Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ

Nature Communications

Volumn 4, Issue , 2013, Pages

  Pilhofer, Martin ^a,b   Aistleitner, Karin ^c   Biboy, Jacob ^d   Gray, Joe ^d   Kuru, Erkin ^e   Hall, Edward ^e   Brun, Yves V ^e   VanNieuwenhze, Michael S ^e   Vollmer, Waldemar ^d   Horn, Matthias ^c   Jensen, Grant J ^a,b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRO ALANINE; FLUORESCENT DYE; FOSFOMYCIN; FTSZ PROTEIN; PENICILLIN DERIVATIVE; PEPTIDOGLYCAN;

BACTERIUM; BIOCHEMISTRY; HYPOTHESIS TESTING; INHIBITOR; POLYMER;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL MEMBRANE; CELL DIVISION; CELL SHAPE; CELL STRUCTURE; CELL WALL; CHEMICAL ANALYSIS; CHLAMYDIA; CONTROLLED STUDY; FLUORESCENCE IMAGING; IN VIVO STUDY; INFECTION RATE; LIFE CYCLE; MASS SPECTROMETRY; PROTEIN SYNTHESIS; SACCULI;

BACTERIA (MICROORGANISMS); CHLAMYDIAE;

BACTERIAL PROTEINS; CELL WALL; CHLAMYDIALES; CYTOSKELETAL PROTEINS; PEPTIDOGLYCAN;

EID: 84890205605     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3856     Document Type: Article

References (56)

1. Wagner, M. & Horn, M. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17, 241-249 (2006). (Pubitemid 43850263)
2. Devos, D. P. & Reynaud, E. G. Evolution. Intermediate steps. Science 330, 1187-1188 (2010).
3. Reynaud, E. G. & Devos, D. P. Transitional forms between the three domains of life and evolutionary implications. Proc. Biol. Sci. 278, 3321-3328 (2011).
4. Erickson, H. P., Anderson, D. E. & Osawa, M. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74, 504-528 (2010).
5. Pilhofer, M. et al. Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J. Bacteriol. 190, 3192-3202 (2008). (Pubitemid 351581415)
6. Lluch-Senar, M., Querol, E. & Pinol, J. Cell division in a minimal bacterium in the absence of ftsZ. Mol. Microbiol. 78, 278-289 (2010).
7. Leaver, M., Dominguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. Life without a wall or division machine in Bacillus subtilis. Nature 457, 849-853 (2009).
8. Manire, G. P. & Tamura, A. Preparation and chemical composition of the cell walls of mature infectious dense forms of meningopneumonitis organisms. J. Bacteriol. 94, 1178-1183 (1967).
9. Tamura, A. & Manire, G. P. Preparation and chemical composition of the cell membranes of developmental reticulate forms of meningopneumonitis organisms. J. Bacteriol. 94, 1184-1188 (1967).
10. Caldwell, H. D., Kromhout, J. & Schachter, J. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31, 1161-1176 (1981). (Pubitemid 11155484)
11. Fox, A. et al. Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry. Infect. Immun. 58, 835-837 (1990). (Pubitemid 20072654)
12. Barbour, A. G., Amano, K., Hackstadt, T., Perry, L. & Caldwell, H. D. Chlamydia trachomatis has penicillin-binding proteins but not detectable muramic acid. J. Bacteriol. 151, 420-428 (1982). (Pubitemid 12013576)
13. McCoy, A. J. & Maurelli, A. T. Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends. Microbiol. 14, 70-77 (2006). (Pubitemid 43190736)
14. Perkins, H. R. & Allison, A. C. Cell-wall constituents of Rickettsiae and Psittacosis-Lymphogranuloma organisms. J. Gen. Microbiol. 30, 469-480 (1963).
15. Garrett, A. J., Harrison, M. J. & Manire, G. P. A search for the bacterial mucopeptide component, muramic acid, in Chlamydia. J. Gen. Microbiol. 80, 315-318 (1974).
16. Moulder, J. W. Why is Chlamydia sensitive to penicillin in the absence of peptidoglycan? Infect. Agents. Dis. 2, 87-99 (1993). (Pubitemid 23252453)
17. Matsumoto, A. Recent progress of electron microscopy in microbiology and its development in future: from a study of the obligate intracellular parasites, chlamydia organisms. J. Electron. Microsc. 28, 57-64 (1979).
18. Tamura, A., Matsumoto, A., Manire, G. P. & Higashi, N. Electron microscopic observations on the structure of the envelopes of mature elementary bodies and developmental reticulate forms of Chlamydia psittaci. J. Bacteriol. 105, 355-360 (1971).
19. Huang, Z. et al. Cryo-electron tomography of Chlamydia trachomatis gives a clue to the mechanism of outer membrane changes. J. Electron. Microsc. 59, 237-241 (2010).
20. McCoy, A. J. & Maurelli, A. T. Characterization of Chlamydia MurC-Ddl, a fusion protein exhibiting D-alanyl-D-alanine ligase activity involved in peptidoglycan synthesis and D-cycloserine sensitivity. Mol. Microbiol. 57, 41-52 (2005). (Pubitemid 40896596)
21. McCoy, A. J., Sandlin, R. C. & Maurelli, A. T. In vitro and in vivo functional activity of Chlamydia MurA, a UDP-N-acetylglucosamine enolpyruvyl transferase involved in peptidoglycan synthesis and fosfomycin resistance. J. Bacteriol. 185, 1218-1228 (2003). (Pubitemid 36176853)
22. Hesse, L. et al. Functional and biochemical analysis of Chlamydia trachomatis MurC, an enzyme displaying UDP-N-acetylmuramate:amino acid ligase activity. J. Bacteriol. 185, 6507-6512 (2003). (Pubitemid 37385868)
23. Patin, D., Bostock, J., Blanot, D., Mengin-Lecreulx, D. & Chopra, I. Functional and biochemical analysis of the Chlamydia trachomatis ligase MurE. J. Bacteriol. 191, 7430-7435 (2009).
24. Patin, D., Bostock, J., Chopra, I., Mengin-Lecreulx, D. & Blanot, D. Biochemical characterisation of the chlamydial MurF ligase, and possible sequence of the chlamydial peptidoglycan pentapeptide stem. Arch. Microbiol. 194, 505-512 (2012).
25. Henrichfreise, B. et al. Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria Chlamydia and Wolbachia: why is lipid II needed? Mol. Microbiol. 73, 913-923 (2009).
26. Horn, M. Chlamydiae as symbionts in eukaryotes. Annu. Rev. Microbiol. 62, 113-131 (2008).
27. Leforestier, A., Lemercier, N. & Livolant, F. Contribution of cryoelectron microscopy of vitreous sections to the understanding of biological membrane structure. Proc. Natl Acad. Sci. USA 109, 8959-8964 (2012).
28. Tocheva, E. I., Li, Z. & Jensen, G. J. Electron cryotomography. Cold Spring Harb. Perspect. Biol. 2, a003442 (2010).
29. Liu, J. et al. Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J. Mol. Biol. 403, 546-561 (2010).
30. Tocheva, E. I. et al. Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation. Cell 146, 799-812 (2011).
31. Hatch, T. Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae? J. Bacteriol. 178, 1-5 (1996). (Pubitemid 26006058)
32. Glauner, B. Separation and quantification of muropeptides with highperformance liquid chromatography. Anal. Biochem. 172, 451-464 (1988).
33. de Jonge, B. L. & Tomasz, A. Abnormal peptidoglycan produced in a methicillin-resistant strain of Staphylococcus aureus grown in the presence of methicillin: functional role for penicillin-binding protein 2A in cell wall synthesis. Antimicrob. Agents. Chemother. 37, 342-346 (1993). (Pubitemid 23046581)
34. Bui, N. K. et al. The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J. Bacteriol. 191, 494-505 (2009).
35. Kuru, E. et al. In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew. Chem. 51, 12519-12523 (2012).
36. Matsumoto, A. & Manire, G. P. Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J. Bacteriol. 101, 278-285 (1970).
37. Skilton, R. J. et al. Penicillin induced persistence in Chlamydia trachomatis: high quality time lapse video analysis of the developmental cycle. PLoS One 4, e7723 (2009).
38. Beatty, W. L., Morrison, R. P. & Byrne, G. I. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 58, 686-699 (1994).
39. Maurin, M., Bryskier, A. & Raoult, D. Antibiotic susceptibilities of Parachlamydia acanthamoeba in amoebae. Antimicrob. Agents Chemother. 46, 3065-3067 (2002).
40. Kahane, S., Gonen, R., Sayada, C., Elion, J. & Friedman, M. G. Description and partial characterization of a new chlamydia-like microorganism. FEMS. Microbiol. Lett. 109, 329-334 (1993). (Pubitemid 23161265)
41. Brown, W. J. & Rockey, D. D. Identification of an antigen localized to an apparent septum within dividing chlamydiae. Infect. Immun. 68, 708-715 (2000). (Pubitemid 30056527)
42. Horn, M. et al. Illuminating the evolutionary history of chlamydiae. Science 304, 728-730 (2004). (Pubitemid 38560877)
43. Collingro, A. et al. Unity in variety-the Pan-genome of the Chlamydiae. Mol. Biol. Evol. 28, 3253-3270 (2011).
44. McPherson, D. C. & Popham, D. L. Peptidoglycan synthesis in the absence of Class A penicillin-binding proteins in Bacillus subtilis. J. Bacteriol. 185, 1423-1431 (2003). (Pubitemid 36176876)
45. Arbeloa, A. et al. Role of class A penicillin-binding proteins in PBP5-mediated b-lactam resistance in Enterococcus faecalis. J. Bacteriol. 186, 1221-1228 (2004). (Pubitemid 38248710)
46. Hedlund, B. P., Gosink, J. J. & Staley, J. T. Phylogeny of Prosthecobacter, the fusiform caulobacters: members of a recently discovered division of the Bacteria. Int. J. Syst. Bacteriol. 46, 960-966 (1996). (Pubitemid 26339221)
47. Schmitz-Esser, S. et al. Diversity of bacterial endosymbionts of environmental Acanthamoeba isolates. Appl. Environ. Microbiol. 74, 5822-5831 (2008).
48. Amann, R. I. et al. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919-1925 (1990). (Pubitemid 20202165)
49. Page, F. C. An Illustrated Key to Freshwater and Soil Amoebae (Freshwater Biological Association, 1976).
50. Tivol, W. F., Briegel, A. & Jensen, G. J. An improved cryogen for plunge freezing. Microsc. Microanal. 14, 375-379 (2008).
51. Iancu, C. V. et al. Electron cryotomography sample preparation using the Vitrobot. Nat. Protocols 1, 2813-2819 (2006).
52. Zheng, S. Q. et al. UCSF tomography: an integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction. J. Struct. Biol. 157, 138-147 (2007). (Pubitemid 44880788)
53. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996/01/01, 71-76 (1996). (Pubitemid 26093126)
54. Amat, F. et al. Markov random field based automatic image alignment for electron tomography. J. Struct. Biol. 161, 260-275 (2008). (Pubitemid 351375088)
55. Aistleitner, K. et al. Identification and characterization of a novel porin family highlights a major difference in the outer membrane of chlamydial symbionts and pathogens. PLoS One 8, e55010 (2013).
56. Frirdich, E. et al. Peptidoglycan-modifying enzyme Pgp1 is required for helical cell shape and pathogenicity traits in Campylobacter jejuni. PLoS. Pathog. 8, e1002602 (2012).