Bacterial cell enlargement requires control of cell wall stiffness mediated by peptidoglycan hydrolases

mBio

Volumn 6, Issue 4, 2015, Pages

  Wheeler, Richard ^a,b   Turner, Robert D ^a   Bailey, Richard G ^a   Salamaga, Bartłomiej ^a   Mesnage, Stéphane ^a   Mohamad, Sharifah A S ^a,c   Hayhurst, Emma J ^a,d   Horsburgh, Malcolm ^a,e   Hobbs, Jamie K ^a   Foster, Simon J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITI TEKNOLOGI MARA   (Malaysia)

^d UNIVERSITY OF GLAMORGAN   (United Kingdom)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSAMINIDASE; PEPTIDOGLYCAN; PEPTIDOGLYCAN HYDROLASE; PROTEIN ATL; PROTEIN SAGB; PROTEIN SCAH; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG; BETA N ACETYLHEXOSAMINIDASE;

ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BIOMECHANICS; CELL ENLARGEMENT; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RIGIDITY; STAPHYLOCOCCUS AUREUS; BIOPHYSICS; CELL WALL; ENZYMOLOGY; GENE INACTIVATION; GENETICS; METABOLISM; PHYSIOLOGY;

BIOPHYSICAL PHENOMENA; CELL ENLARGEMENT; CELL WALL; GENE KNOCKOUT TECHNIQUES; HEXOSAMINIDASES; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS;

EID: 84940842042     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00660-15     Document Type: Article

References (45)

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. Koch AL, Doyle RJ. 1985. Inside-to-outside growth and turnover of the wall of gram-positive rods. J Theor Biol 117:137–157. http://dx.doi.org/10.1016/S0022-5193(85)80169-7
3. Höltje J-V. 1993. Three for one —a simple growth mechanism that guarantees a precise copy of the thin, rod-shaped murein sacculus of Escherichia coli, p 419–426. In de Pedro MA, Höltje J-V, Löffelhardt W (ed), Bacterial growth and lysis: metabolism and structure of the bacterial sacculus. Springer, New York, NY
4. Bartual SG, Straume D, Stamsås GA, Muñoz IG, Alfonso C, Martínez- Ripoll M, Håvarstein LS, Hermoso JA. 2014. Structural basis of PcsBmediated cell separation in Streptococcus pneumoniae. Nat Commun 5:3842. http://dx.doi.org/10.1038/ncomms4842
5. Sham L-T, Barendt SM, Kopecky KE, Winkler ME. 2011. Essential PcsB-putative peptidoglycan hydrolase interacts with the essential FtsXSpn cell division protein in Streptococcus pneumoniae D39. Proc Natl Acad Sci U S A 108:E1061–E1069. http://dx.doi.org/10.1073/pnas.1108323108
6. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S, Jensen T, Jarmer H, Devine KM. 2007. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol Microbiol 65:180–200. http://dx.doi.org/10.1111/j.1365-2958.2007.05782.x
7. Singh S, SaiSree, Amrutha R, Reddy M. 2012. Three redundant murein endopeptidases catalyze an essential cleavage step in peptidoglycan synthesis of Escherichia coli K12. Mol Microbiol. 86:1036–1051. http://dx.doi.org/10.1111/mmi.12058
8. Vollmer W. 2012. Bacterial growth does require peptidoglycan hydrolases. Mol Microbiol 86:1031–1035. http://dx.doi.org/10.1111/mmi.12059
9. Pinho MG, Kjos M, Veening J-W. 2013. How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nat Rev Microbiol 11:601–614. http://dx.doi.org/10.1038/nrmicro3088
10. Uehara T, Bernhardt TG. 2011. More than just lysins: peptidoglycan hydrolases tailor the cell wall. Curr Opin Microbiol 14:698–703. http://dx.doi.org/10.1016/j.mib.2011.10.003
11. Turner R, Ratcliffe E, Wheeler R, Golestanian R, Hobbs J, Foster S. 2010. Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nat Commun 1:1–9
12. Pinho MG, Errington J. 2005. Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol Microbiol 55:799–807. http://dx.doi.org/10.1111/j.1365-2958.2004.04420.x
13. Zhou X, Halladin DK, Rojas ER, Koslover EF, Lee TK, Huang KC, Theriot JA. 2015. Mechanical crack propagation drives millisecond daughter cell separation in Staphylococcus aureus. Science 348:574–578. http://dx.doi.org/10.1126/science.aaa1511
14. Tzagoloff H, Novick R. 1977. Geometry of cell division in Staphylococcus aureus. J Bacteriol 129:343–350
15. Touhami A, Jericho MH, Beveridge TJ. 2004. Atomic force microscopy of cell growth and division in Staphylococcus aureus. J Bacteriol 186: 3286–3295. http://dx.doi.org/10.1128/JB.186.11.3286-3295.2004
16. Bailey RG, Turner RD, Mullin N, Clarke N, Foster SJ, Hobbs JK. 2014. The interplay between cell wall mechanical properties and the cell cycle in Staphylococcus aureus. Biophys J 107:2538–2545. http://dx.doi.org/10.1016/j.bpj.2014.10.036
17. Frankel MB, Hendrickx AP, Missiakas DM, Schneewind O. 2011. LytN, a murein hydrolase in the cross-wall compartment of Staphylococcus aureus, is involved in proper bacterial growth and envelope assembly. J Biol Chem 286:32593–32605. http://dx.doi.org/10.1074/jbc.M111.258863
18. Frankel MB, Schneewind O. 2012. Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J Biol Chem 287:10460–10471. http://dx.doi.org/10.1074/jbc.M111.336404
19. Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson I-M, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J Bacteriol 189:7316–7325. http://dx.doi.org/10.1128/JB.00734-07
20. Boneca IG, Huang Z-H, Gage DA, Tomasz A. 2000. Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new b-Nacetylglucosaminidase activity. J Biol Chem 275:9910–9918. http://dx.doi.org/10.1074/jbc.275.14.9910
21. Wheeler R, Mesnage S, Boneca IG, Hobbs JK, Foster SJ. 2011. Superresolution microscopy reveals cell wall dynamics and peptidoglycan architecture in ovococcal bacteria. Mol Microbiol 82:1096–1109. http://dx.doi.org/10.1111/j.1365-2958.2011.07871.x
22. Oshida T, Sugai M, Komatsuzawa H, Hong YM, Suginaka H, Tomasz A. 1995. A Staphylococcus aureus autolysin that has anN-acetylmuramoyl- L-alanine amidase domain and an endo-b-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization. Proc Natl Acad Sci U S A 92:285–289. http://dx.doi.org/10.1073/pnas.92.1.285
23. Foster SJ. 1995. Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177: 5723–5725
24. Kailas L, Ratcliffe EC, Hayhurst EJ, Walker MG, Foster SJ, Hobbs JK. 2009. Immobilizing live bacteria for AFM imaging of cellular processes. Ultramicroscopy 109:775–780. http://dx.doi.org/10.1016/j.ultramic.2009.01.012
25. Turner RD, Thomson NH, Kirkham J, Devine D. 2010. Improvement of the pore trapping method to immobilize vital coccoid bacteria for highresolution AFM: a study of Staphylococcus aureus. J Microsc 238:102–110. http://dx.doi.org/10.1111/j.1365-2818.2009.03333.x
26. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776. http://dx.doi.org/10.1016/S0092-8674(03)00421-5
27. Hayhurst EJ, Kailas L, Hobbs JK, Foster SJ. 2008. Cell wall peptidoglycan architecture in Bacillus subtilis. Proc Natl Acad Sci U S A 105: 14603–14608. http://dx.doi.org/10.1073/pnas.0804138105
28. Reed P, Veiga H, Jorge AM, Terrak M, Pinho MG. 2011. Monofunctional transglycosylases are not essential for Staphylococcus aureus cell wall synthesis. J Bacteriol 193:2549–2556. http://dx.doi.org/10.1128/JB.01474-10
29. Loskill P, Pereira PM, Jung P, Bischoff M, Herrmann M, Pinho MG, Jacobs K. 2014. Reduction of the peptidoglycan crosslinking causes a decrease in stiffness of the Staphylococcus aureus cell envelope. Biophys J 107:1082–1089. http://dx.doi.org/10.1016/j.bpj.2014.07.029
30. Turner R, Hurd A, Cadby A, Hobbs J, Foster S. 2013. Cell wall elongation mode in gram-negative bacteria is determined by peptidoglycan architecture. Nat Commun 4:1496. http://dx.doi.org/10.1038/ncomms2503
31. 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
32. 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
33. Beeby M, Gumbart JC, Roux B, Jensen GJ. 2013. Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 88:664–672. http://dx.doi.org/10.1111/mmi.12203
34. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, NY
35. Schenk S, Laddaga RA. 1992. Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol Lett 73:133–138
36. Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, Acevedo J, Read RC, Day NP, Peacock SJ, Mond JJ, Kokai-Kun JF, Foster SJ. 2006. Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193:1098–1108. http://dx.doi.org/10.1086/501471
37. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ. 2002. sB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184:5457–5467. http://dx.doi.org/10.1128/JB.184.19.5457-5467.2002
38. Pasztor L, Ziebandt A-K, Nega M, Schlag M, Haase S, Franz-Wachtel M, Madlung J, Nordheim A, Heinrichs DE, Götz F. 2010. Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J Biol Chem 285:36794–36803. http://dx.doi.org/10.1074/jbc.M110.167312
39. Mohamad SAS. 2007. Ph.D. thesis. University of Sheffield, Sheffield, South Yorkshire, United Kingdom
40. Kreiswirth BN, Löfdahl S, Betley MJ, O’Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709–712. http://dx.doi.org/10.1038/305709a0
41. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12:3967–3975
42. Kemp EH, Sammons RL, Moir A, Sun D, Setlow P. 1991. Analysis of transcriptional control of the gerD spore germination gene of Bacillus subtilis 168. J Bacteriol 173:4646–4652
43. Guérout-Fleury AM, Shazand K, Frandsen N, Stragier P. 1995. Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167:335–336. http://dx.doi.org/10.1016/0378-1119(95)00652-4
44. Vagner V, Dervyn E, Ehrlich SD. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144:3097–3104. http://dx.doi.org/10.1099/00221287-144-11-3097
45. Bottomley AL, Kabli AF, Hurd AF, Turner RD, Garcia-Lara J, Foster SJ. 2014. Staphylococcus aureus DivIB is a peptidoglycan-binding protein that is required for a morphological checkpoint in cell division. Mol Microbiol 94:1041–1064. http://dx.doi.org/10.1111/mmi.12813.