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

Vijayaraghavan, Jagamya; Kumar, Vijay; Krishnan, Nikhil P.; Kaufhold, Ross T.; Zeng, Ximin; Lin, Jun; van den Akker, Focco; Sticht, ed., Heinrich

doi:10.1371/journal.pone.0197136

Title: 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

DOI:https://doi.org/10.1371/journal.pone.0197136· OSTI ID:1437092

Vijayaraghavan, Jagamya; Kumar, Vijay; Krishnan, Nikhil P.; Kaufhold, Ross T.; Zeng, Ximin; Lin, Jun;

; Sticht, ed., Heinrich

The bacterial soluble lytic transglycosylase (LT) breaks down the peptidoglycan (PG) layer during processes such as cell division. We present here crystal structures of the soluble LT Cj0843 from Campylobacter jejuni with and without bulgecin A inhibitor in the active site. Cj0843 has a doughnut shape similar but not identical to that of E. coli SLT70. The C-terminal catalytic domain is preceded by an L-domain, a large helical U-domain, a flexible linker, and a small N-terminal NU-domain. The flexible linker allows the NU-domain to reach over and complete the circular shape, using residues conserved in the Epsilonproteobacteria LT family. The inner surface of the Cj0843 doughnut is mostly positively charged including a pocket that has 8 Arg/Lys residues. Molecular dynamics simulations with PG strands revealed a potential functional role for this pocket in anchoring the negatively charged terminal tetrapeptide of the PG during several steps in the reaction including homing and aligning the PG strand for exolytic cleavage, and subsequent ratcheting of the PG strand to enhance processivity in degrading PG strands.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS)

Grant/Contract Number:: AC02-76SF00515; P41GM103393

OSTI ID:: 1437092

Alternate ID(s):: OSTI ID: 1903987

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Vol. 13 Journal Issue: 5; ISSN 1932-6203

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 8 works

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References (59)

A single nucleotide in the promoter region modulates the expression of the -lactamase OXA-61 in Campylobacter jejuni Zeng, X.; Brown, S.; Gillespie, B. Journal of Antimicrobial Chemotherapy, Vol. 69, Issue 5 https://doi.org/10.1093/jac/dkt515	journal	January 2014
Mutation of a Single Lytic Transglycosylase Causes Aberrant Septation and Inhibits Cell Separation of Neisseria gonorrhoeae Cloud, K. A.; Dillard, J. P. Journal of Bacteriology, Vol. 186, Issue 22 https://doi.org/10.1128/JB.186.22.7811-7814.2004	journal	October 2004
Structural and biochemical characterization of the -N-acetylglucosaminidase from Thermotoga maritima: Toward rationalization of mechanistic knowledge in the GH73 family Lipski, A.; Herve, M.; Lombard, V. Glycobiology, Vol. 25, Issue 3 https://doi.org/10.1093/glycob/cwu113	journal	October 2014
Crystal Structure of the Heteromolecular Chaperone, AscE-AscG, from the Type III Secretion System in Aeromonas hydrophila Chatterjee, Chiradip; Kumar, Sundramurthy; Chakraborty, Smarajit PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0019208	journal	April 2011
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
From the regulation of peptidoglycan synthesis to bacterial growth and morphology Typas, Athanasios; Banzhaf, Manuel; Gross, Carol A. Nature Reviews Microbiology, Vol. 10, Issue 2 https://doi.org/10.1038/nrmicro2677	journal	December 2011
Characterization of Soluble and Membrane-Bound Family 3 Lytic Transglycosylases from Pseudomonas aeruginosa ^† Blackburn, Neil T.; Clarke, Anthony J. Biochemistry, Vol. 41, Issue 3 https://doi.org/10.1021/bi011833k	journal	January 2002
Tetratricopeptide Repeat Motifs in the World of Bacterial Pathogens: Role in Virulence Mechanisms Cerveny, Lukas; Straskova, Adela; Dankova, Vera Infection and Immunity, Vol. 81, Issue 3 https://doi.org/10.1128/IAI.01035-12	journal	December 2012
Novel type of murein transglycosylase in Escherichia coli. Höltje, J. V.; Mirelman, D.; Sharon, N. Journal of Bacteriology, Vol. 124, Issue 3 https://doi.org/10.1128/JB.124.3.1067-1076.1975	journal	January 1975
On the Mechanism of Peptidoglycan Binding and Cleavage by the endo -Specific Lytic Transglycosylase MltE from Escherichia coli Fibriansah, Guntur; Gliubich, Francesca I.; Thunnissen, Andy-Mark W. H. Biochemistry, Vol. 51, Issue 45 https://doi.org/10.1021/bi300900t	journal	October 2012
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
Crystallographic Studies of the Interactions of Escherichia coli Lytic Transglycosylase Slt35 with Peptidoglycan ^† ^, ^‡ van Asselt, Erik J.; Kalk, Kor H.; Dijkstra, Bauke W. Biochemistry, Vol. 39, Issue 8 https://doi.org/10.1021/bi992161p	journal	February 2000
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
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
Inhibition of membrane-bound lytic transglycosylase B by NAG-thiazoline Reid, C. W.; Blackburn, N. T.; Legaree, B. A. FEBS Letters, Vol. 574, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.08.006	journal	August 2004
Growth of the Stress-Bearing and Shape-Maintaining Murein Sacculus of Escherichia coli Höltje, Joachim-Volker Microbiology and Molecular Biology Reviews, Vol. 62, Issue 1 https://doi.org/10.1128/MMBR.62.1.181-203.1998	journal	January 1998
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
A Survey of Aspartate−Phenylalanine and Glutamate−Phenylalanine Interactions in the Protein Data Bank: Searching for Anion−π Pairs Philip, Vivek; Harris, Jason; Adams, Rachel Biochemistry, Vol. 50, Issue 14 https://doi.org/10.1021/bi200066k	journal	April 2011
A putative lytic transglycosylase tightly regulated and critical for the EHEC type three secretion Yu, Yen-Chi; Lin, Ching-Nan; Wang, Shao-Hung Journal of Biomedical Science, Vol. 17, Issue 1 https://doi.org/10.1186/1423-0127-17-52	journal	January 2010
An analysis of protein domain linkers: their classification and role in protein folding George, Richard A.; Heringa, Jaap Protein Engineering, Design and Selection, Vol. 15, Issue 11 https://doi.org/10.1093/protein/15.11.871	journal	November 2002
Structural Analysis of a Specialized Type III Secretion System Peptidoglycan-cleaving Enzyme Burkinshaw, Brianne J.; Deng, Wanyin; Lameignère, Emilie Journal of Biological Chemistry, Vol. 290, Issue 16 https://doi.org/10.1074/jbc.M115.639013	journal	February 2015
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
Turnover of Bacterial Cell Wall by SltB3, a Multidomain Lytic Transglycosylase of Pseudomonas aeruginosa Lee, Mijoon; Domínguez-Gil, Teresa; Hesek, Dusan ACS Chemical Biology, Vol. 11, Issue 10 https://doi.org/10.1021/acschembio.6b00756	journal	August 2016
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909012098	journal	May 2009
Searching protein structure databases with DaliLite v.3 Holm, L.; Kaariainen, S.; Rosenstrom, P. Bioinformatics, Vol. 24, Issue 23 https://doi.org/10.1093/bioinformatics/btn507	journal	September 2008
N-Glycosylation of Campylobacter jejuni Surface Proteins Promotes Bacterial Fitness Alemka, Abofu; Nothaft, Harald; Zheng, Jing Infection and Immunity, Vol. 81, Issue 5 https://doi.org/10.1128/IAI.01370-12	journal	March 2013
The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in P seudomonas aeruginosa : RlpA is a peptidoglycan hydrolase Jorgenson, Matthew A.; Chen, Yan; Yahashiri, Atsushi Molecular Microbiology, Vol. 93, Issue 1 https://doi.org/10.1111/mmi.12643	journal	May 2014
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Characterization of Helicobacter pylori Lytic Transglycosylases Slt and MltD Chaput, C.; Labigne, A.; Boneca, I. G. Journal of Bacteriology, Vol. 189, Issue 2 https://doi.org/10.1128/JB.01270-06	journal	November 2006
Characterization of three different lytic transglycosylases in Escherichia coli Romeis, Tina; Vollmer, Waldemar; HÃ¶ltje, Joachim-Volker FEMS Microbiology Letters, Vol. 111, Issue 2-3 https://doi.org/10.1111/j.1574-6968.1993.tb06376.x	journal	August 1993
Reactions of All Escherichia coli Lytic Transglycosylases with Bacterial Cell Wall Lee, Mijoon; Hesek, Dusan; Llarrull, Leticia I. Journal of the American Chemical Society, Vol. 135, Issue 9 https://doi.org/10.1021/ja309036q	journal	February 2013
Susceptibility to Antibiotics and -Lactamase Induction in Murein Hydrolase Mutants of Escherichia coli Korsak, D.; Liebscher, S.; Vollmer, W. Antimicrobial Agents and Chemotherapy, Vol. 49, Issue 4 https://doi.org/10.1128/AAC.49.4.1404-1409.2005	journal	March 2005
IpaB-IpgC interaction defines binding motif for type III secretion translocator Lunelli, M.; Lokareddy, R. K.; Zychlinsky, A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 24 https://doi.org/10.1073/pnas.0812900106	journal	May 2009
Loop-length-dependent SVM prediction of domain linkers for high-throughput structural proteomics Ebina, Teppei; Toh, Hiroyuki; Kuroda, Yutaka Biopolymers, Vol. 92, Issue 1 https://doi.org/10.1002/bip.21105	journal	January 2009
Structural basis for autoinhibition and activation of Auto, a virulence-associated peptidoglycan hydrolase of Listeria monocytogenes Bublitz, Maike; Polle, Lilia; Holland, Christin Molecular Microbiology, Vol. 71, Issue 6 https://doi.org/10.1111/j.1365-2958.2009.06619.x	journal	March 2009
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
Versatile TPR domains accommodate different modes of target protein recognition and function Allan, Rudi Kenneth; Ratajczak, Thomas Cell Stress and Chaperones, Vol. 16, Issue 4 https://doi.org/10.1007/s12192-010-0248-0	journal	December 2010
The Essential Protein for Bacterial Flagella Formation FlgJ Functions as a β- N -Acetylglucosaminidase Herlihey, Francesca A.; Moynihan, Patrick J.; Clarke, Anthony J. Journal of Biological Chemistry, Vol. 289, Issue 45 https://doi.org/10.1074/jbc.M114.603944	journal	September 2014
Outer membrane localization of murein hydrolases: MltA, a third lipoprotein lytic transglycosylase in Escherichia coli. Lommatzsch, J.; Templin, M. F.; Kraft, A. R. Journal of Bacteriology, Vol. 179, Issue 17 https://doi.org/10.1128/jb.179.17.5465-5470.1997	journal	September 1997
Identifying and Characterizing Binding Sites and Assessing Druggability Halgren, Thomas A. Journal of Chemical Information and Modeling, Vol. 49, Issue 2 https://doi.org/10.1021/ci800324m	journal	January 2009
Helicobacter pylori Infection and Gastric Lymphoma Parsonnet, Julie; Hansen, Svein; Rodriguez, Larissa New England Journal of Medicine, Vol. 330, Issue 18 https://doi.org/10.1056/NEJM199405053301803	journal	May 1994
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
Biosynthesis of the N-Linked Glycan in Campylobacter jejuni and Addition onto Protein through Block Transfer Kelly, J.; Jarrell, H.; Millar, L. Journal of Bacteriology, Vol. 188, Issue 7 https://doi.org/10.1128/JB.188.7.2427-2434.2006	journal	March 2006
Peptidoglycan ld-Carboxypeptidase Pgp2 Influences Campylobacter jejuni Helical Cell Shape and Pathogenic Properties and Provides the Substrate for the dl-Carboxypeptidase Pgp1 Frirdich, Emilisa; Vermeulen, Jenny; Biboy, Jacob Journal of Biological Chemistry, Vol. 289, Issue 12 https://doi.org/10.1074/jbc.M113.491829	journal	January 2014
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
Enhanced Transmission of Antibiotic Resistance in Campylobacter jejuni Biofilms by Natural Transformation Bae, Junghee; Oh, Euna; Jeon, Byeonghwa Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 12 https://doi.org/10.1128/AAC.04066-14	journal	September 2014
Beta-Lactam Antibiotics Induce a Lethal Malfunctioning of the Bacterial Cell Wall Synthesis Machinery Cho, Hongbaek; Uehara, Tsuyoshi; Bernhardt, Thomas G. Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.11.017	journal	December 2014
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
Escherichia coli Peptidoglycan Structure and Mechanics as Predicted by Atomic-Scale Simulations Gumbart, James C.; Beeby, Morgan; Jensen, Grant J. PLoS Computational Biology, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pcbi.1003475	journal	February 2014
The Effect of Bulgecin A on Peptidoglycan Metabolism and Physiology of Helicobacter pylori Bonis, Mathilde; Williams, Allison; Guadagnini, Stephanie Microbial Drug Resistance, Vol. 18, Issue 3 https://doi.org/10.1089/mdr.2011.0231	journal	June 2012
Important Role of a Putative Lytic Transglycosylase Cj0843c in β-Lactam Resistance in Campylobacter jejuni Zeng, Ximin; Gillespie, Barbara; Lin, Jun Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01292	journal	November 2015
A structural basis for processivity Breyer, Wendy A.; Matthews, Brian W. Protein Science, Vol. 10, Issue 9 https://doi.org/10.1110/ps.10301	journal	September 2001
ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules Ashkenazy, Haim; Abadi, Shiran; Martz, Eric Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw408	journal	May 2016
Novel morphological changes in gram-negative bacteria caused by combination of bulgecin and cefmenoxime. Nakao, M.; Yukishige, K.; Kondo, M. Antimicrobial Agents and Chemotherapy, Vol. 30, Issue 3 https://doi.org/10.1128/AAC.30.3.414	journal	September 1986
High resolution crystal structures of the Escherichia coli lytic transglycosylase slt70 and its complex with a peptidoglycan fragment van Asselt, Erik J.; Thunnissen, Andy-Mark W. H.; Dijkstra, Bauke W. Journal of Molecular Biology, Vol. 291, Issue 4 https://doi.org/10.1006/jmbi.1999.3013	journal	August 1999
A lytic transglycosylase homologue, PleA, is required for the assembly of pili and the flagellum at the Caulobacter crescentus cell pole: Pleiotropic role of PleA in pili and flagellar biogenesis Viollier, Patrick H.; Shapiro, Lucy Molecular Microbiology, Vol. 49, Issue 2 https://doi.org/10.1046/j.1365-2958.2003.03576.x	journal	June 2003
Protein-protein interactions: General trends in the relationship between binding affinity and interfacial buried surface area: Protein-protein Interactions Chen, Jieming; Sawyer, Nicholas; Regan, Lynne Protein Science, Vol. 22, Issue 4 https://doi.org/10.1002/pro.2230	journal	February 2013
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Helicobacter pylori Infection and the Development of Gastric Cancer Uemura, Naomi; Okamoto, Shiro; Yamamoto, Soichiro New England Journal of Medicine, Vol. 345, Issue 11 https://doi.org/10.1056/NEJMoa001999	journal	September 2001

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

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