Crystal Structures of the SpoIID Lytic Transglycosylases Essential for Bacterial Sporulation

Nocadello, Salvatore; Minasov, George; Shuvalova, Ludmilla S.; Dubrovska, Ievgeniia; Sabini, Elisabetta; Anderson, Wayne F.

doi:10.1074/jbc.m116.729749

Title: Crystal Structures of the SpoIID Lytic Transglycosylases Essential for Bacterial Sporulation

Journal Article · Wed May 18 00:00:00 EDT 2016 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m116.729749· OSTI ID:1328045

Nocadello, Salvatore ^[1]; Minasov, George ^[1]; Shuvalova, Ludmilla S. ^[1]; Dubrovska, Ievgeniia ^[1]; Sabini, Elisabetta ^[1]; Anderson, Wayne F. ^[1]

Northwestern Univ. Feinberg School of Medicine, Chicago, IL (United States)

Bacterial spores are the most resistant form of life known on Earth and represent a serious problem for (i) bioterrorism attack, (ii) horizontal transmission of microbial pathogens in the community, and (iii) persistence in patients and in a nosocomial environment. Stage II sporulation proteinD(SpoIID) is a lytic transglycosylase (LT) essential for sporulation. The LT superfamily is a potential drug target because it is active in essential bacterial processes involving the peptidoglycan, which is unique to bacteria. However, the absence of structural information for the sporulation-specific LT enzymes has hindered mechanistic understanding of SpoIID. In this paper, we report the first crystal structures with and without ligands of the SpoIID family from two community relevant spore-forming pathogens, Bacillus anthracis and Clostridium difficile. The structures allow us to visualize the overall architecture, characterize the substrate recognition model, identify critical residues, and provide the structural basis for catalysis by this new family of enzymes.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH); National Institute of Allergy and Infectious Diseases (NIAID); USDOE Office of Science (SC)

Grant/Contract Number:: HHSN272200700058C; HHSN272201200026C; AC02-06CH11357

OSTI ID:: 1328045

Journal Information:: Journal of Biological Chemistry, Vol. 291, Issue 29; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 13 works

Citation information provided by
Web of Science

References (33)

A highly coordinated cell wall degradation machine governs spore morphogenesis in Bacillus subtilis Morlot, C.; Uehara, T.; Marquis, K. A. Genes & Development, Vol. 24, Issue 4 https://doi.org/10.1101/gad.1878110	journal	February 2010
Regulation of endospore formation in Bacillus subtilis Errington, Jeff Nature Reviews Microbiology, Vol. 1, Issue 2 https://doi.org/10.1038/nrmicro750	journal	November 2003
Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation Hilbert, D. W.; Piggot, P. J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 2 https://doi.org/10.1128/MMBR.68.2.234-262.2004	journal	June 2004
SpoIID-Mediated Peptidoglycan Degradation Is Required throughout Engulfment during Bacillus subtilis Sporulation Gutierrez, J.; Smith, R.; Pogliano, K. Journal of Bacteriology, Vol. 192, Issue 12 https://doi.org/10.1128/JB.00127-10	journal	April 2010
A cytoskeleton-like role for the bacterial cell wall during engulfment of the Bacillus subtilis forespore Abanes-De Mello, A. Genes & Development, Vol. 16, Issue 24 https://doi.org/10.1101/gad.1039902	journal	December 2002
Engulfment during sporulation in Bacillus subtilis is governed by a multi-protein complex containing tandemly acting autolysins: Multi-protein complex containing autolysins Chastanet, Arnaud; Losick, Richard Molecular Microbiology, Vol. 64, Issue 1 https://doi.org/10.1111/j.1365-2958.2007.05652.x	journal	March 2007
Lytic transglycosylases: Bacterial space-making autolysins Scheurwater, Edie; Reid, Chris W.; Clarke, Anthony J. The International Journal of Biochemistry & Cell Biology, Vol. 40, Issue 4 https://doi.org/10.1016/j.biocel.2007.03.018	journal	January 2008
Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography Thunnissen, Andy-Mark W. H.; Dijkstra, Arnoud J.; Kalk, Kor H. Nature, Vol. 367, Issue 6465 https://doi.org/10.1038/367750a0	journal	February 1994
The catalytic domain of a bacterial lytic transglycosylase defines a novel class of lysozymes Thunnissen, Andy-Mark W. H.; Isaacs, Neil W.; Dijkstral, Bauke W. Proteins: Structure, Function, and Genetics, Vol. 22, Issue 3 https://doi.org/10.1002/prot.340220305	journal	July 1995
Identification of Four Families of Peptidoglycan Lytic Transglycosylases Blackburn, Neil T.; Clarke, Anthony J. Journal of Molecular Evolution, Vol. 52, Issue 1 https://doi.org/10.1007/s002390010136	journal	January 2001
Structural Genomics and Drug Discovery for Infectious Diseases Anderson, W. Infectious Disorders - Drug Targets, Vol. 9, Issue 5 https://doi.org/10.2174/187152609789105713	journal	October 2009
The Polymerase Incomplete Primer Extension (PIPE) Method Applied to High-Throughput Cloning and Site-Directed Mutagenesis Klock, Heath E.; Lesley, Scott A. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-196-3_6	book	January 2009
Purification, crystallization and preliminary X-ray study of orotidine 5′-monophosphate decarboxylase Wu, Ning; Christendat, Dinesh; Dharamsi, Akil Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 7 https://doi.org/10.1107/S090744490000576X	journal	July 2000
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
PDBsum additions de Beer, Tjaart A. P.; Berka, Karel; Thornton, Janet M. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt940	journal	October 2013
ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids Ashkenazy, H.; Erez, E.; Martz, E. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq399	journal	May 2010
SiteComp: a server for ligand binding site analysis in protein structures Lin, Yingjie; Yoo, Seungyeul; Sanchez, Roberto Bioinformatics, Vol. 28, Issue 8 https://doi.org/10.1093/bioinformatics/bts095	journal	February 2012
Deciphering key features in protein structures with the new ENDscript server Robert, Xavier; Gouet, Patrice Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku316	journal	April 2014
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Isolation and separation of the glycan strands from murein of Escherichia coli by reversed-phase high-performance liquid chromatography Harz, Hartmann; Burgdorf, Knut; Höltje, Joachim-Volker Analytical Biochemistry, Vol. 190, Issue 1 https://doi.org/10.1016/0003-2697(90)90144-X	journal	October 1990
A dye release assay for determination of lysostaphin activity Zhou, Runqi; Chen, Shigen; Recsei, Paul Analytical Biochemistry, Vol. 171, Issue 1 https://doi.org/10.1016/0003-2697(88)90134-0	journal	May 1988
PROMALS3D: a tool for multiple protein sequence and structure alignments Pei, Jimin; Kim, Bong-Hyun; Grishin, Nick V. Nucleic Acids Research, Vol. 36, Issue 7 https://doi.org/10.1093/nar/gkn072	journal	February 2008
Three-dimensional structure of the bacterial cell wall peptidoglycan Meroueh, S. O.; Bencze, K. Z.; Hesek, D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 12 https://doi.org/10.1073/pnas.0510182103	journal	March 2006
The structure of α-chitin Minke, Ram; Blackwell, John Journal of Molecular Biology, Vol. 120, Issue 2 https://doi.org/10.1016/0022-2836(78)90063-3	journal	April 1978
The catalytic domain of the germination-specific lytic transglycosylase SleB from Bacillus anthracis displays a unique active site topology Jing, Xing; Robinson, Howard R.; Heffron, Jared D. Proteins: Structure, Function, and Bioinformatics, Vol. 80, Issue 10 https://doi.org/10.1002/prot.24140	journal	July 2012
Crystallographic determination of the mode of binding of oligosaccharides to T4 bacteriophage lysozyme: Implications for the mechanism of catalysis Anderson, W. F.; Grütter, M. G.; Remington, S. J. Journal of Molecular Biology, Vol. 147, Issue 4 https://doi.org/10.1016/0022-2836(81)90398-3	journal	April 1981
Relation between hen egg white lysozyme and bacteriophage T4 lysozyme: Evolutionary implications Matthews, B. W.; Remington, S. J.; Grütter, M. G. Journal of Molecular Biology, Vol. 147, Issue 4 https://doi.org/10.1016/0022-2836(81)90399-5	journal	April 1981
Structure of the 70-kDa Soluble Lytic Transglycosylase Complexed with Bulgecin A. Implications for the Enzymic Mechanism Thunnissen, Andy-Mark W. H.; Rozeboom, Henriette J.; Kalk, Kor H. Biochemistry, Vol. 34, Issue 39 https://doi.org/10.1021/bi00039a032	journal	October 1995
Crystal Structure of the Mutant D52S Hen Egg White Lysozyme with an Oligosaccharide Product Hadfield, A. T.; Harvey, D. J.; Archer, D. B. Journal of Molecular Biology, Vol. 243, Issue 5 https://doi.org/10.1006/jmbi.1994.1688	journal	November 1994
Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. Jacobs, C.; Huang, L. J.; Bartowsky, E. The EMBO Journal, Vol. 13, Issue 19 https://doi.org/10.1002/j.1460-2075.1994.tb06792.x	journal	October 1994

Cited By (6)

Acidogenesis, solventogenesis, metabolic stress response and life cycle changes in Clostridium beijerinckii NRRL B-598 at the transcriptomic level Patakova, Petra; Branska, Barbora; Sedlar, Karel Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37679-0	journal	February 2019
Lytic transglycosylases: concinnity in concision of the bacterial cell wall Dik, David A.; Marous, Daniel R.; Fisher, Jed F. Critical Reviews in Biochemistry and Molecular Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10409238.2017.1337705	journal	June 2017
Differential requirements for conserved peptidoglycan remodeling enzymes during Clostridioides difficile spore formation: Regulation of Clostridium difficile Engulfment Ribis, John W.; Fimlaid, Kelly A.; Shen, Aimee Molecular Microbiology, Vol. 110, Issue 3 https://doi.org/10.1111/mmi.14090	journal	October 2018
Peptidoglycan degradation machinery in Clostridium difficile forespore engulfment: Engulfment machinery in C. difficile Dembek, Marcin; Kelly, Abigail; Barwinska-Sendra, Anna Molecular Microbiology, Vol. 110, Issue 3 https://doi.org/10.1111/mmi.14091	journal	October 2018
The engulfasome in C. difficile: Variations on protein machineries Kelly, Abigail; Salgado, Paula S. Anaerobe, Vol. 60 https://doi.org/10.1016/j.anaerobe.2019.102091	journal	December 2019
A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum Jacquier, Nicolas; Yadav, Akhilesh K.; Pillonel, Trestan mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mbio.01128-19	journal	August 2019

Similar Records

Structure of the Bacteriophage [phi]KZ Lytic Transglycosylase gp144

Journal Article · Wed Apr 02 00:00:00 EDT 2008 · J. Biol. Chem. · OSTI ID:1328045

Fokine, Andrei; Miroshnikov, Konstantin A; Shneider, Mikhail M; +2 more

Structural studies and molecular dynamics simulations suggest a processive mechanism of exolytic lytic transglycosylase from Campylobacter jejuni

Journal Article · Mon May 14 00:00:00 EDT 2018 · PLoS ONE · OSTI ID:1328045

Vijayaraghavan, Jagamya; Kumar, Vijay; Krishnan, Nikhil P.; +5 more

The hydrolysis mechanism of a GH45 cellulase and its potential relation to lytic transglycosylase and expansin function

Journal Article · Wed Apr 01 00:00:00 EDT 2020 · Journal of Biological Chemistry · OSTI ID:1328045

Bharadwaj, Vivek S.; Knott, Brandon C.; Ståhlberg, Jerry; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
cell differentiation
cell surface enzyme
enzyme structure
peptidoglycan
sporulation
drug target
lytic transglycosylase
SpoIID

Title: Crystal Structures of the SpoIID Lytic Transglycosylases Essential for Bacterial Sporulation

Citation Formats

References (33)

Cited By (6)

Similar Records

Related Subjects