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Assignment of function to a domain of unknown function: DUF1537 is a new kinase family in catabolic pathways for acid sugars.

Zhang X, Carter MS, Vetting MW, San Francisco B, Zhao S, Al-Obaidi NF, Solbiati JO, Thiaville JJ, de Crécy-Lagard V, Jacobson MP, Almo SC, Gerlt JA
Proc Natl Acad Sci U S A 113 E4161-9 (2016)
Related entries: 4xfr, 4xg0, 4xgj

Cited: 30 times
EuropePMC logo PMID: 27402745

Abstract

Using a large-scale "genomic enzymology" approach, we (i) assigned novel ATP-dependent four-carbon acid sugar kinase functions to members of the DUF1537 protein family (domain of unknown function; Pfam families PF07005 and PF17042) and (ii) discovered novel catabolic pathways for d-threonate, l-threonate, and d-erythronate. The experimentally determined ligand specificities of several solute binding proteins (SBPs) for TRAP (tripartite ATP-independent permease) transporters for four-carbon acids, including d-erythronate and l-erythronate, were used to constrain the substrates for the catabolic pathways that degrade the SBP ligands to intermediates in central carbon metabolism. Sequence similarity networks and genome neighborhood networks were used to identify the enzyme components of the pathways. Conserved genome neighborhoods encoded SBPs as well as permease components of the TRAP transporters, members of the DUF1537 family, and a member of the 4-hydroxy-l-threonine 4-phosphate dehydrogenase (PdxA) oxidative decarboxylase, class II aldolase, or ribulose 1,5-bisphosphate carboxylase/oxygenase, large subunit (RuBisCO) superfamily. Because the characterized substrates of members of the PdxA, class II aldolase, and RuBisCO superfamilies are phosphorylated, we postulated that the members of the DUF1537 family are novel ATP-dependent kinases that participate in catabolic pathways for four-carbon acid sugars. We determined that (i) the DUF1537/PdxA pair participates in a pathway for the conversion of d-threonate to dihydroxyacetone phosphate and CO2 and (ii) the DUF1537/class II aldolase pair participates in pathways for the conversion of d-erythronate and l-threonate (epimers at carbon-3) to dihydroxyacetone phosphate and CO2 The physiological importance of these pathways was demonstrated in vivo by phenotypic and genetic analyses.

Articles - 4xfm mentioned but not cited (2)

  1. Assignment of function to a domain of unknown function: DUF1537 is a new kinase family in catabolic pathways for acid sugars. Zhang X, Carter MS, Vetting MW, San Francisco B, Zhao S, Al-Obaidi NF, Solbiati JO, Thiaville JJ, de Crécy-Lagard V, Jacobson MP, Almo SC, Gerlt JA. Proc Natl Acad Sci U S A 113 E4161-9 (2016)
  2. Functional annotation of uncharacterized proteins from Fusobacterium nucleatum: identification of virulence factors. Rauthan K, Joshi S, Kumar L, Goel D, Kumar S. Genomics Inform 21 e21 (2023)


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  2. Genomic Enzymology: Web Tools for Leveraging Protein Family Sequence-Function Space and Genome Context to Discover Novel Functions. Gerlt JA. Biochemistry 56 4293-4308 (2017)
  3. 'Democratized' genomic enzymology web tools for functional assignment. Zallot R, Oberg NO, Gerlt JA. Curr Opin Chem Biol 47 77-85 (2018)
  4. Biocatalytic Phosphorylations of Metabolites: Past, Present, and Future. Wohlgemuth R, Liese A, Streit W. Trends Biotechnol 35 452-465 (2017)
  5. A Survey of Pyridoxal 5'-Phosphate-Dependent Proteins in the Gram-Positive Model Bacterium Bacillus subtilis. Richts B, Rosenberg J, Commichau FM. Front Mol Biosci 6 32 (2019)
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  8. Underground metabolism facilitates the evolution of novel pathways for vitamin B6 biosynthesis. Richts B, Commichau FM. Appl Microbiol Biotechnol 105 2297-2305 (2021)
  9. Unraveling the Diverse Roles of Neglected Genes Containing Domains of Unknown Function (DUFs): Progress and Perspective. Lv P, Wan J, Zhang C, Hina A, Al Amin GM, Begum N, Zhao T. Int J Mol Sci 24 4187 (2023)

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  1. The EFI Web Resource for Genomic Enzymology Tools: Leveraging Protein, Genome, and Metagenome Databases to Discover Novel Enzymes and Metabolic Pathways. Zallot R, Oberg N, Gerlt JA. Biochemistry 58 4169-4182 (2019)
  2. The Escherichia coli transcriptome mostly consists of independently regulated modules. Sastry AV, Gao Y, Szubin R, Hefner Y, Xu S, Kim D, Choudhary KS, Yang L, King ZA, Palsson BO. Nat Commun 10 5536 (2019)
  3. Parallel evolution of non-homologous isofunctional enzymes in methionine biosynthesis. Bastard K, Perret A, Mariage A, Bessonnet T, Pinet-Turpault A, Petit JL, Darii E, Bazire P, Vergne-Vaxelaire C, Brewee C, Debard A, Pellouin V, Besnard-Gonnet M, Artiguenave F, Médigue C, Vallenet D, Danchin A, Zaparucha A, Weissenbach J, Salanoubat M, de Berardinis V. Nat Chem Biol 13 858-866 (2017)
  4. Elucidation of the trigonelline degradation pathway reveals previously undescribed enzymes and metabolites. Perchat N, Saaidi PL, Darii E, Pellé C, Petit JL, Besnard-Gonnet M, de Berardinis V, Dupont M, Gimbernat A, Salanoubat M, Fischer C, Perret A. Proc Natl Acad Sci U S A 115 E4358-E4367 (2018)
  5. Functional assignment of multiple catabolic pathways for D-apiose. Carter MS, Zhang X, Huang H, Bouvier JT, Francisco BS, Vetting MW, Al-Obaidi N, Bonanno JB, Ghosh A, Zallot RG, Andersen HM, Almo SC, Gerlt JA. Nat Chem Biol 14 696-705 (2018)
  6. The human respiratory tract microbial community structures in healthy and cystic fibrosis infants. Pust MM, Wiehlmann L, Davenport C, Rudolf I, Dittrich AM, Tümmler B. NPJ Biofilms Microbiomes 6 61 (2020)
  7. Single-Cell Genomics of Novel Actinobacteria With the Wood-Ljungdahl Pathway Discovered in a Serpentinizing System. Merino N, Kawai M, Boyd ES, Colman DR, McGlynn SE, Nealson KH, Kurokawa K, Hongoh Y. Front Microbiol 11 1031 (2020)
  8. Unraveling the functions of uncharacterized transcription factors in Escherichia coli using ChIP-exo. Gao Y, Lim HG, Verkler H, Szubin R, Quach D, Rodionova I, Chen K, Yurkovich JT, Cho BK, Palsson BO. Nucleic Acids Res 49 9696-9710 (2021)
  9. Characterization of an l-Ascorbate Catabolic Pathway with Unprecedented Enzymatic Transformations. Stack TMM, Morrison KN, Dettmer TM, Wille B, Kim C, Joyce R, Jermain M, Naing YT, Bhatti K, Francisco BS, Carter MS, Gerlt JA. J Am Chem Soc 142 1657-1661 (2020)
  10. First Occurrence of the OXA-198 Carbapenemase in Enterobacterales. Bonnin RA, Jousset AB, Gauthier L, Emeraud C, Girlich D, Sauvadet A, Cotellon G, Jové T, Dortet L, Naas T. Antimicrob Agents Chemother 64 e01471-19 (2020)
  11. AGeNNT: annotation of enzyme families by means of refined neighborhood networks. Kandlinger F, Plach MG, Merkl R. BMC Bioinformatics 18 274 (2017)
  12. RUS6, a DUF647-containing protein, is essential for early embryonic development in Arabidopsis thaliana. Perry N, Leasure CD, Tong H, Duarte EM, He ZH. BMC Plant Biol 21 232 (2021)
  13. Evaluating Eucalyptus leaf colonization by Brasilonema octagenarum (Cyanobacteria, Scytonemataceae) using in planta experiments and genomics. Alvarenga DO, Franco MW, Sivonen K, Fiore MF, Varani AM. PeerJ 8 e9158 (2020)
  14. Identification of putative essential protein domains from high-density transposon insertion sequencing. Rahman ASMZ, Timmerman L, Gallardo F, Cardona ST. Sci Rep 12 962 (2022)
  15. Linkage and association analyses reveal that hub genes in energy-flow and lipid biosynthesis pathways form a cluster in upland cotton. Gong J, Peng Y, Yu J, Pei W, Zhang Z, Fan D, Liu L, Xiao X, Liu R, Lu Q, Li P, Shang H, Shi Y, Li J, Ge Q, Liu A, Deng X, Fan S, Pan J, Chen Q, Yuan Y, Gong W. Comput Struct Biotechnol J 20 1841-1859 (2022)
  16. Pyridoxal 5'-phosphate synthesis and salvage in Bacteria and Archaea: predicting pathway variant distributions and holes. Denise R, Babor J, Gerlt JA, de Crécy-Lagard V. Microb Genom 9 (2023)
  17. Construction of a synthetic metabolic pathway for biosynthesis of 2,4-dihydroxybutyric acid from ethylene glycol. Frazão CJR, Wagner N, Rabe K, Walther T. Nat Commun 14 1931 (2023)
  18. Designing phage cocktails to combat the emergence of bacteriophage-resistant mutants in multidrug-resistant Klebsiella pneumoniae. Yoo S, Lee K-M, Kim N, Vu TN, Abadie R, Yong D. Microbiol Spectr 12 e0125823 (2024)
  19. Erythronate utilization activates VdtR regulating its metabolism to promote Brucella proliferation, inducing abortion in mice. Yin Y, Fang T, Lian Z, Zuo D, Hu H, Zhang G, Ding C, Tian M, Yu S. Microbiol Spectr e0207423 (2023)


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