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Cited by 10Bacterial Genetics and BiotechnologyRNA and protein synthesis mechanismsBiochemical and Molecular Research

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Queuosine biosynthetic enzyme, QueE moonlights as a cell division regulator

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Adeleye, Samuel A., Yadavalli, Srujana S.·2024·PLOS Genetics
DOI 10.1371/journal.pgen.1011287PMC PMC11142719

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Abstract

In many organisms, stress responses to adverse environments can trigger secondary functions of certain proteins by altering protein levels, localization, activity, or interaction partners. Escherichia coli cells respond to the presence of specific cationic antimicrobial peptides by strongly activating the PhoQ/PhoP two-component signaling system, which regulates genes important for growth under this stress. As part of this pathway, a biosynthetic enzyme called QueE, which catalyzes a step in the formation of queuosine (Q) tRNA modification is upregulated. When cellular QueE levels are high, it co-localizes with the central cell division protein FtsZ at the septal site, blocking division and resulting in filamentous growth. Here we show that QueE affects cell size in a dose-dependent manner. Using alanine scanning mutagenesis of amino acids in the catalytic active site, we pinpoint residues in QueE that contribute distinctly to each of its functions–Q biosynthesis or regulation of cell division, establishing QueE as a moonlighting protein. We further show that QueE orthologs from enterobacteria like Salmonella typhimurium and Klebsiella pneumoniae also cause filamentation in these organisms, but the more distant counterparts from Pseudomonas aeruginosa and Bacillus subtilis lack this ability. By comparative analysis of E . coli QueE with distant orthologs, we elucidate a unique region in this protein that is responsible for QueE’s secondary function as a cell division regulator. A dual-function protein like QueE is an exception to the conventional model of “one gene, one enzyme, one function”, which has divergent roles across a range of fundamental cellular processes including RNA modification and translation to cell division and stress response.

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Fig 1 Dual roles of E. coli QueE (EcQueE) during stress response. (a) Schematic representation of the dual roles of QueE upon strong activation of the PhoQ/PhoP two-component system. QueE is an enzyme required for the biosynthesis of queuosine (Q) tRNA modification. E. coli cells under strong PhoQP-activating stress conditions such as exposure to sub-MIC levels of specific antimicrobial peptides, upregulate QueE, which then modulates cell division in addition to Q biosynthesis. (b) Methods used to study the two activities of QueE–APB (N-acryloyl-3-aminophenylboronic acid) gel and northern blotting to detect Q-tRNAs and microscopy to observe filamentation. (c) APB gel-northern blot detecting tRNATyr in total RNA samples of E. coli wild-type (WT, MG1655) and ΔqueE (SAM31) cells encoding either an empty vector (pEB52) or wild-type (WT) QueE (pRL03). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (d) Representative phase-contrast micrographs of E. coli wild-type (WT, MG1655) and ΔqueE (SAM31) cells expressing either an empty vector (pEB52) or WT QueE (pRL03), scale bar = 5 μm. For (c) and (d), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with IPTG (“+”) for 3 hours.
Fig 1 Dual roles of E. coli QueE (EcQueE) during stress response. (a) Schematic representation of the dual roles of QueE upon strong activation of the PhoQ/PhoP two-component system. QueE is an enzyme required for the biosynthesis of queuosine (Q) tRNA modification. E. coli cells under strong PhoQP-activating stress conditions such as exposure to sub-MIC levels of specific antimicrobial peptides, upregulate QueE, which then modulates cell division in addition to Q biosynthesis. (b) Methods used to study the two activities of QueE–APB (N-acryloyl-3-aminophenylboronic acid) gel and northern blotting to detect Q-tRNAs and microscopy to observe filamentation. (c) APB gel-northern blot detecting tRNATyr in total RNA samples of E. coli wild-type (WT, MG1655) and ΔqueE (SAM31) cells encoding either an empty vector (pEB52) or wild-type (WT) QueE (pRL03). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (d) Representative phase-contrast micrographs of E. coli wild-type (WT, MG1655) and ΔqueE (SAM31) cells expressing either an empty vector (pEB52) or WT QueE (pRL03), scale bar = 5 μm. For (c) and (d), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with IPTG (“+”) for 3 hours.CC BY · PubMed Central
Fig 2 Effect of dose-dependent expression of EcQueE on septation. (a) Measurement of cell lengths of E. coli MG1655 ΔlacZYA (TIM183) cells expressing QueE. Strains containing a plasmid encoding E. coli QueE (pRL03) or empty vector (pEB52) were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with IPTG for 3 hours at the indicated concentration. Gray circles represent individual cells, mean cell length values are indicated in red, and the horizontal gray bars represent the median. Data are obtained from four independent experiments and the number of cells analyzed for each inducer concentration is indicated by (n). Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05 (b) Representative phase-contrast micrographs of ΔlacZYA cells expressing QueE (pRL03) at the indicated inducer concentration, scale bar = 5 μm.
Fig 2 Effect of dose-dependent expression of EcQueE on septation. (a) Measurement of cell lengths of E. coli MG1655 ΔlacZYA (TIM183) cells expressing QueE. Strains containing a plasmid encoding E. coli QueE (pRL03) or empty vector (pEB52) were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with IPTG for 3 hours at the indicated concentration. Gray circles represent individual cells, mean cell length values are indicated in red, and the horizontal gray bars represent the median. Data are obtained from four independent experiments and the number of cells analyzed for each inducer concentration is indicated by (n). Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05 (b) Representative phase-contrast micrographs of ΔlacZYA cells expressing QueE (pRL03) at the indicated inducer concentration, scale bar = 5 μm.CC BY · PubMed Central
Fig 3 Effect of single alanine substitutions of conserved amino acid residues in EcQueE on Q biosynthesis and cell division. (a) Structure of E. coli QueE (EcQueE, PDB ID 6NHL) showing amino acid residues, catalytically important for Q biosynthesis. (b) Summary of alanine scanning mutagenesis of key amino acid residues in EcQueE and the effect of each mutant on cellular morphology and Q biosynthesis indicated by (+) or (-). (c) APB gel-northern blot detecting tRNATyr in total RNA samples of ΔqueE (SAM31) cells encoding either WT QueE (pRL03), QueE-R27A (pSY98), QueE-C31A (pSA1), QueE-C35A (pSA2) or an empty vector (pEB52). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (d) Representative phase-contrast micrographs of ΔqueE (SAM31) cells expressing WT QueE and selected mutants, scale bar = 5 μm. For (c) and (d), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours.
Fig 3 Effect of single alanine substitutions of conserved amino acid residues in EcQueE on Q biosynthesis and cell division. (a) Structure of E. coli QueE (EcQueE, PDB ID 6NHL) showing amino acid residues, catalytically important for Q biosynthesis. (b) Summary of alanine scanning mutagenesis of key amino acid residues in EcQueE and the effect of each mutant on cellular morphology and Q biosynthesis indicated by (+) or (-). (c) APB gel-northern blot detecting tRNATyr in total RNA samples of ΔqueE (SAM31) cells encoding either WT QueE (pRL03), QueE-R27A (pSY98), QueE-C31A (pSA1), QueE-C35A (pSA2) or an empty vector (pEB52). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (d) Representative phase-contrast micrographs of ΔqueE (SAM31) cells expressing WT QueE and selected mutants, scale bar = 5 μm. For (c) and (d), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours.CC BY · PubMed Central
Fig 4 Role of EcQueE-R27A mutant, deficient in Q biosynthesis, in cell division. (a) Representative phase-contrast and fluorescence micrographs of ΔqueE (SAM96) cells co-expressing FtsZ-mCherry (pEG4) and either YFP-EcQueE (pSY76) or YFP-EcQueE-R27A (pSA58). Cells were grown in supplemented MinA minimal medium for 4 hours, followed by 0.5% arabinose induction for FtsZ-mCherry expression for another 1 hour (please see Methods for details on pSY76 and derivatives). Green and red arrowheads represent the localization of YFP-QueE and FtsZ- mCherry, respectively. (b) Representative phase-contrast micrographs of ΔmgrB and ΔmgrBΔqueE cells containing either an empty plasmid (pEB52), or plasmids expressing EcQueE (pRL03) and EcQueE-R27A (pSY98), scale bar = 5 μm. Cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (c) Quantification of YFP-QueE levels in ΔqueE (SAM96) cells transformed with plasmids encoding YFP-tagged WT EcQueE (pSY76), EcQueE-R27A (pSA58), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 5 hours. Data represent the mean and range from two independent experiments and fluorescence was quantified from the number of cells (n) per sample as indicated. The red dotted line represents the expression level for WT YFP-QueE. (d) Measurement of cell lengths of ΔqueE (SAM96) cells encoding WT EcQueE (pRL03), EcQueE-R27A (pSY98), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. Gray circles represent individual cells, mean cell length values are indicated in red and the horizontal gray bars represent the median. Data are obtained from three independent experiments and the total number of cells (n) per sample is indicated. Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.
Fig 4 Role of EcQueE-R27A mutant, deficient in Q biosynthesis, in cell division. (a) Representative phase-contrast and fluorescence micrographs of ΔqueE (SAM96) cells co-expressing FtsZ-mCherry (pEG4) and either YFP-EcQueE (pSY76) or YFP-EcQueE-R27A (pSA58). Cells were grown in supplemented MinA minimal medium for 4 hours, followed by 0.5% arabinose induction for FtsZ-mCherry expression for another 1 hour (please see Methods for details on pSY76 and derivatives). Green and red arrowheads represent the localization of YFP-QueE and FtsZ- mCherry, respectively. (b) Representative phase-contrast micrographs of ΔmgrB and ΔmgrBΔqueE cells containing either an empty plasmid (pEB52), or plasmids expressing EcQueE (pRL03) and EcQueE-R27A (pSY98), scale bar = 5 μm. Cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (c) Quantification of YFP-QueE levels in ΔqueE (SAM96) cells transformed with plasmids encoding YFP-tagged WT EcQueE (pSY76), EcQueE-R27A (pSA58), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 5 hours. Data represent the mean and range from two independent experiments and fluorescence was quantified from the number of cells (n) per sample as indicated. The red dotted line represents the expression level for WT YFP-QueE. (d) Measurement of cell lengths of ΔqueE (SAM96) cells encoding WT EcQueE (pRL03), EcQueE-R27A (pSY98), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. Gray circles represent individual cells, mean cell length values are indicated in red and the horizontal gray bars represent the median. Data are obtained from three independent experiments and the total number of cells (n) per sample is indicated. Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.CC BY · PubMed Central
Fig 5 Analysis of dual functions of QueE among orthologs from E. coli and closely related genera. (a) APB gel-northern blot detecting tRNATyr in total RNA samples of ΔqueE (SAM31) cells encoding QueE orthologs from E. coli (EcQueE, pRL03), Bacillus subtilis (BsQueE, pSY45), Klebsiella pneumoniae (KpQueE, pSA5), Salmonella Typhimurium (StQueE, pSA21), Pseudomonas aeruginosa (PaQueE, pSA127) and an empty vector (pEB52). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (b) Representative phase-contrast micrographs of ΔqueE (SAM31) cells transformed with plasmids encoding either EcQueE, BsQueE, KpQueE, StQueE, pPaQueE, or an empty vector, scale bar = 5μm. For (a) and (b), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (c) Quantification of YFP-QueE levels in E. coli ΔqueE (SAM96) cells transformed with plasmids encoding YFP-tagged EcQueE (pSY76), BsQueE (pSA121), PaQueE (pSA126), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 5 hours (please see Methods for details on pSY76 and derivatives). Data represent the mean and range from two independent experiments, and fluorescence was quantified from the number of cells (n) per sample as indicated. The red dotted line represents the expression level for WT YFP-QueE, Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.
Fig 5 Analysis of dual functions of QueE among orthologs from E. coli and closely related genera. (a) APB gel-northern blot detecting tRNATyr in total RNA samples of ΔqueE (SAM31) cells encoding QueE orthologs from E. coli (EcQueE, pRL03), Bacillus subtilis (BsQueE, pSY45), Klebsiella pneumoniae (KpQueE, pSA5), Salmonella Typhimurium (StQueE, pSA21), Pseudomonas aeruginosa (PaQueE, pSA127) and an empty vector (pEB52). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr. (b) Representative phase-contrast micrographs of ΔqueE (SAM31) cells transformed with plasmids encoding either EcQueE, BsQueE, KpQueE, StQueE, pPaQueE, or an empty vector, scale bar = 5μm. For (a) and (b), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (c) Quantification of YFP-QueE levels in E. coli ΔqueE (SAM96) cells transformed with plasmids encoding YFP-tagged EcQueE (pSY76), BsQueE (pSA121), PaQueE (pSA126), or an empty vector (pEB52). Cells were grown in supplemented MinA minimal medium for 5 hours (please see Methods for details on pSY76 and derivatives). Data represent the mean and range from two independent experiments, and fluorescence was quantified from the number of cells (n) per sample as indicated. The red dotted line represents the expression level for WT YFP-QueE, Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.CC BY · PubMed Central
Fig 6 Role of region E45-W67 in E. coli QueE in the biosynthesis of Q-tRNA modification. (a) Structural alignment of E. coli QueE (EcQueE, PDB 6NHL, dark gray), Bacillus subtilis QueE (BsQueE, PDB 5TH5, light gray), and an Alphafold-generated model of P. aeruginosa QueE (PaQueE, cyan). The variable region E45-W67 in EcQueE is highlighted in red. (b) APB gel-northern blot showing Q-tRNA profiles of ΔqueE cells (SAM31) containing IPTG inducible plasmids encoding E. coli QueE (pRL03), control vector (pEB52), and selected mutants of EcQueE—pQueE-ΔE45-E51 (pSA60), pQueE-ΔV52-W67 (pSA61), and pQueE-ΔE45-W67 (pSA62). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr (c) Phase contrast micrographs of ΔqueE (SAM31) cells transformed with an empty vector and plasmids encoding Wildtype (WT) EcQueE and the selected EcQueE peptide deletion mutants (as in (a) above), Scale bar = 5 μm. For (b) and (c), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (d) Quantification of QueE levels in ΔqueE (SAM96) cells transformed with an empty vector and IPTG inducible plasmids encoding YFP-tagged wild-type QueE (WT, pSY76) and QueE ΔE45-W67 (pSA76). Cells were grown in supplemented MinA minimal medium for 5 hours (please see Methods for details on pSY76 and derivatives). Dots and the error bars represent the mean and range from two independent experiments with quantified fluorescence, and the total number of cells (n) per sample is indicated. The red dotted line represents the expression levels for WT. Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.
Fig 6 Role of region E45-W67 in E. coli QueE in the biosynthesis of Q-tRNA modification. (a) Structural alignment of E. coli QueE (EcQueE, PDB 6NHL, dark gray), Bacillus subtilis QueE (BsQueE, PDB 5TH5, light gray), and an Alphafold-generated model of P. aeruginosa QueE (PaQueE, cyan). The variable region E45-W67 in EcQueE is highlighted in red. (b) APB gel-northern blot showing Q-tRNA profiles of ΔqueE cells (SAM31) containing IPTG inducible plasmids encoding E. coli QueE (pRL03), control vector (pEB52), and selected mutants of EcQueE—pQueE-ΔE45-E51 (pSA60), pQueE-ΔV52-W67 (pSA61), and pQueE-ΔE45-W67 (pSA62). G-tRNATyr = unmodified tRNATyr, Q-tRNATyr = Q-modified tRNATyr (c) Phase contrast micrographs of ΔqueE (SAM31) cells transformed with an empty vector and plasmids encoding Wildtype (WT) EcQueE and the selected EcQueE peptide deletion mutants (as in (a) above), Scale bar = 5 μm. For (b) and (c), cells were grown in supplemented MinA minimal medium for 2 hours (OD600 = 0.2–0.3) and induced with 0.5 mM IPTG for 3 hours. (d) Quantification of QueE levels in ΔqueE (SAM96) cells transformed with an empty vector and IPTG inducible plasmids encoding YFP-tagged wild-type QueE (WT, pSY76) and QueE ΔE45-W67 (pSA76). Cells were grown in supplemented MinA minimal medium for 5 hours (please see Methods for details on pSY76 and derivatives). Dots and the error bars represent the mean and range from two independent experiments with quantified fluorescence, and the total number of cells (n) per sample is indicated. The red dotted line represents the expression levels for WT. Statistical analysis was done using t-test displaying significance at *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001, and “ns” = P >0.05.CC BY · PubMed Central
Fig 7 QueE’s dual roles in Q-biosynthesis and septation inhibition. (a) Structure of E. coli QueE (PDB 6NHL) showing residue affecting Q-biosynthesis only (green, R27) and septation inhibition only (red, C31, C35, E45-W67). (b) A consensus sequence of the E45-W67 region from 18 representative enterobacteria (see Fig (viii) in S1 Text for details) was generated using WebLogo [71].
Fig 7 QueE’s dual roles in Q-biosynthesis and septation inhibition. (a) Structure of E. coli QueE (PDB 6NHL) showing residue affecting Q-biosynthesis only (green, R27) and septation inhibition only (red, C31, C35, E45-W67). (b) A consensus sequence of the E45-W67 region from 18 representative enterobacteria (see Fig (viii) in S1 Text for details) was generated using WebLogo [71].CC BY · PubMed Central

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Metadata

Authors
Adeleye, S. A., & Yadavalli, S. S.
Affiliations
Rutgers, The State University of New Jersey (US)
Corresponding author
Yadavalli, Srujana S.
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2024-05-20
Volume
20
Issue
5
Pages
e1011287
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1011287
PMC
PMC11142719
OpenAlex
W4398145788
Cited by
10
References
78
Citations by year
2026: 4 · 2025: 6
FWCI
2.65
Type
journal article
Language
en
Update notices
new_version (2024-05-31)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Institute of General Medical Sciences (R35 GM147566)
  • Rutgers, The State University of New Jersey (Institutional start-up funds, Waksman Institute Busch Predoctoral Fellowship)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
Keywords
queuosine biosynthesis, moonlighting proteins, cell division regulation, FtsZ, filamentous growth, tRNA modification, antimicrobial peptides, cell size control, Escherichia coli, Salmonella typhimurium, Klebsiella pneumoniae, Pseudomonas aeruginosa, Bacillus subtilis, enzyme active site residues

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