Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 36, 2015, Pages 11347-11352

  Yahashiri, Atsushi ^a   Jorgenson, Matthew A ^a,b   Weiss, David S ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Amidase; Cell division; Divisome; Lytic transglycosylase; Murein

Indexed keywords

AMIDASE; BACTERIAL PROTEIN; DAMX PROTEIN; DEDD PROTEIN; FTSN PROTEIN; GLYCAN; GLYCOSYLTRANSFERASE; PEPTIDOGLYCAN; RLPA PROTEIN; SPOR DOMAIN PROTEIN; UNCLASSIFIED DRUG; DAMX PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; GREEN FLUORESCENT PROTEIN; PEPTIDE; PROTEIN BINDING;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BINDING SITE; BIOGENESIS; CELL DIVISION; CONTROLLED STUDY; DEGRADATION; ESCHERICHIA COLI; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN TARGETING; SACCULUS; SEPTUM PELLUCIDUM; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CELL WALL; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; MUTATION; PHASE CONTRAST MICROSCOPY;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BINDING SITES; CELL DIVISION; CELL WALL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; MODELS, BIOLOGICAL; MUTATION; PEPTIDES; PEPTIDOGLYCAN; PROTEIN BINDING;

EID: 84941243813     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508536112     Document Type: Article

References (52)

1. Vollmer W, Blanot D, de Pedro MA (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32(2):149-167.
2. Turner RD, Vollmer W, Foster SJ (2014) Different walls for rods and balls: The diversity of peptidoglycan. Mol Microbiol 91(5):862-874.
3. Silver LL (2013) Viable screening targets related to the bacterial cell wall. Ann N Y Acad Sci 1277:29-53.
4. Bush K (2012) Antimicrobial agents targeting bacterial cell walls and cell membranes. Rev Sci Tech 31(1):43-56.
5. Lutkenhaus J, Pichoff S, Du S (2012) Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken) 69(10):778-790.
6. Egan AJ, Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8-28.
7. Vollmer W, Joris B, Charlier P, Foster S (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32(2):259-286.
8. Heidrich C, et al. (2001) Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 41(1):167-178.
9. Heidrich C, Ursinus A, Berger J, Schwarz H, Höltje JV (2002) Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J Bacteriol 184(22):6093-6099.
10. Priyadarshini R, de Pedro MA, Young KD (2007) Role of peptidoglycan amidases in the development and morphology of the division septum in Escherichia coli. J Bacteriol 189(14):5334-5347.
11. Priyadarshini R, Popham DL, Young KD (2006) Daughter cell separation by penicillinbinding proteins and peptidoglycan amidases in Escherichia coli. J Bacteriol 188(15):5345-5355.
12. Blackman SA, Smith TJ, Foster SJ (1998) The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144(Pt 1):73-82.
13. Ohnishi R, Ishikawa S, Sekiguchi J (1999) Peptidoglycan hydrolase LytF plays a role in cell separation with CwlF during vegetative growth of Bacillus subtilis. J Bacteriol 181(10):3178-3184.
14. Chen R, Guttenplan SB, Blair KM, Kearns DB (2009) Role of the sigmaD-dependent autolysins in Bacillus subtilis population heterogeneity. J Bacteriol 191(18):5775-5784.
15. Möll A, Thanbichler M (2009) FtsN-like proteins are conserved components of the cell division machinery in proteobacteria. Mol Microbiol 72(4):1037-1053.
16. Gerding MA, et al. (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(24):7383-7401.
17. Arends SJ, et al. (2010) Discovery and characterization of three new Escherichia coli septal ring proteins that contain a SPOR domain: DamX, DedD, and RlpA. J Bacteriol 192(1):242-255.
18. Lutkenhaus J (2009) FtsN-trigger for septation. J Bacteriol 191(24):7381-7382.
19. Dai K, Xu Y, Lutkenhaus J (1993) Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J Bacteriol 175(12):3790-3797.
20. Ursinus A, et al. (2004) Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli. J Bacteriol 186(20):6728-6737.
21. Williams KB, et al. (2013) Nuclear magnetic resonance solution structure of the peptidoglycan-binding SPOR domain from Escherichia coli DamX: Insights into septal localization. Biochemistry 52(4):627-639.
22. Duncan TR, Yahashiri A, Arends SJ, Popham DL, Weiss DS (2013) Identification of SPOR domain amino acids important for septal localization, peptidoglycan binding, and a disulfide bond in the cell division protein FtsN. J Bacteriol 195(23):5308-5315.
23. Müller P, et al. (2007) The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem 282(50):36394-36402.
24. Scheurwater E, Reid CW, Clarke AJ (2008) Lytic transglycosylases: Bacterial spacemaking autolysins. Int J Biochem Cell Biol 40(4):586-591.
25. van Heijenoort J (2011) Peptidoglycan hydrolases of Escherichia coli. Microbiol Mol Biol Rev 75(4):636-663.
26. Lee M, et al. (2013) Reactions of all Escherichia coli lytic transglycosylases with bacterial cell wall. J Am Chem Soc 135(9):3311-3314.
27. Jorgenson MA, Chen Y, Yahashiri A, Popham DL, Weiss DS (2014) The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa. Mol Microbiol 93(1):113-128.
28. Uehara T, Park JT (2007) An anhydro-N-acetylmuramyl-L-alanine amidase with broad specificity tethered to the outer membrane of Escherichia coli. J Bacteriol 189(15):5634-5641.
29. Goehring NW, Beckwith J (2005) Diverse paths to midcell: Assembly of the bacterial cell division machinery. Curr Biol 15(13):R514-R526.
30. de Boer PA (2010) Advances in understanding E. coli cell fission. Curr Opin Microbiol 13(6):730-737.
31. Di Lallo G, Fagioli M, Barionovi D, Ghelardini P, Paolozzi L (2003) Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: Bacterial septosome differentiation. Microbiology 149(Pt 12):3353-3359.
32. Buddelmeijer N, Beckwith J (2004) A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol Microbiol 52(5):1315-1327.
33. Karimova G, Dautin N, Ladant D (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187(7):2233-2243.
34. Daniel RA, Noirot-Gros MF, Noirot P, Errington J (2006) Multiple interactions between the transmembrane division proteins of Bacillus subtilis and the role of FtsL instability in divisome assembly. J Bacteriol 188(21):7396-7404.
35. Alexeeva S, Gadella TW, Jr, Verheul J, Verhoeven GS, den Blaauwen T (2010) Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77(2):384-398.
36. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: Cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74(4):504-528.
37. Höltje JV, Heidrich C (2001) Enzymology of elongation and constriction of the murein sacculus of Escherichia coli. Biochimie 83(1):103-108.
38. Uehara T, Parzych KR, Dinh T, Bernhardt TG (2010) Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J 29(8):1412-1422.
39. Bernhardt TG, de Boer PA (2003) The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol 48(5):1171-1182.
40. Uehara T, Dinh T, Bernhardt TG (2009) LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J Bacteriol 191(16):5094-5107.
41. Peters NT, Dinh T, Bernhardt TG (2011) A fail-safe mechanism in the septal ring assembly pathway generated by the sequential recruitment of cell separation amidases and their activators. J Bacteriol 193(18):4973-4983.
42. Eberhardt C, Kuerschner L, Weiss DS (2003) Probing the catalytic activity of a cell division-specific transpeptidase in vivo with beta-lactams. J Bacteriol 185(13):3726-3734.
43. Ize B, Stanley NR, Buchanan G, Palmer T (2003) Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol 48(5):1183-1193.
44. Korsak D, Liebscher S, Vollmer W (2005) Susceptibility to antibiotics and beta-lactamase induction in murein hydrolase mutants of Escherichia coli. Antimicrob Agents Chemother 49(4):1404-1409.
45. de Pedro MA, Quintela JC, Höltje JV, Schwarz H (1997) Murein segregation in Escherichia coli. J Bacteriol 179(9):2823-2834.
46. Potluri LP, Kannan S, Young KD (2012) ZipA is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J Bacteriol 194(19):5334-5342.
47. Hayashi K (1975) A rapid determination of sodium dodecyl sulfate with methylene blue. Anal Biochem 67(2):503-506.
48. McPherson DC, Popham DL (2003) Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus subtilis. J Bacteriol 185(4):1423-1431.
49. Pogliano K, Harry E, Losick R (1995) Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol Microbiol 18(3):459-470.
50. Tarry M, et al. (2009) The Escherichia coli cell division protein and model Tat substrate SufI (FtsP) localizes to the septal ring and has a multicopper oxidase-like structure. J Mol Biol 386(2):504-519.
51. Baba T, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:2006.0008.
52. R cassettes with the option of Flp-catalyzed excision of the antibioticresistance determinant. Gene 158(1):9-14.