Critical cell wall hole size for lysis in Gram-positive bacteria

Journal of the Royal Society Interface

Volumn 10, Issue 80, 2013, Pages

  Mitchell, Gabriel J ^a   Wiesenfeld, Kurt ^b   Nelson, Daniel C ^c   Weitz, Joshua S ^a,b  

^a School of Biology   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Biophysics; Enzybiotic; Membrane dynamics; Microbiology

Indexed keywords

BACTERIA; BIOPHYSICS; CELLS; CYTOLOGY; MICROBIOLOGY; MOLECULES; TRANSMISSION ELECTRON MICROSCOPY;

BIOPHYSICAL THEORIES; CELL WALLS; CRITICAL CELLS; ENZYBIOTIC; GRAM-POSITIVE BACTERIUM; HOLE SIZE; MEMBRANE DYNAMICS; STREPTOCOCCUS PYOGENES; THEORETICAL PREDICTION; THROUGH HOLE;

WALL FUNCTION;

ARTICLE; BACILLUS CEREUS; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIOLYSIS; BIOPHYSICS; CELL HOLE SIZE; CELL MEMBRANE PERMEABILITY; CELLULAR PARAMETERS; GRAM POSITIVE BACTERIUM; INTERMETHOD COMPARISON; NONHUMAN; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PYOGENES; THICKNESS; TRANSMISSION ELECTRON MICROSCOPY; ACTIVE TRANSPORT; CELL WALL; MEMBRANE STRUCTURE; PHYSIOLOGY; ULTRASTRUCTURE;

BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE STRUCTURES; CELL WALL; MICROSCOPY, ELECTRON, TRANSMISSION; STREPTOCOCCUS PYOGENES;

MLCS; MLOWN;

EID: 84879140363     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0892     Document Type: Article

References (45)

1. Navarre WW, Schneewind O, Navarre WW. 1999 Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63, 174-229.
2. Scott JR, Barnett TC. 2006 Surface proteins of Grampositive bacteria and how they get there. Annu. Rev. Microbiol. 60, 397-423. (doi:10.1146/annurev. micro.60.080805.142256).
3. Boothby D, Daneo-Moore L, Higgins ML, Coyette J, Shockman GD. 1973 Turnover of bacterial cell wall peptidoglycans. J. Biol. Chem. 248, 2161-2169.
4. Scheffers DJ, Pinho MG. 2005 Bacterial cell wall synthesis: new insights from localization studies. Microbiol. Mol. Biol. Rev. 69, 585-607. (doi:10. 1128/MMBR.69.4.585-607.2005).
5. Neu HC. 1992 The crisis in antibiotic resistance. Nat. Med. 256, 1064-1073.
6. Levy SB, Marshall B. 2004 Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10, S122-S129. (doi:10.1038/nm1145).
7. Zetola N, Francis JS, Nuermberger EL, Bishai WR. 2005 Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect. Dis. 5, 275-286. (doi:10.1016/S1473- 3099(05)70112-2).
8. Klevens RM et al. 2007 Invasive methicillin-resistant Staphylococcus aureus infections in the United States. J. Am. Med. Assoc. 298, 1763-1771. (doi:10.1001/jama.298.15.1763).
9. Fischbach MA, Walsh CT. 2009 Antibiotics for emerging pathogens. Science 325, 1089-1093. (doi:10.1126/science.1176667).
10. Clardy J, Fischbach MA, Walsh CT. 2006 New antibiotics from bacterial natural products. Nat. Biotechnol. 24, 1541-1550. (doi:10.1038/nbt1266).
11. Hancock REW, Sahl HG. 2006 Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557. (doi:10.1038/nbt1267).
12. Giuliani A, Pirri G, Nicoletto SF. 2007 Antimicrobial peptides: an overview of a promising class of therapeutics. Cent. Eur. J. Biol. 2, 1-33. (doi:10. 2478/s11535-007-0010-5).
13. Salazar O, Asenjo J. 2007 Enzymatic lysis of microbial cells. Biotechnol. Lett. 29, 985-994. (doi:10.1007/s10529-007-9345-2).
14. Andre G, Leenhouts K, Hols P, Dufrêne YF. 2008 Detection and localization of single LysM- peptidoglycan interactions. J. Bacteriol. 190, 7079-7086. (doi:10.1128/JB.00519-08).
15. Francius G, Domenech O, Mingeot-Leclercq MP, Dufrêne YF. 2008 Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. J. Bacteriol. 190, 7904-7909. (doi:10.1128/JB.01116-08).
16. Matsuzaki S et al. 2005 Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J. Infect. Chemother. 11, 211-219. (doi:10.1007/s10156-005-0408-9).
17. Daly KE, Huang KC, Wingreen NS, Mukhopadhyay R. 2011 Mechanics of membrane bulging during cellwall disruption in Gram-negative bacteria. Phys. Rev. E 83, 041922. (doi:10.1103/PhysRevE.83. 041922).
18. Vollmer W, Blanot D, de Pedro MA. 2008 Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149-167. (doi:10.1111/j.1574- 6976.2007.00094.x).
19. Weidenmaier C, Peschel A. 2008 Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6, 276-287. (doi:10.1038/nrmicro1861).
20. Schleifer KH, Kandler O. 1972 Peptidoglycan types of bacterial cell walls and their taxonomic implications. Microbiol. Mol. Biol. Rev. 36, 407-477.
21. Wagner B. 1978 An electron microscopic study of the location of peptidoglycan in group A and C streptococcal cell walls. Microbiology 108, 283-294.
22. Jiang W, Saxena A, Song B, Ward BB, Beveridge TJ, Myneni SCB. 2004 Elucidation of functional groups on Gram-positive and Gram-negative bacterial surfaces using infrared spectroscopy. Langmuir 20, 11 433-11 442. (doi:10.1021/la049043+).
23. Huang KC, Mukhopadhyay R, Wen B, Gitai Z, Wingreen NS. 2008 Cell shape and cell-wall organization in Gram-negative bacteria. Proc. Natl Acad. Sci. USA 105, 19 282-19 287. (doi:10.1073/pnas.0805309105).
24. Wang S, Furchtgott L, Huang KC, Shaevitz JW. 2012 Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc. Natl Acad. Sci. USA 109, E595-E604. (doi:10.1073/pnas. 1117132109).
25. McGowan S et al. 2012 X-ray crystal structure of the streptococcal specific phage lysin PlyC. Proc. Natl Acad. Sci. USA 109, 12 752-12 757. (doi:10.1073/pnas.1208424109).
26. Do Carmo M. 1976 Differential geometry of curves and surfaces. Englewood Cliffs, NJ: Prentice Hall.
27. Lipowsky R. 1991 The conformation of membranes. Nature 349, 475-481. (doi:10.1038/349475a0).
28. Helfrich W. 1973 Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch 28, 693-703.
29. Nelson D, Loomis L, Fischetti VA. 2001 Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl Acad. Sci. USA 98, 4107-4112. (doi:10.1073/pnas. 061038398).
30. Weaver JC, Chizmadzhev YA. 1996 Theory of electroporation: a review. Bioelectrochem. Bioenerg. 41, 135-160. (doi:10.1016/S0302-4598(96)05062-3).
31. Mitchell P, Moyle J. 1956 Osmotic function and structure in bacteria. In 6th Symp. Soc. Gen. Microbiol, pp. 150-180. Cambridge, UK: Cambridge University Press.
32. Marquis R, Carstensen E. 1973 Electric conductivity and internal osmolality of intact bacterial cells. J. Bacteriol. 113, 1198-1206.
33. Phillips RB, Kondev J, Theriot J, Orme N, Garcia H. 2009 Physical biology of the cell. New York, NY: Garland Science.
34. Demchick P, Koch AL. 1996 The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J. Bacteriol. 178, 768-773.
35. Meyer TH, Breitling R, Miller KR, Akey CW, Rapoport TA. 1999 The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J. Mol. Biol. 285, 1789-1800. (doi:10.1006/jmbi.1998.2413).
36. Meroueh SO, Bencze KZ, Hesek D, Lee M, Fisher JF, Stemmler TL, Mobashery S. 2006 Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc. Natl Acad. Sci. USA 103, 4404-4409. (doi:10. 1073/pnas.0510182103).
37. Loeffler JM, Nelson D, Fischetti VA. 2001 Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294, 2170-2172. (doi:10.1126/science.1066869).
38. Daniel A et al. 2010 Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 54, 1603-1612. (doi:10.1128/AAC. 01625-09).
39. Fischetti VA. 2005 Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol. 13, 491-496. (doi:10.1016/j.tim.2005.08.007).
40. Hunter JB, Asenjo JA. 1988 A structured mechanistic model of the kinetics of enzymatic lysis and disruption of yeast cells. Biotechnol. Bioeng. 31, 929-943. (doi:10.1002/bit.260310906).
41. Rabinovitch A. 1999 Bacterial lysis by phage: a theoretical model. J. Theor. Biol. 201, 209-213. (10.1006/jtbi.1999.1029).
42. Mitchell GJ, Nelson DC, Weitz JS. 2010 Quantifying enzymatic lysis: estimating the combined effects of chemistry, physiology and physics. Phys. Biol. 7, 046002. (doi:10.1088/1478- 3975/7/4/046002).
43. Matias VRF, Beveridge TJ. 2007 Cryo-electron microscopy of cell division in Staphylococcus aureus reveals a midzone between nascent cross walls. Mol. Microbiol. 64, 195-206. (doi:10.1111/j.1365-2958.2007.05634.x).
44. Touhami A, Jericho MH, Beveridge TJ. 2004 Atomic force microscopy of cell growth and division in Staphylococcus aureus. J Bacteriol. 186, 3286- 3295. (doi:10.1128/JB.186.11.3286-3295.2004).
45. Nelson D, Schuch R, Chahales P, Zhu S, Fischetti VA. 2006 PlyC: a multimeric bacteriophage lysin. Proc. Natl Acad. Sci. USA 103, 10 765-10 770. (doi:10. 1073/pnas.0604521103).