Function and localization dynamics of bifunctional penicillin-binding proteins in Caulobacter crescentus

Journal of Bacteriology

Volumn 196, Issue 8, 2014, Pages 1627-1639

  Strobel, Wolfgang ^a,b   M̈ll, Andrea ^a,b,c   Kiekebusch, Daniela ^a,b   Klein, Kathrin E ^a,b   Thanbichler, Martin ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIFUNCTIONAL PENICILLIN BINDING PROTEIN; DEXTRO ALANINE; FTSN PROTEIN; PBP1A PROTEIN; PBPC PROTEIN; PBPX PROTEIN; PBPY PROTEIN; PBPZ PROTEIN; PENICILLIN BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL ELONGATION; CELL FUSION; CELL SHAPE; CELL STRUCTURE; CELL VIABILITY; CYTOKINESIS; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; NONHUMAN; PARALOGY; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; CAULOBACTER CRESCENTUS; CELL WALL; GENE KNOCKOUT TECHNIQUES; MICROBIAL VIABILITY; MICROSCOPY; MOLECULAR SEQUENCE DATA; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN INTERACTION MAPPING;

EID: 84896482697     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01194-13     Document Type: Article

References (62)

1. Typas A, Banzhaf M, Gross CA, Vollmer W. 2012. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10:123-136. http://dx.doi.org/10.1038/nrmicro2677.
2. Lovering AL, de Castro LH, Lim D, Strynadka NC. 2007. Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis. Science 315:1402-1405. http://dx.doi.org/10.1126/science.1136611.
3. Schwartz B, Markwalder JA, Seitz SP, Wang Y, Stein RL. 2002. A kinetic characterization of the glycosyltransferase activity of Escherichia coli PBP1b and development of a continuous fluorescence assay. Biochemistry 41:12552-12561. http://dx.doi.org/10.1021/bi026205x.
4. Sauvage E, KerffF, Terrak M, Ayala JA, Charlier P. 2008. The penicillinbinding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:234-258. http://dx.doi.org/10.1111/j.1574-6976.2008.00105.x.
5. Ropp PA, Nicholas RA. 1997. Cloning and characterization of the ponA gene encoding penicillin-binding protein 1 from Neisseria gonorrhoeae and Neisseria meningitidis. J. Bacteriol. 179:2783-2787.
6. Banzhaf M, van den Berg van Saparoea B, Terrak M, Fraipont C, Egan A, Philippe J, Zapun A, Breukink E, Nguyen-Disteche M, den Blaauwen T, Vollmer W. 2012. Cooperativity of peptidoglycan synthases active in bacterial cell elongation. Mol. Microbiol. 85:179-194. http://dx.doi.org/10.1111/j.1365-2958.2012.08103.x
7. den Blaauwen T, de Pedro MA, Nguyen-Disteche M, Ayala JA. 2008. Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev. 32:321-344. http://dx.doi.org/10.1111/j.1574-6976.2007.00090.x.
8. Bertsche U, Kast T, Wolf B, Fraipont C, Aarsman ME, Kannenberg K, von Rechenberg M, Nguyen-Disteche M, den Blaauwen T, Höltje JV, Vollmer W. 2006. Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol. Microbiol. 61:675-690. http://dx.doi.org/10.1111/j.1365-2958.2006.05280.x.
9. Müller P, Ewers C, Bertsche U, Anstett M, Kallis T, Breukink E, Fraipont C, Terrak M, Nguyen-Disteche M, Vollmer W. 2007. The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J. Biol. Chem. 282:36394-36402. http://dx.doi.org/10.1074/jbc. M706390200.
10. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S, Kahne DE, Bernhardt TG. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110-1120. http://dx.doi.org/10.1016/j.cell.2010.11.037.
11. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, Nichols RJ, Zietek M, Beilharz K, Kannenberg K, von Rechenberg M, Breukink E, den Blaauwen T, Gross CA, Vollmer W. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097-1109. http://dx.doi.org/10.1016/j.cell.2010.11.038.
12. Yousif SY, Broome-Smith JK, Spratt BG. 1985. Lysis of Escherichia coli by beta-lactam antibiotics: deletion analysis of the role of penicillin-binding proteins 1A and 1B. J. Gen. Microbiol. 131:2839-2845.
13. Schiffer G, Höltje JV. 1999. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274:32031-32039. http://dx.doi.org/10.1074/jbc.274.45.32031.
14. Goffin C, Ghuysen JM. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
15. Lazaro S, Fernandez-Pinas F, Fernandez-Valiente E, Blanco-Rivero A, Leganes F. 2001. pbpB, a gene coding for a putative penicillin-binding protein, is required for aerobic nitrogen fixation in the cyanobacterium Anabaena sp. strain PCC7120. J. Bacteriol. 183:628-636. http://dx.doi.org/10.1128/JB.183.2.628-636.2001.
16. Budd A, Blandin S, Levashina EA, Gibson TJ. 2004. Bacterial alpha2-macroglobulins: colonization factors acquired by horizontal gene transfer from the metazoan genome? Genome Biol. 5:R38. http://dx.doi.org/10.1186/gb-2004-5-6-r38.
17. Aaron M, Charbon G, Lam H, Schwarz H, Vollmer W, Jacobs-Wagner C. 2007. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol. 64: 938-952. http://dx.doi.org/10.1111/j.1365-2958.2007.05720.x.
18. Hocking J, Priyadarshini R, Takacs CN, Costa T, Dye NA, Shapiro L, Vollmer W, Jacobs-Wagner C. 2012. Osmolality-dependent relocation of penicillin-binding protein PBP2 to the division site in Caulobacter crescentus. J. Bacteriol. 194:3116-3127. http://dx.doi.org/10.1128/JB.00260-12.
19. Kühn J, Briegel A, Mörschel E, Kahnt J, Leser K, Wick S, Jensen GJ, Thanbichler M. 2010. Bactofilins, a ubiquitous class of cytoskeletal proteins mediating polar localization of a cell wall synthase in Caulobacter crescentus. EMBO J. 29:327-339. http://dx.doi.org/10.1038/emboj.2009.358.
20. Yakhnina AA, Gitai Z. 2013. Diverse functions for six glycosyltransferases in Caulobacter crescentus cell wall assembly. J. Bacteriol. 195:4527-4535. http://dx.doi.org/10.1128/JB.00600-13.
21. Poindexter JS. 1964. Biological properties and classification of the Caulobacter group. Bacteriol. Rev. 28:231-295.
22. Ely B. 1991. Genetics of Caulobacter crescentus. Methods Enzymol. 204: 372-384. http://dx.doi.org/10.1016/0076-6879(91)04019-K.
23. Meisenzahl AC, Shapiro L, Jenal U. 1997. Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus. J. Bacteriol. 179:592-600.
24. Boutte CC, Srinivasan BS, Flannick JA, Novak AF, Martens AT, Batzoglou S, Viollier PH, Crosson S. 2008. Genetic and computational identification of a conserved bacterial metabolic module. PLoS Genet. 4:e1000310. http://dx.doi.org/10.1371/journal.pgen.1000310.
25. Thanbichler M, Iniesta AA, Shapiro L. 2007. A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res. 35:e137. http://dx.doi.org/10.1093/nar/gkm818.
26. Tsai JW, Alley MR. 2001. Proteolysis of the Caulobacter McpA chemoreceptor is cell cycle regulated by a ClpX-dependent pathway. J. Bacteriol. 183:5001-5007. http://dx.doi.org/10.1128/JB.183.17.5001-5007.2001.
27. Botstein K, Lew KK, Jarvik V, Swanson CA. 1975. Role of antirepressor in the bipartite control of repression and immunity by bacteriophage P22. J. Mol. Biol. 91:439-462. http://dx.doi.org/10.1016/0022-2836(75)90271-5.
28. Thanbichler M, Shapiro L. 2006. MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126:147-162. http://dx.doi.org/10.1016/j.cell.2006.05.038.
29. Domian IJ, Quon KC, Shapiro L. 1997. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90:415-424. http://dx.doi.org/10.1016/S0092-8674(00)80502-4.
30. Robichon C, Karimova G, Beckwith J, Ladant D. 2011. Role of leucine zipper motifs in association of the Escherichia coli cell division proteins FtsL and FtsB. J. Bacteriol. 193:4988-4992. http://dx.doi.org/10.1128/JB.00324-11.
31. Karimova G, Pidoux J, Ullmann A, Ladant D. 1998. A bacterial twohybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756. http://dx.doi.org/10.1073/pnas.95.10.5752.
32. de Jonge BL, Chang YS, Gage D, Tomasz A. 1992. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J. Biol. Chem. 267:11248-11254.
33. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95:5857-5864. http://dx.doi.org/10.1073/pnas.95.11.5857.
34. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301. http://dx.doi.org/10.1093/nar/gkr1065.
35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
36. Vollmer W, Bertsche U. 2008. Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim. Biophys. Acta 1778: 1714-1734. http://dx.doi.org/10.1016/j.bbamem.2007.06.007.
37. McGrath PT, Lee H, Zhang L, Iniesta AA, Hottes AK, Tan MH, Hillson NJ, Hu P, Shapiro L, McAdams HH. 2007. High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat. Biotechnol. 25:584-592. http://dx.doi.org/10.1038/nbt1294.
38. Markiewicz Z, Glauner B, Schwarz U. 1983. Murein structure and lack of DD- and LD-carboxypeptidase activities in Caulobacter crescentus. J. Bacteriol. 156:649-655.
39. Takacs CN, Hocking J, Cabeen MT, Bui NK, Poggio S, Vollmer W, Jacobs-Wagner C. 2013. Growth medium-dependent glycine incorporation into the peptidoglycan of Caulobacter crescentus. PLoS One 8:e57579. http://dx.doi.org/10.1371/journal.pone.0057579.
40. Lam H, Oh DC, Cava F, Takacs CN, Clardy J, de Pedro MA, Waldor MK. 2009. D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552-1555. http://dx.doi.org/10.1126/science.1178123.
41. Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK. 2011. Distinct pathways for modification of the bacterial cell wall by non-canonical Damino acids. EMBO J. 30:3442-3453. http://dx.doi.org/10.1038/emboj.2011.246.
42. Cava F, Lam H, de Pedro MA, Waldor MK. 2011. Emerging knowledge of regulatory roles of D-amino acids in bacteria. Cell. Mol. Life Sci. 68: 817-831. http://dx.doi.org/10.1007/s00018-010-0571-8.
43. Egan AJ, Vollmer W. 2013. The physiology of bacterial cell division. Ann. N. Y. Acad. Sci. 1277:8-28. http://dx.doi.org/10.1111/j.1749-6632.2012.06818.x.
44. Lutkenhaus J, PichoffS, Du S. 2012. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton (Hoboken) 69:778-790. http://dx.doi.org/10.1002/cm.21054.
45. Goley ED, Yeh YC, Hong SH, Fero MJ, Abeliuk E, McAdams HH, Shapiro L. 2011. Assembly of the Caulobacter cell division machine. Mol. Microbiol. 80:1680-1698. http://dx.doi.org/10.1111/j.1365-2958.2011.07677.x.
46. Wang Y, Jones BD, Brun YV. 2001. A set of ftsZ mutants blocked at different stages of cell division in Caulobacter. Mol. Microbiol. 40:347-360. http://dx.doi.org/10.1046/j.1365-2958.2001.02395.x.
47. Möll A, Schlimpert S, Briegel A, Jensen GJ, Thanbichler M. 2010. DipM, a new factor required for peptidoglycan remodelling during cell division in Caulobacter crescentus. Mol. Microbiol. 77:90-107. http://dx.doi.org/10.1111/j.1365-2958.2010.07224.x.
48. Möll A, Thanbichler M. 2009. FtsN-like proteins are conserved compo-nents of the cell division machinery in proteobacteria. Mol. Microbiol. 72:1037-1053. http://dx.doi.org/10.1111/j.1365-2958.2009.06706.x.
49. Goley ED, Comolli LR, Fero KE, Downing KH, Shapiro L. 2010. DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter. Mol. Microbiol. 77:56-73. http://dx.doi.org/10.1111/j.1365-2958.2010.07222.x.
50. Poggio S, Takacs CN, Vollmer W, Jacobs-Wagner C. 2010. A protein critical for cell constriction in the Gram-negative bacterium Caulobacter crescentus localizes at the division site through its peptidoglycan-binding LysM domains. Mol. Microbiol. 77:74-89. http://dx.doi.org/10.1111/j.1365-2958.2010.07223.x.
51. Fenton AK, Gerdes K. 2013. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBOJ. 32:1953-1965. http://dx.doi.org/10.1038/emboj.2013.129.
52. Figge RM, Divakaruni AV, Gober JW. 2004. MreB, the cell shapedetermining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51:1321-1332. http://dx.doi.org/10.1111/j.1365-2958.2003.03936.x.
53. Gitai Z, Dye N, Shapiro L. 2004. An actin-like gene can determine cell polarity in bacteria. Proc. Natl. Acad. Sci. U. S. A. 101:8643-8648. http://dx.doi.org/10.1073/pnas.0402638101.
54. Karimova G, Dautin N, Landant D. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233-2243. http://dx.doi.org/10.1128/JB.187.7.2233-2243.2005.
55. Charpentier X, Chalut C, Remy MH, Masson JM. 2002. Penicillinbinding proteins 1a and 1b form independent dimers in Escherichia coli. J. Bacteriol. 184:3749-3752. http://dx.doi.org/10.1128/JB.184.13.3749-37 52.2002.
56. Zapun A, Contreras-Martel C, Vernet T. 2008. Penicillin-binding proteins and beta-lactam resistance. FEMS Microbiol. Rev. 32:361-385. http://dx.doi.org/10.1111/j.1574-6976.2007.00095.x.
57. Simm AM, Higgins CS, Pullan ST, Avison MB, Niumsup P, Erdozain O, Bennett PM, Walsh TR. 2001. A novel metallo-beta-lactamase, Mbl1b, produced by the environmental bacterium Caulobacter crescentus. FEBS Lett. 509:350-354. http://dx.doi.org/10.1016/S0014-5793(01)03152-0.
58. West L, Yang D, Stephens C. 2002. Use of the Caulobacter crescentus genome sequence to develop a method for systematic genetic mapping. J. Bacteriol. 184:2155-2166. http://dx.doi.org/10.1128/JB.184.8.2155-2166.2002.
59. Pepper ED, Farrell MJ, Finkel SE. 2006. Role of penicillin-binding protein 1b in competitive stationary-phase survival of Escherichia coli. FEMS Microbiol. Lett. 263:61-67. http://dx.doi.org/10.1111/j.1574-6968.2006.00418.x.
60. Hughes HV, Lisher JP, Hardy GG, Kysela DT, Arnold RJ, Giedroc DP, Brun YV. 2013. Coordinate synthesis and protein localization in a bacterial organelle by the action of a penicillin-binding-protein. Mol. Microbiol. 90:1162-1170. http://dx.doi.org/10.1111/mmi.12422.
61. Gerding MA, Liu B, Bendezu FO, Hale CA, Bernhardt TG, de Boer PA. 2009. Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J. Bacteriol. 191:7383-7401. http://dx.doi.org/10.1128/JB.00811-09.
62. Vollmer W, von Rechenberg M, Höltje JV. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274:6726-6734. http://dx.doi.org/10.1074/jbc.274.10.6726.