1887

Microbiology Society logo

Volume 169, Issue 3

Characterization of the -arabinofuranose-specific GafABCD ABC transporter essential for -arabinose-dependent growth of the lignocellulose-degrading bacterium sp. ANA-3 Open Access

Abstract

Microbes that have evolved to live on lignocellulosic biomass face unique challenges in the effective and efficient use of this material as food. The bacterium sp. ANA-3 has the potential to utilize arabinan and arabinoxylan, and uptake of the monosaccharide, -arabinose, derived from these polymers, is known to be mediated by a single ABC transporter. We demonstrate that the substrate binding protein of this system, GafA, binds specifically to -arabinofuranose, which is the rare furanose form of -arabinose found in lignocellulosic biomass. The structure of GafA was resolved to 1.7 Å and comparison to YtfQ (GafA) revealed binding site adaptations that confer specificity for furanose over pyranose forms of monosaccharides, while selecting arabinose over another related monosaccharide, galactose. The discovery of a bacterium with a natural predilection for a sugar found abundantly in certain lignocellulosic materials suggests an intimate connection in the enzymatic release and uptake of the sugar, perhaps to prevent other microbes scavenging this nutrient before it mutarotates to -arabinopyranose. This biological discovery also provides a clear route to engineer more efficient utilization of plant biomass components in industrial biotechnology.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): ABC transporter , arabinose , Shewanella , solute transporter and sugars
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/F0147591)
    • Principle Award Recipient: JudithHawkhead
© 2023 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.0.001308
2023-03-15
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/3/mic001308.html?itemId=/content/journal/micro/10.1099/mic.0.001308&mimeType=html&fmt=ahah

References

  1. Henderson PJF. Proton-linked sugar transport systems in bacteria. J Bioenerg Biomembr 1990; 22:525–569 [View Article] [PubMed]
     [Google Scholar]
  2. Saier MH. Families of transmembrane sugar transport proteins. Mol Microbiol 2000; 35:699–710 [View Article] [PubMed]
     [Google Scholar]
  3. Thomas GH. Sialic acid acquisition in bacteria-one substrate, many transporters. Biochem Soc Trans 2016; 44:760–765 [View Article] [PubMed]
     [Google Scholar]
  4. Henderson PJF. Sugar transport proteins. Curr Opin Struct Biol 1991; 1:590–601 [View Article]
     [Google Scholar]
  5. Davidson AL, Dassa E, Orelle C, Chen J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 2008; 72:317–364 [View Article]
     [Google Scholar]
  6. Maqbool A, Horler RSP, Muller A, Wilkinson AJ, Wilson KS et al. The substrate-binding protein in bacterial ABC transporters: dissecting roles in the evolution of substrate specificity. Biochem Soc Trans 2015; 43:1011–1017 [View Article] [PubMed]
     [Google Scholar]
  7. Mowbray SL, Petsko GA. The X-ray structure of the periplasmic galactose binding protein from Salmonella typhimurium at 3.0-Å resolution. J Biol Chem 1983; 258:7991–7997 [View Article]
     [Google Scholar]
  8. Gilliland GL, Quiocho FA. Structure of the L-arabinose-binding protein from Escherichia coli at 2.4 Å resolution. J Mol Biol 1981; 146:341–362 [View Article]
     [Google Scholar]
  9. Mao B, Pear MR, McCammon JA, Quiocho FA. Hinge-bending in L-arabinose-binding protein. The “Venus’s-flytrap” model. J Biol Chem 1982; 257:1131–1133
     [Google Scholar]
  10. Quiocho FA, Pflugrath JW. The structure of D-galactose-binding protein at 4.1 Å resolution looks like L-arabinose-binding protein. J Biol Chem 1980; 255:6559–51 [View Article] [PubMed]
     [Google Scholar]
  11. Horler RSP, Müller A, Williamson DC, Potts JR, Wilson KS et al. Furanose-specific sugar transport: characterization of a bacterial galactofuranose-binding protein. J Biol Chem 2009; 284:31156–31163 [View Article] [PubMed]
     [Google Scholar]
  12. Bagaria A, Kumaran D, Burley SK, Swaminathan S. Structural basis for a ribofuranosyl binding protein: insights into the furanose specific transport. Proteins 2011; 79:1352–1357 [View Article] [PubMed]
     [Google Scholar]
  13. Dodd D, Cann IKO. Enzymatic deconstruction of xylan for biofuel production. Glob Change Biol Bioenergy 2009; 1:2–17 [View Article] [PubMed]
     [Google Scholar]
  14. Shulami S, Raz-Pasteur A, Tabachnikov O, Gilead-Gropper S, Shner I et al. The L-Arabinan utilization system of Geobacillus stearothermophilus. J Bacteriol 2011; 193:2838–2850 [View Article]
     [Google Scholar]
  15. Ndeh D, Rogowski A, Cartmell A, Luis AS, Baslé A et al. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature 2017; 544:65–70 [View Article] [PubMed]
     [Google Scholar]
  16. Adelsberger H, Hertel C, Glawischnig E, Zverlov VV, Schwarz WH. Enzyme system of Clostridium stercorarium for hydrolysis of arabinoxylan: reconstitution of the in vivo system from recombinant enzymes. Microbiology 2004; 150:2257–2266 [View Article]
     [Google Scholar]
  17. Konishi T, Takeda T, Miyazaki Y, Ohnishi-Kameyama M, Hayashi T et al. A plant mutase that interconverts UDP-arabinofuranose and UDP-arabinopyranose. Glycobiology 2007; 17:345–354 [View Article] [PubMed]
     [Google Scholar]
  18. Qaseem MF, Shaheen H, Wu AM. Cell wall hemicellulose for sustainable industrial utilization. Renew Sustain Energy Rev 2021; 144:110996 [View Article]
     [Google Scholar]
  19. Cartmell A, McKee LS, Peña MJ, Larsbrink J, Brumer H et al. The structure and function of an arabinan-specific alpha-1,2-arabinofuranosidase identified from screening the activities of bacterial GH43 glycoside hydrolases. J Biol Chem 2011; 286:15483–15495 [View Article] [PubMed]
     [Google Scholar]
  20. Franks F. Physical chemistry of small carbohydrates - equilibrium solution properties. Pure and Appl Chemist 1987; 59:1189–1202 [View Article]
     [Google Scholar]
  21. Stringer AM, Currenti S, Bonocora RP, Baranowski C, Petrone BL et al. Genome-scale analyses of Escherichia coli and Salmonella enterica AraC reveal noncanonical targets and an expanded core regulon. J Bacteriol 2014; 196:660–671 [View Article]
     [Google Scholar]
  22. Li M, Müller C, Fröhlich K, Gorka O, Zhang L et al. Detection and characterization of a mycobacterial L-arabinofuranose ABC transporter identified with a rapid lipoproteomics protocol. Cell Chem Biol 2019; 26:852–862 [View Article]
     [Google Scholar]
  23. Gunina A, Kuzyakov Y. Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 2015; 90:87–100 [View Article]
     [Google Scholar]
  24. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK et al. MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 2010; 38:D396–400 [View Article] [PubMed]
     [Google Scholar]
  25. Price MN, Wetmore KM, Waters RJ, Callaghan M, Ray J et al. Mutant phenotypes for thousands of bacterial genes of unknown function. Nature 2018; 557:503–509 [View Article] [PubMed]
     [Google Scholar]
  26. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
     [Google Scholar]
  27. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article]
     [Google Scholar]
  28. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 2008; 36:W465–W469 [View Article]
     [Google Scholar]
  29. Guindon S, Lethiec F, Duroux P, Gascuel O. PHYML Online--A web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research 2005; 33:W557–W559 [View Article]
     [Google Scholar]
  30. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  31. Quan S, Hiniker A, Collet JF, Bardwell JCA. Isolation of bacteria envelope proteins. Methods Mol Biol 2013; 966:359–366 [View Article] [PubMed]
     [Google Scholar]
  32. Evans PR. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr D Biol Crystallogr 2011; 67:282–292 [View Article]
     [Google Scholar]
  33. Vagin A, Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 2010; 66:22–25 [View Article]
     [Google Scholar]
  34. Lebedev AA, Vagin AA, Murshudov GN. Model preparation in MOLREP and examples of model improvement using X-ray data. Acta Crystallogr D Biol Crystallogr 2008; 64:33–39 [View Article]
     [Google Scholar]
  35. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 2011; 67:355–367 [View Article]
     [Google Scholar]
  36. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010; 66:486–501 [View Article] [PubMed]
     [Google Scholar]
  37. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004; 60:2256–2268 [View Article]
     [Google Scholar]
  38. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 2014; 42:D206–14 [View Article] [PubMed]
     [Google Scholar]
  39. Watanabe S, Shimada N, Tajima K, Kodaki T, Makino K. Identification and characterization of L-arabonate dehydratase, L-2-keto-3-deoxyarabonate dehydratase, and L-arabinolactonase involved in an alternative pathway of L-arabinose metabolism. Novel evolutionary insight into sugar metabolism. J Biol Chem 2006; 281:33521–33536 [View Article]
     [Google Scholar]
  40. Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY et al. RegPrecise 3.0--A resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genomics 2013; 14:745 [View Article] [PubMed]
     [Google Scholar]
  41. Rodionov DA, Yang C, Li X, Rodionova IA, Wang Y et al. Genomic encyclopedia of sugar utilization pathways in the Shewanella genus. BMC Genomics 2010; 11:1–19 [View Article]
     [Google Scholar]
  42. Mauchline TH, Fowler JE, East AK, Sartor AL, Zaheer R et al. Mapping the Sinorhizobium meliloti 1021 solute-binding protein-dependent transportome. Proc Natl Acad Sci 2006; 103:17933–17938 [View Article]
     [Google Scholar]
  43. Maqbool A, Levdikov VM, Blagova EV, Hervé M, Horler RSP et al. Compensating stereochemical changes allow murein tripeptide to be accommodated in a conventional peptide-binding protein. J Biol Chem 2011; 286:31512–31521 [View Article] [PubMed]
     [Google Scholar]
  44. Vetting MW, Al-Obaidi N, Zhao S, San Francisco B, Kim J et al. Experimental strategies for functional annotation and metabolism discovery: targeted screening of solute binding proteins and unbiased panning of metabolomes. Biochemistry 2015; 54:909–931 [View Article] [PubMed]
     [Google Scholar]
  45. Berntsson RP-A, Smits SHJ, Schmitt L, Slotboom D-J, Poolman B. A structural classification of substrate-binding proteins. FEBS Lett 2010; 584:2606–2617 [View Article] [PubMed]
     [Google Scholar]
  46. Scheepers GH, Lycklama a Nijeholt JA, Poolman B. An updated structural classification of substrate-binding proteins. FEBS Lett 2016; 590:4393–4401 [View Article]
     [Google Scholar]
  47. McNicholas S, Potterton E, Wilson KS, Noble MEM. Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr D Biol Crystallogr 2011; 67:386–394 [View Article]
     [Google Scholar]
  48. Quiocho FA, Vyas NK. Novel stereospecificity of the L-arabinose-binding protein. Nature 1984; 310:381–386 [View Article]
     [Google Scholar]
  49. Rosa LT, Bianconi ME, Thomas GH, Kelly DJ. Tripartite ATP-Independent Periplasmic (TRAP) transporters and Tripartite Tricarboxylate Transporters (TTT): from uptake to pathogenicity. Front Cell Infect Microbiol 2018; 8: [View Article]
     [Google Scholar]
  50. Rosa LT, Springthorpe V, Bianconi ME, Thomas GH, Kelly DJ. Massive over-representation of solute-binding proteins (SBPs) from the tripartite tricarboxylate transporter (TTT) family in the genome of the α-proteobacterium Rhodoplanes sp. Z2-YC6860. Microb Genom 2018; 4:e000176 [View Article]
     [Google Scholar]
  51. Ortega Á, Matilla MA, Krell T, Gao B. The repertoire of solute-binding proteins of model bacteria reveals large differences in number, type, and Ligand range. Microbiol Spectr 2022; 10:e0205422 [View Article]
     [Google Scholar]
  52. Scheepers GH, Lycklama A Nijeholt JA, Poolman B. An updated structural classification of substrate-binding proteins. FEBS Lett 2016; 590:4393–4401 [View Article] [PubMed]
     [Google Scholar]
  53. Elbourne LDH, Tetu SG, Hassan KA, Paulsen IT. TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res 2017; 45:D320–D324 [View Article]
     [Google Scholar]
  54. Mulligan C, Kelly DJ, Thomas GH. Tripartite ATP-independent periplasmic transporters: application of a relational database for genome-wide analysis of transporter gene frequency and organization. J Mol Microbiol Biotechnol 2007; 12:218–226 [View Article] [PubMed]
     [Google Scholar]
  55. Bourdès A, Rudder S, East AK, Poole PS. Mining the Sinorhizobium meliloti transportome to develop FRET biosensors for sugars, dicarboxylates and cyclic polyols. PLoS One 2012; 7:e43578 [View Article]
     [Google Scholar]
  56. Vriezen JAC, de Bruijn FJ, Nüsslein K. Identification and characterization of a NaCl-responsive genetic locus involved in survival during desiccation in Sinorhizobium meliloti. Appl Environ Microbiol 2013; 79:5693–5700 [View Article]
     [Google Scholar]
  57. Zevenhuizen L, Faleschini P. Effect of the concentration of sodium chloride in the medium on the relative proportions of poly- and oligo-saccharides excreted by Rhizobium meliloti strain YE-2SL. Carbohydr Res 1991; 209:203–209 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001308
Loading
Characterization of the l-arabinofuranose-specific GafABCD ABC transporter essential for l-arabinose-dependent growth of the lignocellulose-degrading bacterium Shewanella sp. ANA-3
Microbiology 169, 001308 (2023); https://doi.org/10.1099/mic.0.001308
/content/journal/micro/10.1099/mic.0.001308
/content/journal/micro/10.1099/mic.0.001308
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

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