1887

Microbiology Society logo

Volume 170, Issue 9

Queuosine salvage in Houston 1: a unique evolutionary path Open Access

Graphical Abstract

Graphical Abstract

The substrate specificity of bacterial TGT and Q precursor transporter protein shifts from preQ to the queuine base in intracellular human pathogens such as , driven by adaptation to the intracellular environment. The facultative intracellular pathogen exhibits a rare dual-substrate specificity for these Q salvage enzymes that represents an evolutionary transition state.

Abstract

Queuosine (Q) stands out as the sole tRNA modification that can be synthesized via salvage pathways. Comparative genomic analyses identified specific bacteria that showed a discrepancy between the projected Q salvage route and the predicted substrate specificities of the two identified salvage proteins: (1) the distinctive enzyme tRNA guanine-34 transglycosylase (bacterial TGT, or bTGT), responsible for inserting precursor bases into target tRNAs; and (2) queuosine precursor transporter (QPTR), a transporter protein that imports Q precursors. Organisms such as the facultative intracellular pathogen , which possess only bTGT and QPTR but lack predicted enzymes for converting preQ to Q, would be expected to salvage the queuine (q) base, mirroring the scenario for the obligate intracellular pathogen . However, sequence analyses indicate that the substrate-specificity residues of their bTGTs resemble those of enzymes inserting preQ rather than q. Intriguingly, MS analyses of tRNA modification profiles in reveal trace amounts of preQ, previously not observed in a natural context. Complementation analysis demonstrates that bTGT and QPTR not only utilize preQ, akin to their counterparts, but can also process q when provided at elevated concentrations. The experimental and phylogenomic analyses suggest that the Q pathway in could represent an evolutionary transition among intracellular pathogens – from ancestors that synthesized Q to a state prioritizing the salvage of q. Another possibility that will require further investigations is that the insertion of preQ confers fitness advantages when is growing outside a mammalian host.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Bartonella henselae , intracellular parasite , queuosine , TGT enzyme , tRNA modification and YhhQ
Funding
This study was supported by the:
  • National Research Foundation of Singapore
    • Principle Award Recipient: PeterC. Dedon
  • National Institute of Environmental Health Sciences (Award ES024615)
    • Principle Award Recipient: PeterC. Dedon
  • National Institute of Environmental Health Sciences (Award ES026856)
    • Principle Award Recipient: PeterC. Dedon
  • National Institute of General Medical Sciences (Award GM070641)
    • Principle Award Recipient: Valeriede Crecy-Lagard
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001490
2024-09-05
2024-09-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/9/mic001490.html?itemId=/content/journal/micro/10.1099/mic.0.001490&mimeType=html&fmt=ahah

References

  1. El Yacoubi B, Bailly M, de Crécy-Lagard V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 2012; 46:69–95 [View Article] [PubMed]
     [Google Scholar]
  2. Antoine L, Bahena-Ceron R, Bunwaree HD, Gobry M, Loegler V et al. RNA Modifications in Pathogenic Bacteria: Impact on Host Adaptation and Virulence Genes: MDPI AG; 2021 p 1125
     [Google Scholar]
  3. Fleming BA, Blango MG, Rousek AA, Kincannon WM, Tran A et al. A tRNA modifying enzyme as a tunable regulatory nexus for bacterial stress responses and virulence. Nucleic Acids Res 2022; 50:7570–7590 [View Article] [PubMed]
     [Google Scholar]
  4. Hutinet G, Swarjo MA, de Crécy-Lagard V. Deazaguanine Derivatives, Examples of Crosstalk between RNA and DNA Modification Pathways RNA Biology. Taylor and Francis Inc; 2017 pp 1175–1184
     [Google Scholar]
  5. Fergus C, Barnes D, Alqasem MA, Kelly VP. The Queuine Micronutrient: Charting a Course from Microbe to Man Nutrients: MDPI AG; 2015 pp 2897–2929
     [Google Scholar]
  6. Zallot R, Brochier-Armanet C, Gaston KW, Forouhar F, Limbach PA et al. Plant, animal, and fungal micronutrient queuosine is salvaged by members of the DUF2419 protein family. ACS Chem Biol 2014; 9:1812–1825 [View Article] [PubMed]
     [Google Scholar]
  7. Chevance FFV, Le Guyon S, Hughes KT. The effects of codon context on in vivo translation speed. PLoS Genet 2014; 10:e1004392 [View Article] [PubMed]
     [Google Scholar]
  8. Whittle CA, Kulkarni A, Chung N, Extavour CG. Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes. BMC Genomics 2021; 22:234 [View Article] [PubMed]
     [Google Scholar]
  9. Pollo-Oliveira L, Davis NK, Hossain I, Ho P, Yuan Y et al. The absence of the queuosine tRNA modification leads to pleiotropic phenotypes revealing perturbations of metal and oxidative stress homeostasis in Escherichia coli K12. Metallomics 2022; 14:mfac065 [View Article] [PubMed]
     [Google Scholar]
  10. Durand JM, Dagberg B, Uhlin BE, Björk GR. Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol Microbiol 2000; 35:924–935 [View Article] [PubMed]
     [Google Scholar]
  11. Díaz-Rullo J, González-Pastor JE. tRNA queuosine modification is involved in biofilm formation and virulence in bacteria. Nucleic Acids Res 2023; 51:9821–9837 [View Article] [PubMed]
     [Google Scholar]
  12. Fruchard L, Babosan A, Carvalho A, Lang M, Li B et al. Aminoglycoside tolerance in Vibrio cholerae engages translational reprogramming associated to queuosine tRNA modification. eLife 2024; 13:RP96317 [View Article]
     [Google Scholar]
  13. Zallot R, Ross R, Chen W-H, Bruner SD, Limbach PA et al. Identification of a novel epoxyqueuosine reductase family by comparative genomics. ACS Chem Biol 2017; 12:844–851 [View Article] [PubMed]
     [Google Scholar]
  14. Zallot R, Yuan Y, de Crécy-Lagard V. The Escherichia coli COG1738 Member YhhQ Is Involved in 7-Cyanodeazaguanine (preQ₀) Transport. Biomolecules 2017; 7:12 [View Article] [PubMed]
     [Google Scholar]
  15. Yuan Y, Zallot R, Grove TL, Payan DJ, Martin-Verstraete I et al. Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens. Proc Natl Acad Sci U S A 2019; 116:19126–19135 [View Article] [PubMed]
     [Google Scholar]
  16. Guillén N. Pathogenicity and virulence of Entamoeba histolytica, the agent of amoebiasis. Virulence 2023; 14:2158656 [View Article] [PubMed]
     [Google Scholar]
  17. Dixit S, Kessler AC, Henderson J, Pan X, Zhao R et al. Dynamic queuosine changes in tRNA couple nutrient levels to codon choice in Trypanosoma brucei. Nucleic Acids Res 2021; 49:12986–12999 [View Article] [PubMed]
     [Google Scholar]
  18. Jin X, Gou Y, Xin Y, Li J, Sun J et al. Advancements in understanding the molecular and immune mechanisms of Bartonella pathogenicity. Front Microbiol 2023; 14:1196700 [View Article]
     [Google Scholar]
  19. Hansmann Y, DeMartino S, Piémont Y, Meyer N, Mariet P et al. Diagnosis of cat scratch disease with detection of Bartonella henselae by PCR: A study of patients with lymph node enlargement. J Clin Microbiol 2005; 43:3800–3806 [View Article] [PubMed]
     [Google Scholar]
  20. La Scola B, Liang Z, Zeaiter Z, Houpikian P, Grimont PAD et al. Genotypic characteristics of two serotypes of Bartonella henselae. J Clin Microbiol 2002; 40:2002–2008 [View Article] [PubMed]
     [Google Scholar]
  21. Zeaiter Z, Fournier PE, Raoult D. Genomic variation of Bartonella henselae strains detected in lymph nodes of patients with cat scratch disease. J Clin Microbiol 2002; 40:1023–1030 [View Article] [PubMed]
     [Google Scholar]
  22. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
     [Google Scholar]
  23. Olson RD, Assaf R, Brettin T, Conrad N, Cucinell C et al. Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRDand ViPR. Nucleic Acids Res 2023; 51:D678–D689 [View Article] [PubMed]
     [Google Scholar]
  24. Edgar RC. Muscle5: High-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nat Commun 2022; 13:6968 [View Article] [PubMed]
     [Google Scholar]
  25. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009; 25:1189–1191 [View Article] [PubMed]
     [Google Scholar]
  26. Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto BL et al. InterPro in 2022. Nucleic Acids Res 2023; 51:D418–D427 [View Article] [PubMed]
     [Google Scholar]
  27. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article] [PubMed]
     [Google Scholar]
  28. Varadi M, Anyango S, Deshpande M, Nair S, Natassia C et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res 2022; 50:D439–D444 [View Article] [PubMed]
     [Google Scholar]
  29. Zhu K, Day T, Warshaviak D, Murrett C, Friesner R et al. Antibody structure determination using a combination of homology modeling, energy‐based refinement, and loop prediction. Proteins 2014; 82:1646–1655 [View Article]
     [Google Scholar]
  30. Gerlt JA, Bouvier JT, Davidson DB, Imker HJ, Sadkhin B, Slater DR et al. Enzyme function initiative-enzyme similarity tool (EFI-EST): A web tool for generating protein sequence similarity networks. 1854 Biochimica et Biophysica Acta - Proteins and Proteomics Elsevier B.V; 20151019–37
     [Google Scholar]
  31. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
     [Google Scholar]
  32. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010; 10:210 [View Article] [PubMed]
     [Google Scholar]
  33. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
     [Google Scholar]
  34. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  35. Harrison KJ, Crécy-Lagard V de, Zallot R. Gene Graphics: a genomic neighborhood data visualization web application. Bioinformatics 2018; 34:1406–1408 [View Article] [PubMed]
     [Google Scholar]
  36. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845–858 [View Article] [PubMed]
     [Google Scholar]
  37. Battisti JM, Minnick MF. Laboratory maintenance of Bartonella quintana. Curr Protoc Microbiol 2008; Chapter 3:Unit [View Article] [PubMed]
     [Google Scholar]
  38. Green R, Rogers EJ. Transformation of chemically competent E. coli. Methods Enzymol 2013; 529:329–336 [View Article] [PubMed]
     [Google Scholar]
  39. Johannsson S, Neumann P, Ficner R. Crystal structure of the human tRNA guanine transglycosylase catalytic subunit QTRT1. Biomolecules 2018; 8:81 [View Article] [PubMed]
     [Google Scholar]
  40. Stengl B, Reuter K, Klebe G. Mechanism and substrate specificity of tRNA-guanine transglycosylases (TGTs): tRNA-modifying enzymes from the three different kingdoms of life share a common catalytic mechanism. Chembiochem 2005; 6:1926–1939 [View Article] [PubMed]
     [Google Scholar]
  41. Pan X, Chandrasekaran S, Woodside JV, Riedel-Heller SG, Scherer M et al. Development, validation and application of an LC-MS/MS method quantifying free forms of the micronutrients queuine and queuosine in human plasma using a surrogate matrix approach. Biochemistry 2024 [View Article]
     [Google Scholar]
  42. Quaiyum S, Yuan Y, Kuipers PJ, Martinelli M, Jaroch M et al. Deciphering the diversity in bacterial transporters that salvage queuosine precursors. Epigenomes 2024; 8:16 [View Article] [PubMed]
     [Google Scholar]
  43. Quaiyum S, Sun J, Marchand V, Sun G, Reed CJ et al. Mapping the tRNA modification landscape of Bartonella henselae Houston I and Bartonella quintana Toulouse. Front Microbiol 2024; 15:1369018 [View Article]
     [Google Scholar]
  44. Slany RK, Bösl M, Kersten H. Transfer and isomerization of the ribose moiety of AdoMet during the biosynthesis of queuosine tRNAs, a new unique reaction catalyzed by the QueA protein from Escherichia coli. Biochimie 1994; 76:389–393 [View Article] [PubMed]
     [Google Scholar]
  45. Boccaletto P, Machnicka MA, Purta E, Piatkowski P, Baginski B et al. MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res 2018; 46:D303–D307 [View Article] [PubMed]
     [Google Scholar]
  46. Ferla MP, Thrash JC, Giovannoni SJ, Patrick WM. New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability. PLoS One 2013; 8:e83383 [View Article] [PubMed]
     [Google Scholar]
  47. Cermakian N, Cedergren R. Modified nucleosides always were: an evolutionary model. In Grosjean H, Benne R. eds Modification and Editing of RNA Washington, D. C: ASM Press; 1998 pp 535–541 [View Article]
     [Google Scholar]
  48. Garzón MJ, Reyes-Prieto M, Gil R. The minimal translation machinery: what we can learn from naturally and experimentally reduced genomes. Front Microbiol 2022; 13:858983 [View Article] [PubMed]
     [Google Scholar]
  49. Yan F, Xiang S, Shi L, Zhu X. Synthesis of queuine by colonic gut microbiome via cross‐feeding. Food Frontiers 2024; 5:174–187 [View Article]
     [Google Scholar]
  50. Grosjean H, Breton M, Sirand-Pugnet P, Tardy F, Thiaucourt F et al. Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes. PLoS Genet 2014; 10:e1004363 [View Article] [PubMed]
     [Google Scholar]
  51. de Crécy-Lagard V, Marck C, Grosjean H. Decoding in candidatus Riesia pediculicola, close to a minimal tRNA modification set?. Trends Cell Mol Biol 2012; 7:11–34 [PubMed]
     [Google Scholar]
  52. Murray GGR, Charlesworth J, Miller EL, Casey MJ, Lloyd CT et al. Genome reduction is associated with bacterial pathogenicity across different scales of temporal and ecological divergence. Mol Biol Evol 2021; 38:1570–1579 [View Article] [PubMed]
     [Google Scholar]
  53. McClure EE, Chávez ASO, Shaw DK, Carlyon JA, Ganta RR et al. Engineering of obligate intracellular bacteria: progress, challenges and paradigms. Nat Rev Microbiol 2017; 15:544–558 [View Article] [PubMed]
     [Google Scholar]
  54. Loterio RK, Zamboni DS, Newton HJ. Keeping the host alive - lessons from obligate intracellular bacterial pathogens. Pathog Dis 2021; 79:ftab052 [View Article] [PubMed]
     [Google Scholar]
  55. Alsmark CM, Frank AC, Karlberg EO, Legault B-A, Ardell DH et al. The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae. Proc Natl Acad Sci U S A 2004; 101:9716–9721 [View Article] [PubMed]
     [Google Scholar]
  56. Omasits U, Quebatte M, Stekhoven DJ, Fortes C, Roschitzki B et al. Directed shotgun proteomics guided by saturated RNA-seq identifies a complete expressed prokaryotic proteome. Genome Res 2013; 23:1916–1927 [View Article] [PubMed]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.001490
Loading
Queuosine salvage in Bartonella henselae Houston 1: a unique evolutionary path
Microbiology 170, 001490 (2024); https://doi.org/10.1099/mic.0.001490
/content/journal/micro/10.1099/mic.0.001490
/content/journal/micro/10.1099/mic.0.001490
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error