journal, March 2012

Allene ether Nazarov cyclization journal, January 2014

Novel salvage of queuine from queuosine and absence of queuine synthesis in Chlorella pyrenoidosa and Chlamydomonas reinhardtii. journal, December 1988

Queuosine modification of tRNA: its divergent role in cellular machinery journal, November 2009

Database resources of the National Center for Biotechnology Information journal, January 2006

A Novel Class of Modular Transporters for Vitamins in Prokaryotes journal, October 2008

Cellular dynamics of tRNAs and their genes journal, November 2009

Radical S -Adenosylmethionine Enzymes journal, January 2014

The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes journal, September 2005

BREX is a novel phage resistance system widespread in microbial genomes journal, December 2014

Clostridium difficile Biofilm: Remodeling Metabolism and Cell Surface to Build a Sparse and Heterogeneously Aggregated Architecture journal, September 2018

Crystal structure of tRNA-guanine transglycosylase: RNA modification by base exchange. journal, June 1996

Synthesis of the Transfer-RNA Nucleoside Queuosine by Using a Chiral Allyl Azide Intermediate journal, March 2007

Presence of queuine in Drosophila melanogaster: correlation of free pool with queuosine content of tRNA and effect of mutations in pteridine metabolism journal, January 1981

PROMALS3D: a tool for multiple protein sequence and structure alignments journal, February 2008

‘Democratized’ genomic enzymology web tools for functional assignment journal, December 2018

The Key Sigma Factor of Transition Phase, SigH, Controls Sporulation, Metabolism, and Virulence Factor Expression in Clostridium difficile journal, May 2011

A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain journal, March 2007

Queuosine Formation in Eukaryotic tRNA Occurs via a Mitochondria-localized Heteromeric Transglycosylase journal, May 2009

PreQ0 Base, an Unusual Metabolite with Anti-cancer Activity from Streptomyces qinglanensis 172205 journal, March 2015

Structural Basis for Methyl Transfer by a Radical SAM Enzyme journal, April 2011

A Role for tRNA Modifications in Genome Structure and Codon Usage journal, March 2012

Diet-dependent depletion of queuosine in tRNAs in Caenorhabditis elegans does not lead to a developmental block journal, June 2007

Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome journal, June 2019

Structural, Functional, and Taxonomic Diversity of Three PreQ1 Riboswitch Classes journal, July 2014

The Radical SAM Superfamily journal, January 2008

Effect of diet on the queuosine family of tRNAs of germ-free mice. journal, July 1980

Administration of exogenous queuine is essential for the biosynthesis of the queuosine-containing transfer RNAs in the mouse. journal, November 1981

Structure of an amniotic fluid component, 7-(4,5-cis-dihydroxy-1-cyclopenten-3-ylaminomethyl)-7-deazaguanine (queuine), a substrate for tRNA: guanine transglycosylase. journal, September 1980

Isolation and characterization of an Escherichia coli mutant lacking tRNA-guanine transglycosylase. Function and biosynthesis of queuosine in tRNA. journal, June 1982

Database resources of the National Center for Biotechnology Information journal, October 2020

Database resources of the National Center for Biotechnology Information journal, December 2007

Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015

Nutrition and Bipartite Metabolism of Intracellular Pathogens
journal, June 2019

Synthesis of the Transfer-RNA Nucleoside Queuosine by Using a Chiral Allyl Azide Intermediate.
journal, July 2007

Dali server update
journal, April 2016

Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ
journal, March 2013

Slight sequence variations of a common fold explain the substrate specificities of tRNA-guanine transglycosylases from the three kingdoms
journal, October 1997

Possible anticodon sequences of tRNAHis, tRNAAsn, and tRNAAsp from Escherichia coli. Universal presence of nucleoside O in the first position of the anticodons of these transfer ribonucleic acid
journal, January 1972

Transcriptional response of Clostridium difficile to low iron conditions
journal, January 2018

Increased Expression of Queuosine Synthesizing Enzyme, tRNA-Guanine Transglycosylase, and Queuosine Levels in tRNA of Leukemic Cells
journal, January 2001

Database resources of the National Center for Biotechnology Information
journal, November 2018

Structural Insights into Thioether Bond Formation in the Biosynthesis of Sactipeptides
journal, August 2017

Reannotation of the genome sequence of Clostridium difficile strain 630
journal, February 2011

Basic Local Alignment Search Tool
journal, October 1990

Worlds within worlds: evolution of the vertebrate gut microbiota
journal, October 2008

Evolution of eukaryal tRNA-guanine transglycosylase: insight gained from the heterocyclic substrate recognition by the wild-type and mutant human and Escherichia coli tRNA-guanine transglycosylases
journal, December 2010

Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center
journal, November 2016

Novel genomic island modifies DNA with 7-deazaguanine derivatives
journal, February 2016

Queuosine modification in tRNA and expression of the nitrate reductase in Escherichia coli.
journal, July 1984

Deazaguanine derivatives, examples of crosstalk between RNA and DNA modification pathways
journal, December 2016

Catalysis by nucleoside hydrolases
journal, December 2003

The Queuine Micronutrient: Charting a Course from Microbe to Man
journal, April 2015

Prolonging healthy aging: Longevity vitamins and proteins
journal, October 2018

Three-dimensional structure of hyper-modified nucleoside Q located in the wobbling position of tRNA
journal, November 1979

Queuosine‐modified tRNAs confer nutritional control of protein translation
journal, August 2018

Queuine, a modified base incorporated posttranscriptionally into eukaryotic transfer RNA: wide distribution in nature
journal, April 1982

Involvement of protein kinase C in the control of tRNA modification with queuine in HeLa cells
journal, January 1995

Structural and biochemical characterization of the nucleoside hydrolase from C . elegans reveals the role of two active site cysteine residues in catalysis : Structure of the
journal, March 2017

Comparative genomics of metabolic capacities of regulons controlled by cis-regulatory RNA motifs in bacteria
journal, January 2013

A Nutrient-Driven tRNA Modification Alters Translational Fidelity and Genome-wide Protein Coding across an Animal Genus
journal, December 2014

Characterization of the human tRNA-guanine transglycosylase: Confirmation of the heterodimeric subunit structure
journal, March 2010

Mechanism and Substrate Specificity of tRNA-Guanine Transglycosylases (TGTs): tRNA-Modifying Enzymes from the Three Different Kingdoms of Life Share a Common Catalytic Mechanism
journal, October 2005

The Escherichia coli COG1738 Member YhhQ Is Involved in 7-Cyanodeazaguanine (preQ0) Transport
journal, February 2017

Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods
journal, March 2001

Interactions Between the Gastrointestinal Microbiome and Clostridium difficile
journal, October 2015

Paramagnetic Intermediates Generated by Radical S-Adenosylmethionine (SAM) Enzymes
journal, July 2014

Identification of the minimal bacterial 2′-deoxy-7-amido-7-deazaguanine synthesis machinery
journal, October 2018

Investigation of Specificity Determinants in Bacterial tRNA-Guanine Transglycosylase Reveals Queuine, the Substrate of Its Eucaryotic Counterpart, as Inhibitor
journal, May 2013

Complex Biotransformations Catalyzed by Radical S -Adenosylmethionine Enzymes
journal, July 2011

RegPrecise 3.0 – A resource for genome-scale exploration of transcriptional regulation in bacteria
journal, January 2013

Affinity electrophoresis for monitoring terminal phosphorylation and the presence of queuosine in RNA. Application of polyacrylamide containing a covalently bound boronic acid
journal, January 1985

Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme
journal, October 2008

Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats
journal, March 2012

Allene ether Nazarov cyclization
journal, January 2014

Novel salvage of queuine from queuosine and absence of queuine synthesis in Chlorella pyrenoidosa and Chlamydomonas reinhardtii.
journal, December 1988

Queuosine modification of tRNA: its divergent role in cellular machinery
journal, November 2009

Database resources of the National Center for Biotechnology Information
journal, January 2006

A Novel Class of Modular Transporters for Vitamins in Prokaryotes
journal, October 2008

Cellular dynamics of tRNAs and their genes
journal, November 2009

Radical S -Adenosylmethionine Enzymes
journal, January 2014

The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes
journal, September 2005

BREX is a novel phage resistance system widespread in microbial genomes
journal, December 2014

Clostridium difficile Biofilm: Remodeling Metabolism and Cell Surface to Build a Sparse and Heterogeneously Aggregated Architecture
journal, September 2018

Crystal structure of tRNA-guanine transglycosylase: RNA modification by base exchange.
journal, June 1996

Synthesis of the Transfer-RNA Nucleoside Queuosine by Using a Chiral Allyl Azide Intermediate
journal, March 2007

Presence of queuine in Drosophila melanogaster: correlation of free pool with queuosine content of tRNA and effect of mutations in pteridine metabolism
journal, January 1981

PROMALS3D: a tool for multiple protein sequence and structure alignments
journal, February 2008

‘Democratized’ genomic enzymology web tools for functional assignment
journal, December 2018

The Key Sigma Factor of Transition Phase, SigH, Controls Sporulation, Metabolism, and Virulence Factor Expression in Clostridium difficile
journal, May 2011

A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain
journal, March 2007

Queuosine Formation in Eukaryotic tRNA Occurs via a Mitochondria-localized Heteromeric Transglycosylase
journal, May 2009

PreQ₀ Base, an Unusual Metabolite with Anti-cancer Activity from Streptomyces qinglanensis 172205
journal, March 2015

Structural Basis for Methyl Transfer by a Radical SAM Enzyme
journal, April 2011

A Role for tRNA Modifications in Genome Structure and Codon Usage
journal, March 2012

Diet-dependent depletion of queuosine in tRNAs in Caenorhabditis elegans does not lead to a developmental block
journal, June 2007

Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome
journal, June 2019

Structural, Functional, and Taxonomic Diversity of Three PreQ1 Riboswitch Classes
journal, July 2014

The Radical SAM Superfamily
journal, January 2008

Effect of diet on the queuosine family of tRNAs of germ-free mice.
journal, July 1980

Administration of exogenous queuine is essential for the biosynthesis of the queuosine-containing transfer RNAs in the mouse.
journal, November 1981

Structure of an amniotic fluid component, 7-(4,5-cis-dihydroxy-1-cyclopenten-3-ylaminomethyl)-7-deazaguanine (queuine), a substrate for tRNA: guanine transglycosylase.
journal, September 1980

Isolation and characterization of an Escherichia coli mutant lacking tRNA-guanine transglycosylase. Function and biosynthesis of queuosine in tRNA.
journal, June 1982

Database resources of the National Center for Biotechnology Information
journal, October 2020

Database resources of the National Center for Biotechnology Information
journal, December 2007