Enterococcus faecium biofilm formation: Identification of major autolysin AtlAefm, associated acm surface localization, and AtlAefm-independent extracellular DNA release

mBio

Volumn 4, Issue 2, 2013, Pages

  Paganelli, Fernanda L ^a   Willems, Rob J L Willems ^a   Jansen, Pamela ^a   Hendrickx, Antoni ^a   Zhang, Xinglin ^a   Bonten, Marc J M Bonten ^a   Leavis, Helen L ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACM PROTEIN; AUTOLYSIN; BACTERIAL DNA; COLLAGEN TYPE 1; COLLAGEN TYPE 4; UNCLASSIFIED DRUG; VIRULENCE FACTOR; ACM PROTEIN, ENTEROCOCCUS FAECIUM; ADHESIN; COLLAGEN; N ACETYLMURAMOYLALANINE AMIDASE;

ARTICLE; AUTOLYSIN GENE; BACTERIAL GENE; BACTERIOLYSIS; BACTERIUM ADHERENCE; BIOFILM; BIOINFORMATICS; CELL INTERACTION; CELL SURFACE; CELL WALL; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; GENE INSERTION; GENE LOCUS; GENETIC ANALYSIS; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; STRAIN DIFFERENCE; WILD TYPE; BIOLOGY; CHEMISTRY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PHYSIOLOGY;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BIOFILMS; CELL WALL; COLLAGEN; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; ENTEROCOCCUS FAECIUM; GENE KNOCKOUT TECHNIQUES; HUMANS; MUTAGENESIS, INSERTIONAL; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; VIRULENCE FACTORS;

EID: 84880059458     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00154-13     Document Type: Article

References (51)

1. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, Fridkin SK, National Healthcare Safety Network Team, Participating National Healthcare Safety Network Facilities. 2008. NHSN annual update: antimicrobial-resistant pathogens associated with healthcareassociated infections: annual summary of data reported to the national healthcare safety network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29:996-1011
2. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193
3. Sandoe JA, Witherden IR, Cove JH, Heritage J, Wilcox MH. 2003. Correlation between enterococcal biofilm formation in vitro and medicaldevice-related infection potential in vivo. J. Med. Microbiol. 52:547-550
4. O'Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79
5. Abee T, Kovács AT, Kuipers OP, van der Veen S. 2011. Biofilm formation and dispersal in Gram-positive bacteria. Curr. Opin. Biotechnol. 22: 172-179
6. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T. 2006. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59:1114-1128
7. Petersen FC, Tao L, Scheie AA. 2005. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J. Bacteriol. 187:4392-4400
8. Ahn SJ, Burne RA. 2006. The atlA operon of Streptococcus mutans: role in autolysin maturation and cell surface biogenesis. J. Bacteriol. 188: 6877-6888
9. Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D. 2007. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083-2092
10. Vilain S, Pretorius JM, Theron J, Brözel VS. 2009. DNA as an adhesin: Bacillus cereus requires extracellularDNAto form biofilms. Appl. Environ. Microbiol. 75:2861-2868
11. Thomas VC, Hiromasa Y, Harms N, Thurlow L, Tomich J, Hancock LE. 2009. A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol. Microbiol. 72:1022-1036
12. Izano EA, Amarante MA, Kher WB, Kaplan JB. 2008. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl. Environ. Microbiol. 74:470-476
13. Bose JL, Lehman MK, Fey PD, Bayles KW. 2012. Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS One 7:e42244
14. Thomas VC, Thurlow LR, Boyle D, Hancock LE. 2008. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J. Bacteriol. 190: 5690-5698
15. Heilmann C, Hartleib J, Hussain MS, Peters G. 2005. The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect. Immun. 73:4793-4802
16. Allignet J, Aubert S, Dyke KG, El Solh N. 2001. Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect. Immun. 69:712-718
17. Heilmann C, Hussain M, Peters G, Götz F. 1997. Evidence for autolysinmediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol. 24:1013-1024
18. Liu G, Xiang H, Tang X, Zhang K, Wu X, Wang X, Guo N, Feng H, Wang G, Liu L, Shi Q, Shen F, Xing M, Yuan P, Liu M, Yu L. 2011. Transcriptional and functional analysis shows sodium houttuyfonate- mediated inhibition of autolysis in Staphylococcus aureus. Molecules 16: 8848-8865
19. Schlag M, Biswas R, Krismer B, Kohler T, Zoll S, Yu W, Schwarz H, Peschel A, Götz F. 2010. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol. Microbiol. 75:864-873
20. O'Gara JP. 2007. Ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270:179-188
21. Nallapareddy SR, Weinstock GM, Murray BE. 2003. Clinical isolates of Enterococcus faecium exhibit strain-specific collagen binding mediated by ACM, a new member of the MSCRAMM family. Mol. Microbiol. 47: 1733-1747
22. Shockman GD, Holtje J-V. 1994. Microbial peptidoglycan (murein) hydrolases, p 131-166. In Ghuysen J-M, Hakenbeck R (ed), Bacterial cell wall. Elsevier, Amsterdam, the Netherlands.
23. Eckert C, Lecerf M, Dubost L, Arthur M, Mesnage S. 2006. Functional analysis of AtlA, the majorN-acetylglucosaminidase of Enterococcus faecalis. J. Bacteriol. 188:8513- 8519
24. Buist G, Steen A, Kok J, Kuipers OP. 2008. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68: 838-847
25. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH. 2013. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 41:D348-D352
26. Emirian A, Fromentin S, Eckert C, Chau F, Dubost L, Delepierre M, Gutmann L, Arthur M, Mesnage S. 2009. Impact of peptidoglycan O-acetylation on autolytic activities of the Enterococcus faecalis N-acetylglucosaminidase AtlA and N-acetylmuramidase AtlB. FEBS Lett. 583:3033-3038
27. Shibata Y, Kawada M, Nakano Y, Toyoshima K, Yamashita Y. 2005. Identification and characterization of an autolysin-encoding gene of Streptococcus mutans. Infect. Immun. 73:3512-3520
28. Mohamed JA, Huang W, Nallapareddy SR, Teng F, Murray BE. 2004. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72: 3658-3663
29. Gross M, Cramton SE, Götz F, Peschel A. 2001. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69:3423-3426
30. Koprivnjak T, Mlakar V, Swanson L, Fournier B, Peschel A, Weiss JP. 2006. Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J. Bacteriol. 188:3622-3630
31. Mesnage S, Chau F, Dubost L, Arthur M. 2008. Role of N-acetylglucosaminidase and N-acetylmuramidase activities in Enterococcus faecalis peptidoglycan metabolism. J. Biol. Chem. 283:19845-19853
32. Barnes AM, Ballering KS, Leibman RS, Wells CL, Dunny GM. 2012. Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. mBio 3(4):e00193-12
33. Li YH, Lau PC, Tang N, Svensäter G, Ellen RP, Cvitkovitch DG. 2002. Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J. Bacteriol. 184:6333-6342
34. Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG. 2002. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184:2699-2708
35. Wen ZT, Burne RA. 2002. Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl. Environ. Microbiol. 68:1196-1203
36. Koraimann G. 2003. Lytic transglycosylases in macromolecular transport systems of gram-negative bacteria. Cell. Mol. Life Sci. 60:2371-2388
37. Miller EJ, Gay S. 1987. The collagens: an overview and update. Methods Enzymol. 144:3-41
38. Qin X, Singh KV, Xu Y, Weinstock GM, Murray BE. 1998. Effect of disruption of a gene encoding an autolysin of Enterococcus faecalis OG1RF. Antimicrob. Agents Chemother. 42:2883-2888
39. Paganelli FL, Willems RJ, Leavis HL. 2012. Optimizing future treatment of enterococcal infections: attacking the biofilm? Trends Microbiol. 20: 40-49
40. van Schaik W, Top J, Riley DR, Boekhorst J, Vrijenhoek JE, Schapendonk CM, Hendrickx AP, Nijman IJ, Bonten MJ, Tettelin H, Willems RJ. 2010. Pyrosequencing-based comparative genome analysis of the nosocomial pathogen Enterococcus faecium and identification of a large transferable pathogenicity island. BMC Genomics 11:239
41. Leenhouts K, Buist G, Bolhuis A, ten Berge A, Kiel J, Mierau I, Dabrowska M, Venema G, Kok J. 1996. A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol. Gen. Genet. 253:217-224
42. Zhang X, Paganelli FL, Bierschenk D, Kuipers A, Bonten MJ, Willems RJ, van Schaik W. 2012. Genome-wide identification of ampicillin resistance determinants in Enterococcus faecium. PLoS Genet. 8:e1002804
43. Zhang X, Vrijenhoek JE, Bonten MJ, Willems RJ, van Schaik W. 2011. Agenetic element present on megaplasmids allows Enterococcus faecium to use raffinose as carbon source. Environ. Microbiol. 13:518-528
44. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, Harrison M, Burgis TA, Lockyer M, Garcia-Lara J, Foster SJ, Pleasance SJ, Peters SE, Maskell DJ, Charles IG. 2009. Comprehensive identification of essential Staphylococcus aureus genes using transposon-mediated differential hybridisation (TMDH). BMC Genomics 10:291
45. Liu Y, Burne RA. 2011. The major autolysin of Streptococcus gordonii is subject to complex regulation and modulates stress tolerance, biofilm formation, and extracellular-DNA release. J. Bacteriol. 193:2826-2837
46. Ju CX, Gu HW, Lu CP. 2012. Characterization and functional analysis of atl, a novel gene encoding autolysin in Streptococcus suis. J. Bacteriol. 194: 1464-1473
47. Heikens E, Bonten MJ, Willems RJ. 2007. Enterococcal surface protein Esp is important for biofilm formation of Enterococcus faecium E1162. J. Bacteriol. 189:8233-8240
48. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407
49. Bardoel BW, van Kessel KP, van Strijp JA, Milder FJ. 2012. Inhibition of Pseudomonas aeruginosa virulence: characterization of the AprA-Apri interface and species selectivity. J. Mol. Biol. 415:573-583
50. Hendrickx AP, van Wamel WJ, Posthuma G, Bonten MJ, Willems RJ. 2007. Five genes encoding surface-exposed LPXTG proteins are enriched in hospital-adapted Enterococcus faecium clonal complex 17 isolates. J. Bacteriol. 189:8321-8332
51. Hendrickx AP, van Luit-Asbroek M, Schapendonk CM, van Wamel WJ, Braat JC, Wijnands LM, Bonten MJ, Willems RJ. 2009. SgrA, a nidogenbinding LPXTG surface adhesin implicated in biofilm formation, and EcbA, a collagen binding MSCRAMM, are two novel adhesins of hospitalacquired Enterococcus faecium. Infect. Immun. 77:5097-5106.