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Antimicrobial Resistance in Biofilm Communities

  • Christine SedgleyEmail author
  • Gary Dunny
Chapter
  • 1.1k Downloads
Part of the Springer Series on Biofilms book series (BIOFILMS, volume 9)

Abstract

Biofilms are composed of microcolonies encased in an extracellular polymeric substance (EPS) matrix. Wide-ranging differences exist between the biofilm and planktonic states in growth, structure, behavior, and physiology, all of which can have profound effects on their susceptibility to antimicrobials. Other factors that can contribute to the decreased susceptibility of biofilm microorganisms to antimicrobial agents include provision of a physical barrier to antimicrobial agents by the EPS matrix, facilitation of horizontal gene transfer (HGT) of DNA trapped within the extracellular matrix, quorum sensing and stress responses resulting in the recruitment and expression of resistance determinants such as multidrug resistance efflux pumps, the presence of persister cells that survive antibiotic treatment, and metabolic heterogeneity throughout the biofilm resulting in slow growth and protection against antibiotics active on rapidly growing bacteria. While further work is needed to fully understand antimicrobial resistance in biofilm communities, including the multispecies biofilms found in root canal infections, the accumulative effects of various processes, rather than individual involvement, are likely to be important. It is clear that much remains to be learned about the critical events in the development of antimicrobial resistance in biofilm communities.

Keywords

Extracellular Polymeric Substance Horizontal Gene Transfer Root Canal Persister Cell Efflux Pump Inhibitor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Absalon C, Van Dellen K, Watnick PI (2011) A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS Pathog 7, e1002210PubMedCentralPubMedCrossRefGoogle Scholar
  2. Adam B, Baillie GS, Douglas LJ (2002) Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344–349Google Scholar
  3. Adnan M, Morton G, Singh J et al (2010) Contribution of rpoS and bolA genes in biofilm formation in Escherichia coli K-12 MG1655. Mol Cell Biochem 342:207–213Google Scholar
  4. Allegrucci M, Sauer K (2007) Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol 189:2030–2038PubMedCentralPubMedCrossRefGoogle Scholar
  5. Allesen-Holm M, Barken KB, Yang L et al (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128PubMedCrossRefGoogle Scholar
  6. Anderl JN, Franklin MJ, Stewart PS (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44:1818–1824PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bandara HM, Lam OL, Watt RM et al (2010) Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59:1225–1234Google Scholar
  8. Barnes AM, Ballering KS, Leibman RS et al (2012) Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. MBio 3:e00193–e00112PubMedCentralPubMedCrossRefGoogle Scholar
  9. Baugh S, Ekanayaka AS, Piddock LJ et al (2012) Loss of or inhibition of all multidrug resistance efflux pumps of Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J Antimicrob Chemother 67:2409–2417PubMedCrossRefGoogle Scholar
  10. Baumgartner JC, Xia T (2003) Antibiotic susceptibility of bacteria associated with endodontic abscesses. J Endod 29:44–47PubMedCrossRefGoogle Scholar
  11. Belitsky M, Avshalom H, Erental A et al (2011) The Escherichia coli extracellular death factor EDF induces the endoribonucleolytic activities of the toxins MazF and ChpBK. Mol Cell 41:625–635PubMedCrossRefGoogle Scholar
  12. Benitez JA, Spelbrink RG, Silva A et al (1997) Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infect Immun 65:3474–3477PubMedCentralPubMedGoogle Scholar
  13. Bhullar K, Waglechner N, Pawlowski A et al (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 7, e34953PubMedCentralPubMedCrossRefGoogle Scholar
  14. Boles BR, Thoendel M, Singh PK (2004) Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101:16630–16635PubMedCentralPubMedCrossRefGoogle Scholar
  15. Borriello G, Werner E, Roe F et al (2004) Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob Agents Chemother 48:2659–2664PubMedCentralPubMedCrossRefGoogle Scholar
  16. Burmolle M, Webb JS, Rao D et al (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923PubMedCentralPubMedCrossRefGoogle Scholar
  17. Carr GB, Schwartz RS, Schaudinn C et al (2009) Ultrastructural examination of failed molar retreatment with secondary apical periodontitis: an examination of endodontic biofilms in an endodontic retreatment failure. J Endod 35:1303–1309PubMedCrossRefGoogle Scholar
  18. Ceri H, Olson ME, Stremick C et al (1999) The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776PubMedCentralPubMedGoogle Scholar
  19. Chavez de Paz LE, Lemos JA, Wickstrom C et al (2012) Role of (p)ppGpp in biofilm formation by Enterococcus faecalis. Appl Environ Microbiol 78:1627–1630PubMedCentralPubMedCrossRefGoogle Scholar
  20. Chia N, Woese CR, Goldenfeld N (2008) A collective mechanism for phase variation in biofilms. Proc Natl Acad Sci USA 105:14597–14602PubMedCentralPubMedCrossRefGoogle Scholar
  21. Ciofu O (2003) Pseudomonas aeruginosa chromosomal beta-lactamase in patients with cystic fibrosis and chronic lung infection. Mechanism of antibiotic resistance and target of the humoral immune response. APMIS Suppl 116:1–47PubMedGoogle Scholar
  22. Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541–548PubMedCrossRefGoogle Scholar
  23. Claverys JP, Havarstein LS (2007) Cannibalism and fratricide: mechanisms and raisons d’etre. Nat Rev Microbiol 5:219–229PubMedCrossRefGoogle Scholar
  24. Claverys JP, Martin B, Havarstein LS (2007) Competence-induced fratricide in streptococci. Mol Microbiol 64:1423–1433PubMedCrossRefGoogle Scholar
  25. Clewell DB, Francia MV (2004) Conjugation in gram-positive bacteria. In: Funnell BE, Phillips GJ (eds) Plasmid biology. ASM Press, Washington, D.C., pp 227–256CrossRefGoogle Scholar
  26. Conlon KM, Humphreys H, O’Gara JP (2004) Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol 186:6208–6219PubMedCentralPubMedCrossRefGoogle Scholar
  27. Cook L, Chatterjee A, Barnes A et al (2011) Biofilm growth alters regulation of conjugation by a bacterial pheromone. Mol Microbiol 81:1499–1510PubMedCentralPubMedCrossRefGoogle Scholar
  28. Costerton JW, Irvin RT, Cheng KJ (1981) The bacterial glycocalyx in nature and disease. Annu Rev Microbiol 35:299–324PubMedCrossRefGoogle Scholar
  29. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322PubMedCrossRefGoogle Scholar
  30. Cotter PA, Stibitz S (2007) c-di-GMP-mediated regulation of virulence and biofilm formation. Curr Opin Microbiol 10:17–23PubMedCrossRefGoogle Scholar
  31. Cucarella C, Solano C, Valle J et al (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896PubMedCentralPubMedCrossRefGoogle Scholar
  32. Dahlen G, Magnusson BC, Moller A (1981) Histological and histochemical study of the influence of lipopolysaccharide extracted from Fusobacterium nucleatum on the periapical tissues in the monkey Macaca fascicularis. Arch Oral Biol 26:591–598PubMedCrossRefGoogle Scholar
  33. Dahlen G, Samuelsson W, Molander A et al (2000) Identification and antimicrobial susceptibility of enterococci isolated from the root canal. Oral Microbiol Immunol 15:309–312PubMedCrossRefGoogle Scholar
  34. Danese PN, Pratt LA, Kolter R (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182:3593–3596PubMedCentralPubMedCrossRefGoogle Scholar
  35. de Beer D, Stoodley P, Roe F et al (1994) Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43:1131–1138PubMedCrossRefGoogle Scholar
  36. de Sousa EL, Ferraz CC, Gomes BP et al (2003) Bacteriological study of root canals associated with periapical abscesses. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 96:332–339PubMedCrossRefGoogle Scholar
  37. Dieppois G, Ducret V, Caille O et al (2012) The transcriptional regulator CzcR modulates antibiotic resistance and quorum sensing in Pseudomonas aeruginosa. PLoS ONE 7, e38148PubMedCentralPubMedCrossRefGoogle Scholar
  38. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193PubMedCentralPubMedCrossRefGoogle Scholar
  39. Dorr T, Lewis K, Vulic M (2009) SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet 5, e1000760PubMedCentralPubMedCrossRefGoogle Scholar
  40. Dorr T, Vulic M, Lewis K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8, e1000317PubMedCentralPubMedCrossRefGoogle Scholar
  41. Drenkard E, Ausubel FM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740–743PubMedCrossRefGoogle Scholar
  42. Duan K, Dammel C, Stein J et al (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50:1477–1491PubMedCrossRefGoogle Scholar
  43. Dunny GM, Brown BL, Clewell DB (1978) Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc Natl Acad Sci USA 75:3479–3483PubMedCentralPubMedCrossRefGoogle Scholar
  44. Dunny GM, Craig RA, Carron RL et al (1979) Plasmid transfer in Streptococcus faecalis: production of multiple sex pheromones by recipients. Plasmid 2:454–465PubMedCrossRefGoogle Scholar
  45. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990–1004PubMedCrossRefGoogle Scholar
  46. Fauvart M, De Groote VN, Michiels J (2011) Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60:699–709PubMedCrossRefGoogle Scholar
  47. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633PubMedGoogle Scholar
  48. Foster PL (2007) Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 42:373–397PubMedCentralPubMedCrossRefGoogle Scholar
  49. Fuqua C, Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695PubMedCrossRefGoogle Scholar
  50. Fux CA, Costerton JW, Stewart PS et al (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34–40PubMedCrossRefGoogle Scholar
  51. Gefen O, Balaban NQ (2009) The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol Rev 33:704–717PubMedCrossRefGoogle Scholar
  52. Gomes BP, Jacinto RC, Montagner F et al (2011) Analysis of the antimicrobial susceptibility of anaerobic bacteria isolated from endodontic infections in Brazil during a period of nine years. J Endod 37:1058–1062PubMedCrossRefGoogle Scholar
  53. Guisbert E, Yura T, Rhodius VA et al (2008) Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol Mol Biol Rev 72:545–554PubMedCentralPubMedCrossRefGoogle Scholar
  54. Hausner M, Wuertz S (1999) High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl Environ Microbiol 65:3710–3713PubMedCentralPubMedGoogle Scholar
  55. Havarstein LS, Martin B, Johnsborg O et al (2006) New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol Microbiol 59:1297–1307PubMedCrossRefGoogle Scholar
  56. Hayes F, Van Melderen L (2011) Toxins-antitoxins: diversity, evolution and function. Crit Rev Biochem Mol Biol 46:386–408PubMedCrossRefGoogle Scholar
  57. Henderson IR, Owen P, Nataro JP (1999) Molecular switches–the ON and OFF of bacterial phase variation. Mol Microbiol 33:919–932PubMedCrossRefGoogle Scholar
  58. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395PubMedCentralPubMedCrossRefGoogle Scholar
  59. Hentzer M, Wu H, Andersen JB et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. Embo J 22:3803–3815PubMedCentralPubMedCrossRefGoogle Scholar
  60. Hoiby N, Bjarnsholt T, Givskov M et al (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332PubMedCrossRefGoogle Scholar
  61. Houry A, Gohar M, Deschamps J et al (2012) Bacterial swimmers that infiltrate and take over the biofilm matrix. Proc Natl Acad Sci USA 109:13088–13093PubMedCentralPubMedCrossRefGoogle Scholar
  62. Islam S, Oh H, Jalal S et al (2009) Chromosomal mechanisms of aminoglycoside resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Clin Microbiol Infect 15:60–66PubMedCrossRefGoogle Scholar
  63. Iwahara K, Kuriyama T, Shimura S et al (2006) Detection of cfxA and cfxA2, the beta-lactamase genes of Prevotella spp., in clinical samples from dentoalveolar infection by real-time PCR. J Clin Microbiol 44:172–176PubMedCentralPubMedCrossRefGoogle Scholar
  64. Izano EA, Amarante MA, Kher WB et al (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74:470–476PubMedCentralPubMedCrossRefGoogle Scholar
  65. Jacinto RC, Gomes BP, Ferraz CC et al (2003) Microbiological analysis of infected root canals from symptomatic and asymptomatic teeth with periapical periodontitis and the antimicrobial susceptibility of some isolated anaerobic bacteria. Oral Microbiol Immunol 18:285–292PubMedCrossRefGoogle Scholar
  66. Jacinto RC, Gomes BP, Shah HN et al (2006) Incidence and antimicrobial susceptibility of Porphyromonas gingivalis isolated from mixed endodontic infections. Int Endod J 39:62–70PubMedCrossRefGoogle Scholar
  67. Jacinto RC, Montagner F, Signoretti FG et al (2008) Frequency, microbial interactions, and antimicrobial susceptibility of Fusobacterium nucleatum and Fusobacterium necrophorum isolated from primary endodontic infections. J Endod 34:1451–1456PubMedCrossRefGoogle Scholar
  68. Jalal S, Ciofu O, Hoiby N et al (2000) Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother 44:710–712PubMedCentralPubMedCrossRefGoogle Scholar
  69. Johnson EM, Flannagan SE, Sedgley CM (2006) Coaggregation interactions between oral and endodontic Enterococcus faecalis and bacterial species isolated from persistent apical periodontitis. J Endod 32:946–950PubMedCrossRefGoogle Scholar
  70. Jungermann GB, Burns K, Nandakumar R et al (2011) Antibiotic resistance in primary and persistent endodontic infections. J Endod 37:1337–1344PubMedCentralPubMedCrossRefGoogle Scholar
  71. Kara D, Luppens SB, Cate JM (2006) Differences between single- and dual-species biofilms of Streptococcus mutans and Veillonella parvula in growth, acidogenicity and susceptibility to chlorhexidine. Eur J Oral Sci 114:58–63PubMedCrossRefGoogle Scholar
  72. Kara D, Luppens SB, van Marle J et al (2007) Microstructural differences between single-species and dual-species biofilms of Streptococcus mutans and Veillonella parvula, before and after exposure to chlorhexidine. FEMS Microbiol Lett 271:90–97PubMedCrossRefGoogle Scholar
  73. Keller L, Surette MG (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4:249–258PubMedCrossRefGoogle Scholar
  74. Kelley WL (2006) Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol 62:1228–1238PubMedCrossRefGoogle Scholar
  75. Keren I, Kaldalu N, Spoering A et al (2004a) Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230:13–18PubMedCrossRefGoogle Scholar
  76. Keren I, Shah D, Spoering A et al (2004b) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172–8180PubMedCentralPubMedCrossRefGoogle Scholar
  77. Khemaleelakul S, Baumgartner JC, Pruksakorn S (2002) Identification of bacteria in acute endodontic infections and their antimicrobial susceptibility. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94:746–755PubMedCrossRefGoogle Scholar
  78. Khemaleelakul S, Baumgartner JC, Pruksakom S (2006) Autoaggregation and coaggregation of bacteria associated with acute endodontic infections. J Endod 32:312–318PubMedCrossRefGoogle Scholar
  79. Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379:324–329PubMedCrossRefGoogle Scholar
  80. Kim Y, Wang X, Zhang XS et al (2010) Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD. Environ Microbiol 12:1105–1121PubMedCentralPubMedCrossRefGoogle Scholar
  81. Kirisits MJ, Prost L, Starkey M et al (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821PubMedCentralPubMedCrossRefGoogle Scholar
  82. Kobayashi K, Iwano M (2012) BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85:51–66PubMedCrossRefGoogle Scholar
  83. Kolenbrander PE, Palmer RJ Jr, Periasamy S et al (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8:471–480PubMedCrossRefGoogle Scholar
  84. Konig C, Schwank S, Blaser J (2001) Factors compromising antibiotic activity against biofilms of Staphylococcus epidermidis. Eur J Clin Microbiol Infect Dis 20:20–26PubMedCrossRefGoogle Scholar
  85. Korch SB, Henderson TA, Hill TM (2003) Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol Microbiol 50:1199–1213PubMedCrossRefGoogle Scholar
  86. Kvist M, Hancock V, Klemm P (2008) Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Environ Microbiol 74:7376–7382PubMedCentralPubMedCrossRefGoogle Scholar
  87. Lafleur MD, Qi Q, Lewis K (2010) Patients with long-term oral carriage harbor high-persister mutants of Candida albicans. Antimicrob Agents Chemother 54:39–44PubMedCentralPubMedCrossRefGoogle Scholar
  88. Lawrence JR, Korber DR, Hoyle BD et al (1991) Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567PubMedCentralPubMedGoogle Scholar
  89. Le Goff A, Bunetel L, Mouton C et al (1997) Evaluation of root canal bacteria and their antimicrobial susceptibility in teeth with necrotic pulp. Oral Microbiol Immunol 12:318–322PubMedCrossRefGoogle Scholar
  90. Leriche V, Briandet R, Carpentier B (2003) Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: spatial distribution of bacterial species suggests a protective effect of one species to another. Environ Microbiol 5:64–71PubMedCrossRefGoogle Scholar
  91. Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56PubMedCrossRefGoogle Scholar
  92. Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372PubMedCrossRefGoogle Scholar
  93. Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals. Protein Sci 21(10):1403–1417PubMedCentralPubMedCrossRefGoogle Scholar
  94. Li XZ, Nikaido H (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555–1623PubMedCentralPubMedCrossRefGoogle Scholar
  95. Li YH, Hanna MN, Svensater G et al (2001a) Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J Bacteriol 183:6875–6884PubMedCentralPubMedCrossRefGoogle Scholar
  96. Li YH, Lau PC, Lee JH et al (2001b) Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897–908PubMedCentralPubMedCrossRefGoogle Scholar
  97. Li YH, Tang N, Aspiras MB et al (2002) A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699–2708PubMedCentralPubMedCrossRefGoogle Scholar
  98. Li L, Hsiao WW, Nandakumar R et al (2010) Analyzing endodontic infections by deep coverage pyrosequencing. J Dent Res 89:980–984PubMedCentralPubMedCrossRefGoogle Scholar
  99. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602PubMedCentralPubMedGoogle Scholar
  100. Love RM, Jenkinson HF (2002) Invasion of dentinal tubules by oral bacteria. Crit Rev Oral Biol Med 13:171–183PubMedCrossRefGoogle Scholar
  101. Love RM, McMillan MD, Park Y et al (2000) Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin. Infect Immun 68:1359–1365PubMedCentralPubMedCrossRefGoogle Scholar
  102. Luppens SB, Kara D, Bandounas L et al (2008) Effect of Veillonella parvula on the antimicrobial resistance and gene expression of Streptococcus mutans grown in a dual-species biofilm. Oral Microbiol Immunol 23:183–189PubMedCrossRefGoogle Scholar
  103. Lynch DJ, Fountain TL, Mazurkiewicz JE et al (2007) Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett 268:158–165PubMedCentralPubMedCrossRefGoogle Scholar
  104. Ma L, Conover M, Lu H et al (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5, e1000354PubMedCentralPubMedCrossRefGoogle Scholar
  105. Mah TF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39PubMedCrossRefGoogle Scholar
  106. Mah TF, Pitts B, Pellock B et al (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310PubMedCrossRefGoogle Scholar
  107. Mandsberg LF, Ciofu O, Kirkby N et al (2009) Antibiotic resistance in Pseudomonas aeruginosa strains with increased mutation frequency due to inactivation of the DNA oxidative repair system. Antimicrob Agents Chemother 53:2483–2491PubMedCentralPubMedCrossRefGoogle Scholar
  108. Matsumura K, Furukawa S, Ogihara H et al (2011) Roles of multidrug efflux pumps on the biofilm formation of Escherichia coli K-12. Biocontrol Sci 16:69–72PubMedCrossRefGoogle Scholar
  109. May T, Ito A, Okabe S (2009) Induction of multidrug resistance mechanism in Escherichia coli biofilms by interplay between tetracycline and ampicillin resistance genes. Antimicrob Agents Chemother 53:4628–4639PubMedCentralPubMedCrossRefGoogle Scholar
  110. McDougald D, Rice SA, Barraud N et al (2012) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10:39–50Google Scholar
  111. Molin S, Tolker-Nielsen T (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261PubMedCrossRefGoogle Scholar
  112. Moyed HS, Bertrand KP (1983) hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 155:768–775PubMedCentralPubMedGoogle Scholar
  113. Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4, e1000213PubMedCentralPubMedCrossRefGoogle Scholar
  114. Mulcahy LR, Burns JL, Lory S et al (2010) Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol 192:6191–6199PubMedCentralPubMedCrossRefGoogle Scholar
  115. Oliver A, Baquero F, Blazquez J (2002) The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol Microbiol 43:1641–1650PubMedCrossRefGoogle Scholar
  116. Ozok AR, Persoon IF, Huse SM et al (2012) Ecology of the microbiome of the infected root canal system: a comparison between apical and coronal root segments. Int Endod J 45:530–541PubMedCrossRefGoogle Scholar
  117. Parsek MR, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33PubMedCrossRefGoogle Scholar
  118. Pinheiro ET, Gomes BP, Ferraz CC et al (2003) Evaluation of root canal microorganisms isolated from teeth with endodontic failure and their antimicrobial susceptibility. Oral Microbiol Immunol 18:100–103PubMedCrossRefGoogle Scholar
  119. Pinheiro ET, Gomes BP, Drucker DB et al (2004) Antimicrobial susceptibility of Enterococcus faecalis isolated from canals of root filled teeth with periapical lesions. Int Endod J 37:756–763PubMedCrossRefGoogle Scholar
  120. Poole K (2012) Bacterial stress responses as determinants of antimicrobial resistance. J Antimicrob Chemother 67(9):2069–2089PubMedCrossRefGoogle Scholar
  121. Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51PubMedCrossRefGoogle Scholar
  122. Qin Z, Ou Y, Yang L et al (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–2092PubMedCrossRefGoogle Scholar
  123. Rachid S, Ohlsen K, Witte W et al (2000) Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 44:3357–3363PubMedCentralPubMedCrossRefGoogle Scholar
  124. Rendueles O, Ghigo JM (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36(5):972–989PubMedCrossRefGoogle Scholar
  125. Rendueles O, Travier L, Latour-Lambert P et al (2011) Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. MBio 2:e00043–e00011PubMedCentralPubMedCrossRefGoogle Scholar
  126. Rendueles O, Kaplan JB, Ghigo JM (2012) Antibiofilm polysaccharides. Environ Microbiol 15(2):334–346PubMedCentralPubMedCrossRefGoogle Scholar
  127. Reynaud Af Geijersstam A, Culak R, Molenaar L et al (2007) Comparative analysis of virulence determinants and mass spectral profiles of Finnish and Lithuanian endodontic Enterococcus faecalis isolates. Oral Microbiol Immunol 22:87–94PubMedCrossRefGoogle Scholar
  128. Rice LB (1998) Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 42:1871–1877PubMedCentralPubMedGoogle Scholar
  129. Ricucci D, Siqueira JF Jr (2010) Biofilms and apical periodontitis: study of prevalence and association with clinical and histopathologic findings. J Endod 36:1277–1288PubMedCrossRefGoogle Scholar
  130. Ricucci D, Siqueira JF Jr, Bate AL et al (2009) Histologic investigation of root canal-treated teeth with apical periodontitis: a retrospective study from twenty-four patients. J Endod 35:493–502PubMedCrossRefGoogle Scholar
  131. Roberts AP, Mullany P (2010) Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti Infect Ther 8:1441–1450PubMedCrossRefGoogle Scholar
  132. Rossi-Fedele G, Scott W, Spratt D et al (2006) Incidence and behaviour of Tn916-like elements within tetracycline-resistant bacteria isolated from root canals. Oral Microbiol Immunol 21:218–222PubMedCrossRefGoogle Scholar
  133. Salyers AA, Shoemaker NB, Stevens AM et al (1995) Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol Rev 59:579–590PubMedCentralPubMedGoogle Scholar
  134. Sauer K, Camper AK, Ehrlich GD et al (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154PubMedCentralPubMedCrossRefGoogle Scholar
  135. Sauer K, Cullen MC, Rickard AH et al (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326PubMedCentralPubMedCrossRefGoogle Scholar
  136. Schembri MA, Kjaergaard K, Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267PubMedCrossRefGoogle Scholar
  137. Sedgley CM, Molander A, Flannagan SE et al (2005) Virulence, phenotype and genotype characteristics of endodontic Enterococcus spp. Oral Microbiol Immunol 20:10–19PubMedCrossRefGoogle Scholar
  138. Sedgley CM, Lee EH, Martin MJ et al (2008) Antibiotic resistance gene transfer between Streptococcus gordonii and Enterococcus faecalis in root canals of teeth ex vivo. J Endod 34:570–574PubMedCrossRefGoogle Scholar
  139. Shah D, Zhang Z, Khodursky A et al (2006) Persisters: a distinct physiological state of E. coli. BMC Microbiol 6:53PubMedCentralPubMedCrossRefGoogle Scholar
  140. Siqueira JF Jr, Rocas IN (2005) Uncultivated phylotypes and newly named species associated with primary and persistent endodontic infections. J Clin Microbiol 43:3314–3319PubMedCentralPubMedCrossRefGoogle Scholar
  141. Siqueira JF Jr, Rocas IN, Ricucci D (2010) Biofilms in endodontic infections. Endod Topics 22:33–49CrossRefGoogle Scholar
  142. Siqueira JF Jr, Alves FR, Rocas IN (2011) Pyrosequencing analysis of the apical root canal microbiota. J Endod 37:1499–1503PubMedCrossRefGoogle Scholar
  143. Skillman LC, Sutherland IW, Jones MV (1998) The role of exopolysaccharides in dual species biofilm development. J Appl Microbiol 85(Suppl 1):13S–18SPubMedCrossRefGoogle Scholar
  144. Skucaite N, Peciuliene V, Vitkauskiene A et al (2010) Susceptibility of endodontic pathogens to antibiotics in patients with symptomatic apical periodontitis. J Endod 36:1611–1616PubMedCrossRefGoogle Scholar
  145. Sorensen SJ, Bailey M, Hansen LH et al (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3:700–710PubMedCrossRefGoogle Scholar
  146. Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746–6751PubMedCentralPubMedCrossRefGoogle Scholar
  147. Srivastava D, Waters CM (2012) A tangled web: regulatory connections between quorum sensing and cyclic Di-GMP. J Bacteriol 194:4485–4493PubMedCentralPubMedCrossRefGoogle Scholar
  148. Staal M, Borisov SM, Rickelt LF et al (2011) Ultrabright planar optodes for luminescence life-time based microscopic imaging of O2 dynamics in biofilms. J Microbiol Methods 85:67–74PubMedCrossRefGoogle Scholar
  149. Stanley NR, Britton RA, Grossman AD et al (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951–1957PubMedCentralPubMedCrossRefGoogle Scholar
  150. Sternberg C, Christensen BB, Johansen T et al (1999) Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol 65:4108–4117PubMedCentralPubMedGoogle Scholar
  151. Stewart PS (2012) Mini-review: convection around biofilms. Biofouling 28:187–198PubMedCrossRefGoogle Scholar
  152. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138PubMedCrossRefGoogle Scholar
  153. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210PubMedCrossRefGoogle Scholar
  154. Suci PA, Mittelman MW, Yu FP et al (1994) Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 38:2125–2133PubMedCentralPubMedCrossRefGoogle Scholar
  155. Sutherland I (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9PubMedCrossRefGoogle Scholar
  156. Thomas VC, Thurlow LR, Boyle D et al (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190:5690–5698PubMedCentralPubMedCrossRefGoogle Scholar
  157. Thomas VC, Hiromasa Y, Harms N et al (2009) A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol Microbiol 72:1022–1036PubMedCentralPubMedCrossRefGoogle Scholar
  158. Tielker D, Hacker S, Loris R et al (2005) Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology 151:1313–1323PubMedCrossRefGoogle Scholar
  159. Tormo MA, Ubeda C, Marti M et al (2007) Phase-variable expression of the biofilm-associated protein (Bap) in Staphylococcus aureus. Microbiology 153:1702–1710PubMedCrossRefGoogle Scholar
  160. Trotonda MP, Manna AC, Cheung AL et al (2005) SarA positively controls bap-dependent biofilm formation in Staphylococcus aureus. J Bacteriol 187:5790–5798PubMedCentralPubMedCrossRefGoogle Scholar
  161. Upadya M, Shrestha A, Kishen A (2011) Role of efflux pump inhibitors on the antibiofilm efficacy of calcium hydroxide, chitosan nanoparticles, and light-activated disinfection. J Endod 37:1422–1426PubMedCrossRefGoogle Scholar
  162. Valle J, Vergara-Irigaray M, Merino N et al (2007) sigmaB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. J Bacteriol 189:2886–2896PubMedCentralPubMedCrossRefGoogle Scholar
  163. Vigil GV, Wayman BE, Dazey SE et al (1997) Identification and antibiotic sensitivity of bacteria isolated from periapical lesions. J Endod 23:110–114PubMedCrossRefGoogle Scholar
  164. Vrany JD, Stewart PS, Suci PA (1997) Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa bofilms displaying rapid-transport characteristics. Antimicrob Agents Chemother 41:1352–1358PubMedCentralPubMedGoogle Scholar
  165. Vuong C, Voyich JM, Fischer ER et al (2004) Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6:269–275PubMedCrossRefGoogle Scholar
  166. Walters MC 3rd, Roe F, Bugnicourt A et al (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47:317–323PubMedCentralPubMedCrossRefGoogle Scholar
  167. Wang X, Wood TK (2011) Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl Environ Microbiol 77:5577–5583PubMedCentralPubMedCrossRefGoogle Scholar
  168. Wang X, Kim Y, Hong SH et al (2011) Antitoxin MqsA helps mediate the bacterial general stress response. Nat Chem Biol 7:359–366PubMedCentralPubMedCrossRefGoogle Scholar
  169. Werner E, Roe F, Bugnicourt A et al (2004) Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70:6188–6196PubMedCentralPubMedCrossRefGoogle Scholar
  170. Whitchurch CB, Tolker-Nielsen T, Ragas PC et al (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487PubMedCrossRefGoogle Scholar
  171. Whiteley M, Bangera MG, Bumgarner RE et al (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864PubMedCrossRefGoogle Scholar
  172. Wiuff C, Zappala RM, Regoes RR et al (2005) Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob Agents Chemother 49:1483–1494PubMedCentralPubMedCrossRefGoogle Scholar
  173. Wu Y, Vulic M, Keren I et al (2012) Role of oxidative stress in persister tolerance. Antimicrob Agents Chemother 56(9):4922–4926PubMedCentralPubMedCrossRefGoogle Scholar
  174. Zahller J, Stewart PS (2002) Transmission electron microscopic study of antibiotic action on Klebsiella pneumoniae biofilm. Antimicrob Agents Chemother 46:2679–2683PubMedCentralPubMedCrossRefGoogle Scholar
  175. Zhang L, Mah TF (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190:4447–4452PubMedCentralPubMedCrossRefGoogle Scholar
  176. Zhang XQ, Bishop PL, Kupferle MJ (1998) Measurement of polysaccharides and proteins in biofilm extracellular polymers. Water Sci Technol 37:345–348CrossRefGoogle Scholar
  177. Zheng Z, Stewart PS (2002) Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 46:900–903PubMedCentralPubMedCrossRefGoogle Scholar
  178. Zhu X, Wang Q, Zhang C et al (2010) Prevalence, phenotype, and genotype of Enterococcus faecalis isolated from saliva and root canals in patients with persistent apical periodontitis. J Endod 36:1950–1955PubMedCrossRefGoogle Scholar
  179. Ziebuhr W, Krimmer V, Rachid S et al (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32:345–356PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of EndodontologySchool of Dentistry, Oregon Health & Science UniversityPortlandUSA
  2. 2.Department of MicrobiologyUniversity of MinnesotaMinneapolisUSA

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