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Research Article

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

Yifeng Yuan, Rémi Zallot, Tyler L. Grove, Daniel J. Payan, Isabelle Martin-Verstraete, Sara Šepić, Seetharamsingh Balamkundu, Ramesh Neelakandan, Vinod K. Gadi, Chuan-Fa Liu, Manal A. Swairjo, Peter C. Dedon, Steven C. Almo, John A. Gerlt, and Valérie de Crécy-Lagard
PNAS September 17, 2019 116 (38) 19126-19135; first published September 3, 2019 https://doi.org/10.1073/pnas.1909604116
Yifeng Yuan
aDepartment of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611;
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Rémi Zallot
bInstitute for Genomic Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Tyler L. Grove
cDepartment of Biochemistry, Albert Einstein College of Medicine, Bronx, NY 10461;
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Daniel J. Payan
bInstitute for Genomic Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Isabelle Martin-Verstraete
dLaboratoire de Pathogénèse des Bactéries Anaérobies, Institut Pasteur et Université de Paris, F-75015 Paris, France;
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Sara Šepić
aDepartment of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611;
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Seetharamsingh Balamkundu
eSingapore-MIT Alliance for Research and Technology, Infectious Disease Interdisciplinary Research Group, 138602 Singapore, Singapore;
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Ramesh Neelakandan
eSingapore-MIT Alliance for Research and Technology, Infectious Disease Interdisciplinary Research Group, 138602 Singapore, Singapore;
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Vinod K. Gadi
eSingapore-MIT Alliance for Research and Technology, Infectious Disease Interdisciplinary Research Group, 138602 Singapore, Singapore;
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Chuan-Fa Liu
eSingapore-MIT Alliance for Research and Technology, Infectious Disease Interdisciplinary Research Group, 138602 Singapore, Singapore;
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Manal A. Swairjo
fDepartment of Chemistry and Biochemistry, San Diego State University, San Diego, CA 92182;gThe Viral Information Institute, San Diego State University, San Diego, CA 92182;
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Peter C. Dedon
eSingapore-MIT Alliance for Research and Technology, Infectious Disease Interdisciplinary Research Group, 138602 Singapore, Singapore;hDepartment of Biological Engineering and Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139;iCenter for Environmental Health Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139;
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Steven C. Almo
cDepartment of Biochemistry, Albert Einstein College of Medicine, Bronx, NY 10461;
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John A. Gerlt
bInstitute for Genomic Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;jDepartment of Biochemistry, University of Illinois at Urbana–Champaign, Urbana, IL 61801;kDepartment of Chemistry, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Valérie de Crécy-Lagard
aDepartment of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611;lUniversity of Florida Genetics Institute, Gainesville, FL 32610
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  • For correspondence: vcrecy@ufl.edu
  1. Edited by Tina M. Henkin, The Ohio State University, Columbus, OH, and approved August 1, 2019 (received for review June 16, 2019)

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Significance

Queuosine (Q) is a tRNA modification found in eukaryotes and bacteria that plays an important role in translational efficiency and accuracy. Queuine (q), the Q nucleobase, is increasingly appreciated as an important micronutrient that contributes to human health. We describe here that q salvage pathways exist in bacteria, including many pathogens and host-associated organisms, suggesting a direct competition for the q precursor in the human gut microbiome. We also show how a rational use of comparative genomics can lead to the discovery of novel types of enzymatic reactions, illustrated by the discovery of the queuine lyase enzyme.

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 preQ0 and preQ1 also occurs. With the exception of Escherichia coli YhhQ, shown to transport preQ0 and preQ1, the enzymes and transporters involved in Q salvage and recycling have not been well described. 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 preQ1 from 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.

  • queuosine
  • nucleoside transport
  • sequence similarity network
  • comparative genomics
  • rSAM

Footnotes

  • ↵1Y.Y., R.Z., and T.L.G. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: vcrecy{at}ufl.edu.
  • Author contributions: Y.Y., R.Z., I.M.-V., S.C.A., J.A.G., and V.d.C.-L. designed research; Y.Y., R.Z., T.L.G., D.J.P., and I.M.-V. performed research; S.B., R.N., V.K.G., C.-F.L., and P.C.D. contributed new reagents/analytic tools; Y.Y., R.Z., T.L.G., S.Š., M.A.S., and V.d.C.-L. analyzed data; and Y.Y., R.Z., T.L.G., I.M.-V., P.C.D., and V.d.C.-L. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the Protein Data Bank, https://www.rcsb.org (ID code 6P78).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1909604116/-/DCSupplemental.

Published under the PNAS license.

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Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens
Yifeng Yuan, Rémi Zallot, Tyler L. Grove, Daniel J. Payan, Isabelle Martin-Verstraete, Sara Šepić, Seetharamsingh Balamkundu, Ramesh Neelakandan, Vinod K. Gadi, Chuan-Fa Liu, Manal A. Swairjo, Peter C. Dedon, Steven C. Almo, John A. Gerlt, Valérie de Crécy-Lagard
Proceedings of the National Academy of Sciences Sep 2019, 116 (38) 19126-19135; DOI: 10.1073/pnas.1909604116

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Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens
Yifeng Yuan, Rémi Zallot, Tyler L. Grove, Daniel J. Payan, Isabelle Martin-Verstraete, Sara Šepić, Seetharamsingh Balamkundu, Ramesh Neelakandan, Vinod K. Gadi, Chuan-Fa Liu, Manal A. Swairjo, Peter C. Dedon, Steven C. Almo, John A. Gerlt, Valérie de Crécy-Lagard
Proceedings of the National Academy of Sciences Sep 2019, 116 (38) 19126-19135; DOI: 10.1073/pnas.1909604116
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