Structure of the stationary phase survival protein YuiC from B.subtilis

BMC Structural Biology

Nicholas H. Keep¹  Sanjib Bhakta¹  Mark A. Williams¹  Konstantinos Thalassinos²  Adam Cryar²  Ambrose R. Cole¹  Doris H.X. Quay¹ 

[1] Institute for Structural and Molecular Biology, Crystallography, Department of Biological Sciences, Birkbeck University of London, Malet Street, London WC1E 7HX, UK;Institute of Structural and Molecular Biology, Division of Biosciences, University College London, Gower Street, London WC1E 6BT, UK

关键词: Firmicutes;    Resuscitation promoting factors;    Peptidoglycan;    Stationary phase survival;    Dormancy;   

Others  :  1220329
DOI  :  10.1186/s12900-015-0039-z

 received in 2015-03-11, accepted in 2015-07-02,  发布年份 2015

【 摘 要 】

Background

Stationary phase survival proteins (Sps) were found in Firmicutes as having analogous domain compositions, and in some cases genome context, as the resuscitation promoting factors of Actinobacteria, but with a different putative peptidoglycan cleaving domain.

Results

The first structure of a Firmicute Sps protein YuiC from B. subtilis, is found to be a stripped down version of the cell-wall peptidoglycan hydrolase MltA. The YuiC structures are of a domain swapped dimer, although some monomer is also found in solution. The protein crystallised in the presence of pentasaccharide shows a 1,6-anhydrodisaccharide sugar product, indicating that YuiC cleaves the sugar backbone to form an anhydro product at least on lengthy incubation during crystallisation.

Conclusions

The structural simplification of MltA in Sps proteins is analogous to that of the resuscitation promoting factor domains of Actinobacteria, which are stripped down versions of lysozyme and soluble lytic transglycosylase proteins.

【 授权许可】

   
2015 Quay et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

【 参考文献 】

• [1]Tan IS, Ramamurthi KS: Spore formation in Bacillus subtilis. Environ Microbiol Rep 2014, 6(3):212-225.
• [2]Keep NH, Ward JM, Cohen-Gonsaud M, Henderson B: Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol 2006, 14(6):271-276.
• [3]Wayne LG, Sohaskey CD: Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 2001, 55:139-163.
• [4]Shah IM, Dworkin J: Induction and regulation of a secreted peptidoglycan hydrolase by a membrane Ser/Thr kinase that detects muropeptides. Mol Microbiol 2010, 75(5):1232-1243.
• [5]Pascoe B, Dams L, Wilkinson TS, Harris LG, Bodger O, Mack D, et al. Dormant Cells of Staphylococcus aureus Are Resuscitated by Spent Culture Supernatant. Plos One. 2014;9(2):e85998.
• [6]Mukamolova GV, Kaprelyants AS, Young DI, Young M, Kell DB: A bacterial cytokine. Proc Natl Acad Sci U S A 1998, 95(15):8916-8921.
• [7]Cohen-Gonsaud M, Barthe P, Bagneris C, Henderson B, Ward J, Roumestand C, Keep NH: The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat Struct Mol Biol 2005, 12(3):270-273.
• [8]Mukamolova GV, Murzin AG, Salina EG, Demina GR, Kell DB, Kaprelyants AS, Young M: Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol Microbiol 2006, 59(1):84-98.
• [9]Cohen-Gonsaud M, Keep NH, Davies AP, Ward J, Henderson B, Labesse G: Resuscitation-promoting factors possess a lysozyme-like domain. Trends Biochem Sci 2004, 29(1):7-10.
• [10]Keep NH, Ward JM, Robertson G, Cohen-Gonsaud M, Henderson B: Bacterial resuscitation factors: revival of viable but non-culturable bacteria. Cell Mol Life Sci 2006, 63(22):2555-2559.
• [11]Kana BD, Mizrahi V: Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunol Med Microbiol 2010, 58(1):39-50.
• [12]Dworkin J, Shah IM: Exit from dormancy in microbial organisms. Nat Rev Microbiol 2010, 8(12):890-896.
• [13]Nikitushkin VD, Demina GR, Shleeva MO, Kaprelyants AS: Peptidoglycan fragments stimulate resuscitation of "non-culturable" mycobacteria. Antonie Van Leeuwenhoek 2013, 103(1):37-46.
• [14]Ravagnani A, Finan CL, Young M: A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement. BMC Genomics 2005, 6:39. BioMed Central Full Text
• [15]Chauviac FX, Robertson G, Quay DHX, Bagneris C, Dumas C, Henderson B, Ward J, Keep NH, Cohen-Gonsaud M: The RpfC (Rv1884) atomic structure shows high structural conservation within the resuscitation-promoting factor catalytic domain. Acta Crystallogr F Struct Biol Commun 2014, 70(Pt 8):1022-1026.
• [16]Pinto D, Sao-Jose C, Santos MA, Chambel L: Characterization of two resuscitation promoting factors of Listeria monocytogenes. Microbiology 2013, 159:1390-1401.
• [17]Bennett MJ, Schlunegger MP, Eisenberg D: 3D Domain swapping - A mechanism for oligomer assembly. Protein Sci 1995, 4(12):2455-2468.
• [18]Krissinel E, Henrick K: Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007, 372(3):774-797.
• [19]van Straaten KE, Dijkstra BW, Vollmer W, Thunnissen A: Crystal structure of MltA from Escherichia coli reveals a unique lytic transglycosylase fold. J Mol Biol 2005, 352(5):1068-1080.
• [20]van Straaten KE, Barends TRM, Dijkstra BW, Thunnissen A-MWH: Structure of Escherichia coli lytic transglycosylase MltA with bound chitohexaose - Implications for peptidoglycan binding and cleavage. J Biol Chem 2007, 282(29):21197-21205.
• [21]Powell AJ, Liu ZJ, Nicholas RA, Davies C: Crystal structures of the lytic transglycosylase MItA from N. gonorrhoeae and E. coli: Insights into interdomain movements and substrate binding. J Mol Biol 2006, 359(1):122-136.
• [22]Hett EC, Chao MC, Steyn AJ, Fortune SM, Deng LL, Rubin EJ: A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol Microbiol 2007, 66(3):658-668.
• [23]Hett EC, Chao MC, Deng LL, Rubin EJ. A mycobacterial enzyme essential for cell division synergizes with resuscitation-promoting factor. Plos Pathog. 2008;4(2):e1000001.
• [24]Hett EC, Chao MC, Rubin EJ: Interaction and modulation of two antagonistic cell wall enzymes of mycobacteria. Plos Pathog: 2010, 6(7):e1001020.
• [25]Vollmer W, von Rechenberg M, Holtje JV: Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J Biol Chem 1999, 274(10):6726-6734.
• [26]Savitsky P, Bray J, Cooper CDO, Marsden BD, Mahajan P, Burgess-Brown NA, Gileadi O: High-throughput production of human proteins for crystallization: The SGC experience. J Struct Biol 2010, 172(1):3-13.
• [27]Grimm C, Chari A, Reuter K, Fischer U: A crystallization screen based on alternative polymeric precipitants. Acta Crystallogr D Biol Crystallogr 2010, 66:685-697.
• [28]Yao JX, Dodson EJ, Wilson KS, Woolfson MM: ACORN: a review. Acta Crystallogr D Biol Crystallogr 2006, 62:901-908.
• [29]Terwilliger TC, DiMaio F, Read RJ, Baker D, Bunkoczi G, Adams PD, et al. phenix.mr_rosetta: molecular replacement and model rebuilding with Phenix and Rosetta. J Struct Funct Genomics. 2012;13(2, Sp. Iss. SI):81–90.
• [30]Hildebrand A, Remmert M, Biegert A, Söding J: Fast and accurate automatic structure prediction with HHpred. Proteins 2009, 77:128-132.
• [31]Morris RJ, Zwart PH, Cohen S, Fernandez FJ, Kakaris M, Kirillova O, Vonrhein C, Perrakis A, Lamzin VS: Breaking good resolutions with ARP/wARP. J Synchrotron Radiat 2004, 11(Pt 1):56-59.
• [32]Emsley P, Lohkamp B, Scott WG, Cowtan K: Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010, 66(Pt 4):486-501.
• [33]Murshudov GN, Vagin AA, Dodson EJ: Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997, 53(Pt 3):240-255.
• [34]McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ: Phaser crystallographic software. J Appl Crystallogr 2007, 40(Pt 4):658-674.
• [35]Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al.: PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010, 66(Pt 2):213-221.
• [36]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(Pt 12 Nb 1):2256–68.
• [37]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.
• [38]Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE: UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 2004, 25(13):1605-1612.
• [39]Gouet P, Courcelle E, Stuart DI, Metoz F: ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15(4):305-308.