4p56 › Citations

Experimental strategies for functional annotation and metabolism discovery: targeted screening of solute binding proteins and unbiased panning of metabolomes.

Figure 1
Figure 2
Figure 3
Vetting MW, Al-Obaidi N, Zhao S, San Francisco B, Kim J, Wichelecki DJ, Bouvier JT, Solbiati JO, Vu H, Zhang X, Rodionov DA, Love JD, Hillerich BS, Seidel RD, Quinn RJ, Osterman AL, Cronan JE, Jacobson MP, Gerlt JA, Almo SC
OpenAccess logo Biochemistry 54 909-31 (2015)

Cited: 63 times
EuropePMC logo PMID: 25540822

Abstract

The rate at which genome sequencing data is accruing demands enhanced methods for functional annotation and metabolism discovery. Solute binding proteins (SBPs) facilitate the transport of the first reactant in a metabolic pathway, thereby constraining the regions of chemical space and the chemistries that must be considered for pathway reconstruction. We describe high-throughput protein production and differential scanning fluorimetry platforms, which enabled the screening of 158 SBPs against a 189 component library specifically tailored for this class of proteins. Like all screening efforts, this approach is limited by the practical constraints imposed by construction of the library, i.e., we can study only those metabolites that are known to exist and which can be made in sufficient quantities for experimentation. To move beyond these inherent limitations, we illustrate the promise of crystallographic- and mass spectrometric-based approaches for the unbiased use of entire metabolomes as screening libraries. Together, our approaches identified 40 new SBP ligands, generated experiment-based annotations for 2084 SBPs in 71 isofunctional clusters, and defined numerous metabolic pathways, including novel catabolic pathways for the utilization of ethanolamine as sole nitrogen source and the use of d-Ala-d-Ala as sole carbon source. These efforts begin to define an integrated strategy for realizing the full value of amassing genome sequence data.

Articles - 4p56 mentioned but not cited (1)

  1. Experimental strategies for functional annotation and metabolism discovery: targeted screening of solute binding proteins and unbiased panning of metabolomes. Vetting MW, Al-Obaidi N, Zhao S, San Francisco B, Kim J, Wichelecki DJ, Bouvier JT, Solbiati JO, Vu H, Zhang X, Rodionov DA, Love JD, Hillerich BS, Seidel RD, Quinn RJ, Osterman AL, Cronan JE, Jacobson MP, Gerlt JA, Almo SC. Biochemistry 54 909-931 (2015)


Reviews citing this publication (14)

  1. Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks. Gerlt JA, Bouvier JT, Davidson DB, Imker HJ, Sadkhin B, Slater DR, Whalen KL. Biochim Biophys Acta 1854 1019-1037 (2015)
  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. Sharing vitamins: Cobamides unveil microbial interactions. Sokolovskaya OM, Shelton AN, Taga ME. Science 369 eaba0165 (2020)
  5. Tripartite ATP-Independent Periplasmic (TRAP) Transporters and Tripartite Tricarboxylate Transporters (TTT): From Uptake to Pathogenicity. Rosa LT, Bianconi ME, Thomas GH, Kelly DJ. Front Cell Infect Microbiol 8 33 (2018)
  6. Discovery of new enzymatic functions and metabolic pathways using genomic enzymology web tools. Zallot R, Oberg N, Gerlt JA. Curr Opin Biotechnol 69 77-90 (2021)
  7. Towards functional characterization of archaeal genomic dark matter. Makarova KS, Wolf YI, Koonin EV. Biochem Soc Trans 47 389-398 (2019)
  8. Methanobactins: from genome to function. Dassama LM, Kenney GE, Rosenzweig AC. Metallomics 9 7-20 (2017)
  9. Selective Nutrient Transport in Bacteria: Multicomponent Transporter Systems Reign Supreme. Davies JS, Currie MJ, Wright JD, Newton-Vesty MC, North RA, Mace PD, Allison JR, Dobson RCJ. Front Mol Biosci 8 699222 (2021)
  10. Converting a Periplasmic Binding Protein into a Synthetic Biosensing Switch through Domain Insertion. Ribeiro LF, Amarelle V, Ribeiro LFC, Guazzaroni ME. Biomed Res Int 2019 4798793 (2019)
  11. Biofuel metabolic engineering with biosensors. Morgan SA, Nadler DC, Yokoo R, Savage DF. Curr Opin Chem Biol 35 150-158 (2016)
  12. Functional characterisation of substrate-binding proteins to address nutrient uptake in marine picocyanobacteria. Ford BA, Sullivan GJ, Moore L, Varkey D, Zhu H, Ostrowski M, Mabbutt BC, Paulsen IT, Shah BS. Biochem Soc Trans 49 2465-2481 (2021)
  13. Discovery of novel pathways for carbohydrate metabolism. Stack TMM, Gerlt JA. Curr Opin Chem Biol 61 63-70 (2021)
  14. Designing optimal experiments in metabolomics. Sørensen MB, Møller JK, Strube ML, Gotfredsen CH. Metabolomics 20 69 (2024)

Articles citing this publication (48)

  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. An updated structural classification of substrate-binding proteins. Scheepers GH, Lycklama A Nijeholt JA, Poolman B. FEBS Lett 590 4393-4401 (2016)
  3. Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics. Shelton AN, Seth EC, Mok KC, Han AW, Jackson SN, Haft DR, Taga ME. ISME J 13 789-804 (2019)
  4. Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. Bergauer K, Fernandez-Guerra A, Garcia JAL, Sprenger RR, Stepanauskas R, Pachiadaki MG, Jensen ON, Herndl GJ. Proc Natl Acad Sci U S A 115 E400-E408 (2018)
  5. Evolution of cyclohexadienyl dehydratase from an ancestral solute-binding protein. Clifton BE, Kaczmarski JA, Carr PD, Gerth ML, Tokuriki N, Jackson CJ. Nat Chem Biol 14 542-547 (2018)
  6. Fragment-Based Screening of a Natural Product Library against 62 Potential Malaria Drug Targets Employing Native Mass Spectrometry. Vu H, Pedro L, Mak T, McCormick B, Rowley J, Liu M, Di Capua A, Williams-Noonan B, Pham NB, Pouwer R, Nguyen B, Andrews KT, Skinner-Adams T, Kim J, Hol WGJ, Hui R, Crowther GJ, Van Voorhis WC, Quinn RJ. ACS Infect Dis 4 431-444 (2018)
  7. 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)
  8. Radical-mediated C-S bond cleavage in C2 sulfonate degradation by anaerobic bacteria. Xing M, Wei Y, Zhou Y, Zhang J, Lin L, Hu Y, Hua G, N Nanjaraj Urs A, Liu D, Wang F, Guo C, Tong Y, Li M, Liu Y, Ang EL, Zhao H, Yuchi Z, Zhang Y. Nat Commun 10 1609 (2019)
  9. Linking Bacillus cereus Genotypes and Carbohydrate Utilization Capacity. Warda AK, Siezen RJ, Boekhorst J, Wells-Bennik MH, de Jong A, Kuipers OP, Nierop Groot MN, Abee T. PLoS One 11 e0156796 (2016)
  10. A bacterial chemoreceptor that mediates chemotaxis to two different plant hormones. Rico-Jiménez M, Roca A, Krell T, Matilla MA. Environ Microbiol 24 3580-3597 (2022)
  11. Prediction of enzymatic pathways by integrative pathway mapping. Calhoun S, Korczynska M, Wichelecki DJ, San Francisco B, Zhao S, Rodionov DA, Vetting MW, Al-Obaidi NF, Lin H, O'Meara MJ, Scott DA, Morris JH, Russel D, Almo SC, Osterman AL, Gerlt JA, Jacobson MP, Shoichet BK, Sali A. Elife 7 e31097 (2018)
  12. Structure to function of an α-glucan metabolic pathway that promotes Listeria monocytogenes pathogenesis. Light SH, Cahoon LA, Halavaty AS, Freitag NE, Anderson WF. Nat Microbiol 2 16202 (2016)
  13. 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)
  14. PELDOR Spectroscopy Reveals Two Defined States of a Sialic Acid TRAP Transporter SBP in Solution. Glaenzer J, Peter MF, Thomas GH, Hagelueken G. Biophys J 112 109-120 (2017)
  15. Tripartite ATP-independent Periplasmic (TRAP) Transporters Use an Arginine-mediated Selectivity Filter for High Affinity Substrate Binding. Fischer M, Hopkins AP, Severi E, Hawkhead J, Bawdon D, Watts AG, Hubbard RE, Thomas GH. J Biol Chem 290 27113-27123 (2015)
  16. Two radical-dependent mechanisms for anaerobic degradation of the globally abundant organosulfur compound dihydroxypropanesulfonate. Liu J, Wei Y, Lin L, Teng L, Yin J, Lu Q, Chen J, Zheng Y, Li Y, Xu R, Zhai W, Liu Y, Liu Y, Cao P, Ang EL, Zhao H, Yuchi Z, Zhang Y. Proc Natl Acad Sci U S A 117 15599-15608 (2020)
  17. ATP-binding Cassette (ABC) Transport System Solute-binding Protein-guided Identification of Novel d-Altritol and Galactitol Catabolic Pathways in Agrobacterium tumefaciens C58. Wichelecki DJ, Vetting MW, Chou L, Al-Obaidi N, Bouvier JT, Almo SC, Gerlt JA. J Biol Chem 290 28963-28976 (2015)
  18. Genomic Reconstruction of Carbohydrate Utilization Capacities in Microbial-Mat Derived Consortia. Leyn SA, Maezato Y, Romine MF, Rodionov DA. Front Microbiol 8 1304 (2017)
  19. Structural and mechanistic analysis of a tripartite ATP-independent periplasmic TRAP transporter. Peter MF, Ruland JA, Depping P, Schneberger N, Severi E, Moecking J, Gatterdam K, Tindall S, Durand A, Heinz V, Siebrasse JP, Koenig PA, Geyer M, Ziegler C, Kubitscheck U, Thomas GH, Hagelueken G. Nat Commun 13 4471 (2022)
  20. Novel Metabolic Pathways and Regulons for Hexuronate Utilization in Proteobacteria. Bouvier JT, Sernova NV, Ghasempur S, Rodionova IA, Vetting MW, Al-Obaidi NF, Almo SC, Gerlt JA, Rodionov DA. J Bacteriol 201 e00431-18 (2019)
  21. Development of a target identification approach using native mass spectrometry. Liu M, Van Voorhis WC, Quinn RJ. Sci Rep 11 2387 (2021)
  22. Structural basis for high-affinity adipate binding to AdpC (RPA4515), an orphan periplasmic-binding protein from the tripartite tricarboxylate transporter (TTT) family in Rhodopseudomonas palustris. Rosa LT, Dix SR, Rafferty JB, Kelly DJ. FEBS J 284 4262-4277 (2017)
  23. Structure and mechanism of a tripartite ATP-independent periplasmic TRAP transporter. Davies JS, Currie MJ, North RA, Scalise M, Wright JD, Copping JM, Remus DM, Gulati A, Morado DR, Jamieson SA, Newton-Vesty MC, Abeysekera GS, Ramaswamy S, Friemann R, Wakatsuki S, Allison JR, Indiveri C, Drew D, Mace PD, Dobson RCJ. Nat Commun 14 1120 (2023)
  24. 129Xe NMR-Protein Sensor Reveals Cellular Ribose Concentration. Zemerov SD, Roose BW, Farenhem KL, Zhao Z, Stringer MA, Goldman AR, Speicher DW, Dmochowski IJ. Anal Chem 92 12817-12824 (2020)
  25. Bacterial catabolism of membrane phospholipids links marine biogeochemical cycles. Westermann LM, Lidbury IDEA, Li CY, Wang N, Murphy ARJ, Aguilo Ferretjans MDM, Quareshy M, Shanmugan M, Torcello-Requena A, Silvano E, Zhang YZ, Blindauer CA, Chen Y, Scanlan DJ. Sci Adv 9 eadf5122 (2023)
  26. Structural and biochemical characterization of Rv0187, an O-methyltransferase from Mycobacterium tuberculosis. Lee S, Kang J, Kim J. Sci Rep 9 8059 (2019)
  27. Sensing preferences for prokaryotic solute binding protein families. Cerna-Vargas JP, Sánchez-Romera B, Matilla MA, Ortega Á, Krell T. Microb Biotechnol 16 1823-1833 (2023)
  28. The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range. Ortega Á, Matilla MA, Krell T. Microbiol Spectr 10 e0205422 (2022)
  29. Carbohydrate uptake in Advenella mimigardefordensis strain DPN7T is mediated by periplasmic sugar oxidation and a TRAP-transport system. Meinert C, Senger J, Witthohn M, Wübbeler JH, Steinbüchel A. Mol Microbiol 104 916-930 (2017)
  30. Collision-Induced Affinity Selection Mass Spectrometry for Identification of Ligands. Mak T, Rossjohn J, Littler DR, Liu M, Quinn RJ. ACS Bio Med Chem Au 2 450-455 (2022)
  31. The Birth of Genomic Enzymology: Discovery of the Mechanistically Diverse Enolase Superfamily. Allen KN, Whitman CP. Biochemistry 60 3515-3528 (2021)
  32. Transcriptome analysis and anaerobic C4 -dicarboxylate transport in Actinobacillus succinogenes. Rhie MN, Park B, Ko HJ, Choi IG, Kim OB. Microbiologyopen 7 e00565 (2018)
  33. Structure of an ABC transporter solute-binding protein specific for the amino sugars glucosamine and galactosamine. Yadava U, Vetting MW, Al Obaidi N, Carter MS, Gerlt JA, Almo SC. Acta Crystallogr F Struct Biol Commun 72 467-472 (2016)
  34. Transport capabilities of environmental Pseudomonads for sulfur compounds. Zerbs S, Korajczyk PJ, Noirot PH, Collart FR. Protein Sci 26 784-795 (2017)
  35. A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain. Wu R, Wilton R, Cuff ME, Endres M, Babnigg G, Edirisinghe JN, Henry CS, Joachimiak A, Schiffer M, Pokkuluri PR. Protein Sci 26 857-869 (2017)
  36. Characterization of the l-arabinofuranose-specific GafABCD ABC transporter essential for l-arabinose-dependent growth of the lignocellulose-degrading bacterium Shewanella sp. ANA-3. Drousiotis K, Herman R, Hawkhead J, Leech A, Wilkinson A, Thomas GH. Microbiology (Reading) 169 (2023)
  37. Membrane-anchored substrate binding proteins are deployed in secondary TAXI transporters. Roden A, Engelin MK, Pos KM, Geertsma ER. Biol Chem 404 715-725 (2023)
  38. On the pull: periplasmic trapping of sugars before transport. Thomas GH. Mol Microbiol 104 883-888 (2017)
  39. The Salmonella enterica serovar Typhimurium virulence factor STM3169 is a hexuronic acid binding protein component of a TRAP transporter. Herman R, Bennett-Ness C, Maqbool A, Afzal A, Leech A, Thomas GH. Microbiology (Reading) 166 981-987 (2020)
  40. Auxin-mediated regulation of susceptibility to toxic metabolites, c-di-GMP levels, and phage infection in the rhizobacterium Serratia plymuthica. Rico-Jiménez M, Udaondo Z, Krell T, Matilla MA. mSystems 9 e0016524 (2024)
  41. Enhancing catalytic efficiency of Bacillus subtilis laccase BsCotA through active site pocket design. Hou Y, Zhao L, Yue C, Yang J, Zheng Y, Peng W, Lei L. Appl Microbiol Biotechnol 108 460 (2024)
  42. How Bioinformatic Tools Guide Experiments To Resolve the Chaos of Apparently Unlimited Metabolic Variation. Cole JA. J Bacteriol 201 e00628-18 (2019)
  43. Novel functional insights into a modified sugar-binding protein from Synechococcus MITS9220. Ford BA, Michie KA, Paulsen IT, Mabbutt BC, Shah BS. Sci Rep 12 4805 (2022)
  44. PDBe CCDUtils: an RDKit-based toolkit for handling and analysing small molecules in the Protein Data Bank. Kunnakkattu IR, Choudhary P, Pravda L, Nadzirin N, Smart OS, Yuan Q, Anyango S, Nair S, Varadi M, Velankar S. J Cheminform 15 117 (2023)
  45. Structural and biophysical analysis of a Haemophilus influenzae tripartite ATP-independent periplasmic (TRAP) transporter. Currie MJ, Davies JS, Scalise M, Gulati A, Wright JD, Newton-Vesty MC, Abeysekera GS, Subramanian R, Wahlgren WY, Friemann R, Allison JR, Mace PD, Griffin MDW, Demeler B, Wakatsuki S, Drew D, Indiveri C, Dobson RCJ, North RA. Elife 12 RP92307 (2024)
  46. The ultra-high affinity transport proteins of ubiquitous marine bacteria. Clifton BE, Alcolombri U, Uechi GI, Jackson CJ, Laurino P. Nature (2024)
  47. Two new clades recovered at high temperatures provide novel phylogenetic and genomic insights into Candidatus Accumulibacter. Xie X, Deng X, Chen J, Chen L, Yuan J, Chen H, Wei C, Liu X, Qiu G. ISME Commun 4 ycae049 (2024)
  48. Vitamin B12 Auxotrophy in Isolates from the Deep Subsurface of the Iberian Pyrite Belt. Mateos G, Martínez-Bonilla A, Martínez JM, Amils R. Genes (Basel) 14 1339 (2023)


Quick links