Extracellular DNA facilitates the formation of functional amyloids in Staphylococcus aureus biofilms

Molecular Microbiology

Volumn 99, Issue 1, 2016, Pages 123-134

  Schwartz, Kelly ^a   Ganesan, Mahesh ^a   Payne, David E ^a,b   Solomon, Michael J ^a   Boles, Blaise R ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; BACTERIAL PROTEIN; DNA; EXTRACELLULAR DNA; PHENOL SOLUBLE MODULIN PEPTIDE; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL TOXIN; STAPHYLOCOCCAL DELTA TOXIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BIOFILM; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; GLYCOPROTEIN SYNTHESIS; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN POLYMERIZATION; STAPHYLOCOCCUS AUREUS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

AMYLOID; BACTERIAL TOXINS; BIOFILMS; DNA, BACTERIAL; STAPHYLOCOCCUS AUREUS;

EID: 84955195607     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13219     Document Type: Article

References (79)

1. Alteri, C.J., Xicohtencatl-Cortes, J., Hess, S., Caballero-Olin, G., Giron, J.A., and Friedman, R.L. (2007) Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci USA 104: 5145-5150.
2. Baba, T., and Schneewind, O. (1998) Targeting of muralytic enzymes to the cell division site of Gram-positive bacteria: repeat domains direct autolysin to the equatorial surface ring of Staphylococcus aureus. EMBO J 17: 4639-4646.
3. Barrantes, A., Rejas, M.T., Benitez, M.J., and Jimenez, J.S. (2007) Interaction between Alzheimer's Abeta1-42 peptide and DNA detected by surface plasmon resonance. J Alzheimers Dis 12: 345-355.
4. Beenken, K.E., Spencer, H., Griffin, L.M., and Smeltzer, M.S. (2012) Impact of extracellular nuclease production on the biofilm phenotype of Staphylococcus aureus under in vitro and in vivo conditions. Infect Immun 80: 1634-1638.
5. Berne, B.J.A.P.R., (2000) Dynamic light scattering: with applications to chemistry, biology, and physics. Courier corporation.
6. Bieler, S., Estrada, L., Lagos, R., Baeza, M., Castilla, J., and Soto, C. (2005) Amyloid formation modulates the biological activity of a bacterial protein. J Biol Chem 280: 26880-26885.
7. Biswas, R., Voggu, L., Simon, U.K., Hentschel, P., Thumm, G., and Gotz, F. (2006) Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259: 260-268.
8. Boles, B.R., and Horswill, A.R. (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4: e1000052.
9. Boles, B.R., Thoendel, M., Roth, A.J., and Horswill, A.R. (2010) Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS ONE 5: e10146.
10. Bose, J.L., Lehman, M.K., Fey, P.D., and Bayles, K.W. (2012) Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS ONE 7: e42244.
11. Brinkmann, V., and Zychlinsky, A. (2007) Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 5: 577-582.
12. Calamai, M., Kumita, J.R., Mifsud, J., Parrini, C., Ramazzotti, M., Ramponi, G., etal. (2006) Nature and significance of the interactions between amyloid fibrils and biological polyelectrolytes. Biochemistry 45: 12806-12815.
13. Camero, S., Ayuso, J.M., Barrantes, A., Benitez, M.J., and Jimenez, J.S. (2013) Specific binding of DNA to aggregated forms of Alzheimer's disease amyloid peptides. Int J Biol Macromol 55: 201-206.
14. Carny, O., and Gazit, E. (2005) A model for the role of short self-assembled peptides in the very early stages of the origin of life. FASEB J 19: 1051-1055.
15. Chapman, M.R., Robinson, L.S., Pinkner, J.S., Roth, R., Heuser, J., Hammar, M., etal. (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science (New York, N.Y.) 295: 851-855.
16. Chiang, W.C., Nilsson, M., Jensen, P.O., Hoiby, N., Nielsen, T.E., Givskov, M., and Tolker-Nielsen, T. (2013) Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 57: 2352-2361.
17. Conover, M.S., Mishra, M., and Deora, R. (2011) Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE 6: e16861.
18. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M.A., Brentani, R.R., Foguel, D., and Silva, J.L. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276: 49400-49409.
19. Deleault, N.R., Harris, B.T., Rees, J.R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc Natl Acad Sci USA 104: 9741-9746.
20. DePas, W.H., and Chapman, M.R. (2012) Microbial manipulation of the amyloid fold. Res Microbiol 163: 592-606.
21. Di Domizio, J., Dorta-Estremera, S., Gagea, M., Ganguly, D., Meller, S., Li, P., etal. (2012a) Nucleic acid-containing amyloid fibrils potently induce type I interferon and stimulate systemic autoimmunity. Proc Natl Acad Sci USA 109: 14550-14555.
22. Di Domizio, J., Zhang, R., Stagg, L.J., Gagea, M., Zhuo, M., Ladbury, J.E., and Cao, W. (2012b) Binding with nucleic acids or glycosaminoglycans converts soluble protein oligomers to amyloid. J Biol Chem 287: 736-747.
23. Dominiak, D.M., Nielsen, J.L., and Nielsen, P.H. (2011) Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 13: 710-721.
24. Dueholm, M.S., Petersen, S.V., Sonderkaer, M., Larsen, P., Christiansen, G., Hein, K.L., etal. (2010) Functional amyloid in Pseudomonas. Mol Microbiol 77: 1009-1020.
25. Fernandez-Tresguerres, M.E., de la Espina, S.M., Gasset-Rosa, F., and Giraldo, R. (2010) A DNA-promoted amyloid proteinopathy in Escherichia coli. Mol Microbiol 77: 1456-1469.
26. Flemming, H.C., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
27. Foster, T.J., Geoghegan, J.A., Ganesh, V.K., and Hook, M. (2014) Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12: 49-62.
28. Foulston, L., Elsholz, A.K., DeFrancesco, A.S., and Losick, R. (2014) The extracellular matrix of Staphylococcus aureus biofilms comprises cytoplasmic proteins that associate with the cell surface in response to decreasing pH. mBio 5: e1667-e1614.
29. Gallo, P.M., Rapsinski, G.J., Wilson, R.P., Oppong, G.O., Sriram, U., Goulian, M., etal. (2015) Amyloid-DNA composites of bacterial biofilms stimulate autoimmunity. Immunity 42: 1171-1184.
30. Ganesan, M., Stewart, E.J., Szafranski, J., Satorius, A.E., Younger, J.G., and Solomon, M.J. (2013) Molar mass, entanglement, and associations of the biofilm polysaccharide of Staphylococcus epidermidis. Biomacromolecules 14: 1474-1481.
31. Gloag, E.S., Turnbull, L., Huang, A., Vallotton, P., Wang, H., Nolan, L.M., etal. (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 110: 11541-11546.
32. Gotz, F. (2002) Staphylococcus and biofilms. Mol Microbiol 43: 1367-1378.
33. Gour, N., Kedracki, D., Safir, I., Ngo, K.X., and Vebert-Nardin, C. (2012) Self-assembling DNA-peptide hybrids: morphological consequences of oligonucleotide grafting to a pathogenic amyloid fibrils forming dipeptide. Chem Commun (Camb) 48: 5440-5442.
34. Hegde, M.L., and Rao, K.S. (2007) DNA induces folding in alpha-synuclein: understanding the mechanism using chaperone property of osmolytes. Arch Biochem Biophys 464: 57-69.
35. Heilmann, C., Hussain, M., Peters, G., and Gotz, F. (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24: 1013-1024.
36. Horsburgh, M.J., Aish, J.L., White, I.J., Shaw, L., Lithgow, J.K., and Foster, S.J. (2002) sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184: 5457-5467.
37. Houston, P., Rowe, S.E., Pozzi, C., Waters, E.M., and O'Gara, J.P. (2011) Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun 79: 1153-1165.
38. Hu, W., Li, L., Sharma, S., Wang, J., McHardy, I., Lux, R., etal. (2012) DNA builds and strengthens the extracellular matrix in Myxococcus xanthus biofilms by interacting with exopolysaccharides. PLoS ONE 7: e51905.
39. Huseby, M.J., Kruse, A.C., Digre, J., Kohler, P.L., Vocke, J.A., Mann, E.E., etal. (2010) Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. Proc Natl Acad Sci USA 107: 14407-14412.
40. Jakubovics, N.S., Shields, R.C., Rajarajan, N., and Burgess, J.G. (2013) Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 57: 467-475.
41. Jones, E.A., McGillivary, G., and Bakaletz, L.O. (2013) Extracellular DNA within a nontypeable Haemophilus influenzae-induced biofilm binds human beta defensin-3 and reduces its antimicrobial activity. J innate Immun 5: 24-38.
42. Kiedrowski, M.R., Kavanaugh, J.S., Malone, C.L., Mootz, J.M., Voyich, J.M., Smeltzer, M.S., etal. (2011) Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS ONE 6: e26714.
43. Landini, P. (2009) Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res Microbiol 160: 259-266.
44. LeVine, H., 3rd (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309: 274-284.
45. Li, M., Diep, B.A., Villaruz, A.E., Braughton, K.R., Jiang, X., DeLeo, F.R., etal. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 106: 5883-5888.
46. Lowy, F.D. (1998) Staphylococcus aureus infections. NEJM 339: 520-532.
47. Malone, C.L., Boles, B.R., Lauderdale, K.J., Thoendel, M., Kavanaugh, J.S., and Horswill, A.R. (2009) Fluorescent reporters for Staphylococcus aureus. J Microbiol Methods 77: 251-260.
48. Mann, E.E., Rice, K.C., Boles, B.R., Endres, J.L., Ranjit, D., Chandramohan, L., etal. (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4: e5822.
49. Molin, S., and Tolker-Nielsen, T. (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14: 255-261.
50. Moormeier, D.E., Endres, J.L., Mann, E.E., Sadykov, M.R., Horswill, A.R., Rice, K.C., etal. (2013) Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches. Appl Environ Microbiol 79: 3413-3424.
51. Nedelcu, A.M., Driscoll, W.W., Durand, P.M., Herron, M.D., and Rashidi, A. (2011) On the paradigm of altruistic suicide in the unicellular world. Evolution Int J Org Evolution 65: 3-20.
52. Oli, M.W., Otoo, H.N., Crowley, P.J., Heim, K.P., Nascimento, M.M., Ramsook, C.B., etal. (2012) Functional amyloid formation by Streptococcus mutans. Microbiology 158: 2903-2916.
53. Orberg, M.L., Schillen, K., and Nylander, T. (2007) Dynamic light scattering and fluorescence study of the interaction between double-stranded DNA and poly(amido amine) dendrimers. Biomacromolecules 8: 1557-1563.
54. Oshida, T., Sugai, M., Komatsuzawa, H., Hong, Y.M., Suginaka, H., and Tomasz, A. (1995) A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-beta-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization. Proc Natl Acad Sci USA 92: 285-289.
55. Otzen, D., and Nielsen, P.H. (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65: 910-927.
56. Patel, R. (2005) Biofilms and antimicrobial resistance. Clin Orthop Relat Res 437: 41-47.
57. Pavlovsky, L., Younger, J.G., and Solomon, M.J. (2013) Rheology of bacterial biofilms. Soft matter 9: 122-131.
58. Periasamy, S., Joo, H.-S., Duong, A.C., Bach, T.-H.L., Tan, V.Y., Chatterjee, S.S., etal. (2012) How Staphylococcus aureus biofilms develop their characteristic structure. PNAS 109: 1281-1286.
59. Pressler, T. (2008) Review of recombinant human deoxyribonuclease (rhDNase) in the management of patients with cystic fibrosis. Biol: Targets Ther 2: 611-617.
60. Rice, K.C., Mann, E.E., Endres, J.L., Weiss, E.C., Cassat, J.E., Smeltzer, M.S., and Bayles, K.W. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104: 8113-8118.
61. Rohde, H., Knobloch, J.K., Horstkotte, M.A., and Mack, D. (2001) Correlation of biofilm expression types of Staphylococcus epidermidis with polysaccharide intercellular adhesin synthesis: evidence for involvement of icaADBC genotype-independent factors. Med Microbiol Immunol (Berl) 190: 105-112.
62. Schwartz, K., and Boles, B.R. (2013) Microbial amyloids - functions and interactions within the host. Curr Opin Microbiol 16: 93-99.
63. Schwartz, K., Stephenson, R., Hernandez, M., Jambang, N., and Boles, B.R. (2010) The use of drip flow and rotating disk reactors for Staphylococcus aureus biofilm analysis. JoVE (46). pii: 2470.
64. Schwartz, K., Syed, A.K., Stephenson, R.E., Rickard, A.H., and Boles, B.R. (2012) Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog 8: e1002744.
65. Schwartz, K., Sekedat, M.D., Syed, A.K., O'Hara, B., Payne, D.E., Lamb, A., and Boles, B.R. (2014) The AgrD N-terminal leader peptide of Staphylococcus aureus has cytolytic and amyloidogenic properties. Infect Immun 82: 3837-3844.
66. Sharma-Kuinkel, B.K., Mann, E.E., Ahn, J.S., Kuechenmeister, L.J., Dunman, P.M., and Bayles, K.W. (2009) The Staphylococcus aureus LytSR two-component regulatory system affects biofilm formation. J Bacteriol 191: 4767-4775.
67. Shewmaker, F., McGlinchey, R.P., and Wickner, R.B. (2011) Structural insights into functional and pathological amyloid. J Biol Chem 286: 16533-16540.
68. Soreghan, B., Kosmoski, J., and Glabe, C. (1994) Surfactant properties of Alzheimer's A beta peptides and the mechanism of amyloid aggregation. J Biol Chem 269: 28551-28554.
69. Suram, A., Rao, K.S., Latha, K.S., and Viswamitra, M.A. (2002) First evidence to show the topological change of DNA from B-dNA to Z-DNA conformation in the hippocampus of Alzheimer's brain. Neuromolecular Med 2: 289-297.
70. Suram, A., Hegde, M.L., and Rao, K.S. (2007) A new evidence for DNA nicking property of amyloid beta-peptide (1-42): relevance to Alzheimer's disease. Arch Biochem Biophys 463: 245-252.
71. Thomas, V.C., and Hancock, L.E. (2009) Suicide and fratricide in bacterial biofilms. Int J Artif Organs 32: 537-544.
72. Tsompanidou, E., Sibbald, M.J., Chlebowicz, M.A., Dreisbach, A., Back, J.W., van Dijl, J.M., etal. (2011) Requirement of the agr locus for colony spreading of Staphylococcus aureus. J Bacteriol 193: 1267-1272.
73. Wang, R., Braughton, K.R., Kretschmer, D., Bach, T.H., Queck, S.Y., Li, M., etal. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510-1514.
74. Wang, R., Khan, B.A., Cheung, G.Y., Bach, T.H., Jameson-Lee, M., Kong, K.F., etal. (2011) Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J Clin Invest 121: 238-248.
75. Wang, S., Liu, X., Liu, H., Zhang, L., Guo, Y., Yu, S., etal. (2015) The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Reports 7: 330-340.
76. Wertheim, H.F., Melles, D.C., Vos, M.C., van Leeuwen, W., van Belkum, A., Verbrugh, H.A., and Nouwen, J.L. (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5: 751-762.
77. Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., and Mattick, J.S. (2002) Extracellular DNA required for bacterial biofilm formation. Science (New York, N.Y. 295: 1487.
78. Yu, H., Ren, J., and Qu, X. (2007) Time-dependent DNA condensation induced by amyloid beta-peptide. Biophys J 92: 185-191.
79. Zhou, B., Xing, L., Wu, W., Zhang, X.E., and Lin, Z. (2012) Small surfactant-like peptides can drive soluble proteins into active aggregates. Microb Cell Fact 11: 10.