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

Journal Article · 03 September 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1909604116 · OSTI ID:1576001

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)

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.

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

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

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

OSTI ID:: 1576001

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, Issue 38; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 27 works

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

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

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