Abstract
Streptococcus pneumoniae is a Gram-positive human pathogen that causes millions of infections worldwide with an increasing occurrence of antibiotic resistance. Iron acquisition is essential for its survival and virulence, especially under host-imposed nutritional immunity. S. pneumoniae expresses several ATP-binding cassette (ABC) transporters to facilitate acquisition under iron limitation, including PitABCD, PiaABCD, and PiuBCDA. The substrate specificity of PiuBCDA is not fully established. Herein, we report the backbone 1H, 13C and 15N resonance assignments of the 31 kDa soluble, extracellular domain of the substrate binding protein PiuA in the apo form and in complex with Ga(III) and the catechol siderophore-mimic 4-LICAM. These studies provide valuable information for further functional studies of interactions with other proteins, metals, and small molecules.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andreini C, Putignano V, Rosato A, Banci L (2018) The human iron-proteome. Metallomics 10:1223–1231. https://doi.org/10.1039/c8mt00146d
Cheng W, Li Q, Jiang YL, Zhou CZ, Chen Y (2013) Structures of Streptococcus pneumoniae PiaA and Its Complex with Ferrichrome Reveal Insights into the Substrate Binding and Release of High Affinity Iron Transporters. PLoS One 8:e71451. https://doi.org/10.1371/journal.pone.0071451
Chu BCH, Otten R, Krewulak KD, Mulder FAA, Vogel HJ (2014) The solution structure, binding properties, and dynamics of the bacterial siderophore-binding protein FepB. J Biol Chem 289:29219–29234. https://doi.org/10.1074/jbc.M114.564021
de Boer M, Gouridis G, Vietrov R, Begg SL, Schuurman-Wolters GK, Husada F, Eleftheriadis N, Poolman B, McDevitt CA, Cordes T (2019) Conformational and dynamic plasticity in substrate-binding proteins underlies selective transport in ABC importers. Elife 8:e44652. https://doi.org/10.7554/eLife.44652
Delaglio F, Grzesiek S, Vuister GW, Pfeifer J, Bax A (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293
Delepelaire P (2019) Bacterial ABC transporters of iron containing compounds. Res Microbiol 170:345–357. https://doi.org/10.1016/j.resmic.2019.10.008
Hood MI, Skaar EP (2012) Nutritional immunity: Transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525–537
Hyberts SG, Takeuchi K, Wagner G (2010) Poisson-gap sampling and forward maximum entropy reconstruction for enhancing the resolution and sensitivity of protein NMR data. J Am Chem Soc 132:2145–2147
Hyberts SG, Milbradt AG, Arthanari H, Wagner G (2012) Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson Gap scheduling. J Biomol NMR 52:1–13
Keller RLJ (2004) Cantina Verlag, Goldau
Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, Wayne KJ, Tettelin H, Glass JI, Winkler ME (2007) Genome sequence of Avery’s virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189:38–51. https://doi.org/10.1128/JB.01148-06
Lee W, Tonelli M, Markley JL (2015) NMRFAM-SPARKY: Enhanced software for biomolecular NMR spectroscopy. Bioinformatics 31:1325–1327. https://doi.org/10.1093/bioinformatics/btu830
Lynch JP, Zhanel GG (2010) Streptococcus pneumoniae: epidemiology and risk factors, evolution of antimicrobial resistance, and impact of vaccines. Curr Opin Pulm Med 16:217–225. https://doi.org/10.1097/MCP.0b013e3283385653
Maciejewski MW, Schuyler AD, Gryk MR, Moraru II, Romero PR, Ulrich EL, Eghbalnia HR, Livny M, Delaglio F, Hoch JC (2017) NMRbox: a resource for biomolecular NMR computation. Biophys J 112:1529–1534. https://doi.org/10.1016/j.bpj.2017.03.011
Peroutka RJ, Orcutt SJ, Strickler JE, Butt TR (2011) SUMO fusion technology for enhanced protein expression and purification in prokaryotes and eukaryotes. Methods Mol Biol 705:15–30. https://doi.org/10.1007/978-1-61737-967-3_2
Raines DJ, Moroz OV, Wilson KS, Duhme-Klair A-K (2013) Interactions of a Periplasmic Binding Protein with a Tetradentate Siderophore Mimic. Angew Chemie Int Ed 52:4595–4598. https://doi.org/10.1002/anie.201300751
Raines DJ, Moroz OV, Blagova EV, Turkenburg JP, Wilson KS, Duhme-Klair A-K (2016) Bacteria in an intense competition for iron: key component of the Campylobacter jejuni iron uptake system scavenges enterobactin hydrolysis product. Proc Natl Acad Sci U S A 113:5850–5855. https://doi.org/10.1073/pnas.1520829113
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:320–324. https://doi.org/10.1093/nar/gku316
Salzmann M, Wider G, Pervushin K, Senn H, Wüthrich K (1999) TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins. J Am Chem Soc 121:844–848. https://doi.org/10.1021/ja9834226
Shen Y, Bax A (2014) Protein structural information derived from NMR chemical shift with the neural network program TALOS-N. In: Artificial Neural Networks: Second Edition. Springer, New York, pp 17–32
Wilde EJ, Hughes A, Blagova EV, Moroz OV, Thomas RP, Turkenburg JP, Raines DJ, Duhme-Klair AK, Wilson KS (2017) Interactions of the periplasmic binding protein CeuE with Fe(III) n-LICAM 4- siderophore analogues of varied linker length. Sci Rep 7:1–14. https://doi.org/10.1038/srep45941
Zhang Y, Sen S, Giedroc DP (2020) Iron acquisition by bacterial pathogens: beyond tris-catecholate complexes. ChemBioChem 21:cbic.201900778. https://doi.org/10.1002/cbic.201900778
Acknowledgements
This research was supported by US National Institutes of Health grant R35 GM118157 to D.P.G. and UK Engineering and Physical Sciences Research Council grant EP/L024829/1 to A.K.D.K. We thank Dr. Hongwei Wu for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Edmonds, K.A., Zhang, Y., Raines, D.J. et al. 1H, 13C, 15N backbone resonance assignments of the apo and holo forms of the ABC transporter solute binding protein PiuA from Streptococcus pneumoniae. Biomol NMR Assign 14, 233–238 (2020). https://doi.org/10.1007/s12104-020-09952-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12104-020-09952-9