Pathogens protection against the action of disinfectants in multispecies biofilms

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Sanchez Vizuete, P ^a   Orgaz, B ^b   Aymerich, S ^a   Le Coq, D ^a,c   Briandet, R ^a  

^a UMR1319 MICALIS   (France)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c CNRS   (France)

Author keywords

Bacterial pathogens; Disinfectants; Interspecies interactions; Multispecies biofilm; Protection

Indexed keywords

AMYLOID; CHLORINE; DISINFECTANT AGENT; HYDROLASE;

ARTICLE; AUTORADIOGRAPHY; BACILLUS CEREUS; BACILLUS SUBTILIS; BIOFILM; CONFOCAL LASER MICROSCOPY; DRUG TOLERANCE; ENTEROBACTER CLOACAE; ENTEROCOCCUS FAECALIS; FLUORESCENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC VARIABILITY; HAEMOPHILUS INFLUENZAE; HORIZONTAL GENE TRANSFER; INTERSPECIFIC RELATIONSHIP; LACTOBACILLUS PLANTARUM; LISTERIA MONOCYTOGENES; MASS SPECTROMETRY; MICROBIAL COMMUNITY; MORAXELLA CATARRHALIS; NONHUMAN; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; QUORUM SENSING; RAMAN SPECTROMETRY; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SPATIAL BEHAVIOR; VEILLONELLA PARVULA;

BACTERIA (MICROORGANISMS);

EID: 84937127269     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00705     Document Type: Article

References (177)

1. Abdallah, M., Benoliel, C., Drider, D., Dhulster, P., and Chihib, N.-E. (2014). Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch. Microbiol. 196, 453-72. doi:10.1007/s00203-014-0983-1.
2. Adam, B., Baillie, G. S., and Douglas, L. J. (2002). Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J. Med. Microbiol. 51, 344-9.
3. Al-Bakri, A. G., Gilbert, P., and Allison, D. G. (2005). Influence of gentamicin and tobramycin on binary biofilm formation by co-cultures of Burkholderia cepacia and Pseudomonas aeruginosa. J. Basic Microbiol. 45, 392-396. doi:10.1002/jobm.200510011.
4. Almeida, C., Azevedo, N. F., Iversen, C., Fanning, S., Keevil, C. W., and Vieira, M. J. (2009). Development and application of a novel peptide nucleic acid probe for the specific detection of Cronobacter genomospecies (Enterobacter sakazakii) in powdered infant formula. Appl. Environ. Microbiol. 75, 2925-30. doi:10.1128/AEM.02470-08.
5. Almeida, C., Azevedo, N. F., Santos, S., Keevil, C. W., and Vieira, M. J. (2011). Discriminating multi-species populations in biofilms with peptide nucleic acid fluorescence in situ hybridization (PNA FISH). PLoS One 6, e14786. doi:10.1371/journal.pone.0014786.
6. Almstrand, R., Daims, H., Persson, F., Sörensson, F., and Hermansson, M. (2013). New methods for analysis of spatial distribution and coaggregation of microbial populations in complex biofilms. Appl. Environ. Microbiol. 79, 5978-87. doi:10.1128/AEM.01727-13.
7. Alvarez, G., González, M., Isabal, S., Blanc, V., and León, R. (2013). Method to quantify live and dead cells in multi-species oral biofilm by real-time PCR with propidium monoazide. AMB Express 3, 1. doi:10.1186/2191-0855-3-1.
8. Amann, R., and Fuchs, B. M. (2008). Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat. Rev. Microbiol. 6, 339-48. doi:10.1038/nrmicro1888.
9. Andersson, S., Dalhammar, G., and Kuttuva Rajarao, G. (2011). Influence of microbial interactions and EPS/polysaccharide composition on nutrient removal activity in biofilms formed by strains found in wastewater treatment systems. Microbiol. Res. 166, 449-57. doi:10.1016/j.micres.2010.08.005.
10. Antonova, E. S., and Hammer, B. K. (2011). Quorum-sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae. FEMS Microbiol. Lett. 322, 68-76. doi:10.1111/j.1574- 6968.2011.02328.x.
11. Armbruster, C. E., Hong, W., Pang, B., Weimer, K. E. D., Juneau, R. A., Turner, J., and Swords, W. E. (2010). Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio 1. doi:10.1128/mBio.00102-10
12. Baffone, W., Sorgente, G., Campana, R., Patrone, V., Sisti, D., and Falcioni, T. (2011). Comparative effect of chlorhexidine and some mouthrinses on bacterial biofilm formation on titanium surface. Curr. Microbiol. 62, 445-51. doi:10.1007/s00284-010- 9727-x.
13. Barlow, M. (2009). What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol. Biol. 532, 397-411. doi:10.1007/978-1-60327-853-9_23.
14. Baudart, J., Olaizola, A., Coallier, J., Gauthier, V., and Laurent, P. (2005). Assessment of a new technique combining a viability test, whole-cell hybridization and laser-scanning cytometry for the direct counting of viable Enterobacteriaceae cells in drinking water. FEMS Microbiol. Lett. 243, 405-9. doi:10.1016/j.femsle.2005.01.001.
15. Bauer, W. D., and Robinson, J. B. (2002). Disruption of bacterial quorum sensing by other organisms. Curr. Opin. Biotechnol. 13, 234-7.
16. Behnke, S., Parker, A. E., Woodall, D., and Camper, A. K. (2011). Comparing the chlorine disinfection of detached biofilm clusters with those of sessile biofilms and planktonic cells in single- and dual-species cultures. Appl. Environ. Microbiol. 77, 7176-84. doi:10.1128/AEM.05514-11.
17. Bhargava, N., Sharma, P., and Capalash, N. (2014). Pyocyanin stimulates quorum sensing mediated tolerance to oxidative stress and increases persister cell populations in Acinetobacter baumannii. Infect. Immun. 82, 3417-25. doi:10.1128/IAI.01600-14.
18. Blanco, L. P., Evans, M. L., Smith, D. R., Badtke, M. P., and Chapman, M. R. (2012). Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 20, 66-73. doi:10.1016/j.tim.2011.11.005.
19. Boles, B. R., Thoendel, M., and Singh, P. K. (2004). Self-generated diversity produces "insurance effects" in biofilm communities. Proc. Natl. Acad. Sci. U. S. A. 101, 16630-5. doi:10.1073/pnas.0407460101.
20. Bourion, F., and Cerf, O. (1996). Disinfection efficacy against pure-culture and mixed populations biofilms of Listeria innocua and Pseudomonas aeruginosa on stainless steel, Teflon and rubber. Sci. Aliments 16, 151-166.
21. Branda, S. S., Vik, S., Friedman, L., and Kolter, R. (2005). Biofilms: the matrix revisited. Trends Microbiol. 13, 20-6. doi:10.1016/j.tim.2004.11.006.
22. Bredenbruch, F., Geffers, R., Nimtz, M., Buer, J., and Häussler, S. (2006). The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ. Microbiol. 8, 1318-29. doi:10.1111/j.1462-2920.2006.01025.x.
23. Bridier, A., Briandet, R., Bouchez, T., and Jabot, F. (2014). A model-based approach to detect interspecific interactions during biofilm development. Biofouling 30, 761-71. doi:10.1080/08927014.2014.923409.
24. Bridier, A., Briandet, R., Thomas, V., and Dubois-Brissonnet, F. (2011a). Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27, 1017-32. doi:10.1080/08927014.2011.626899.
25. Bridier, A., Dubois-Brissonnet, F., Boubetra, A., Thomas, V., and Briandet, R. (2010). The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J. Microbiol. Methods 82, 64-70. doi:10.1016/j.mimet.2010.04.006.
26. Bridier, A., Dubois-Brissonnet, F., Greub, G., Thomas, V., and Briandet, R. (2011b). Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 55, 2648-54. doi:10.1128/AAC.01760-10.
27. Bridier, A., Sanchez-Vizuete, M. del P., Le Coq, D., Aymerich, S., Meylheuc, T., Maillard, J. Y., Thomas, V., Dubois-Brissonnet, F., and Briandet, R. (2012). Biofilms of a Bacillus subtilis Hospital Isolate Protect Staphylococcus aureus from Biocide Action. PLoS One 7, e44506. doi:10.1371/journal.pone.0044506.
28. Bridier, A., Sanchez-Vizuete, P., Guilbaud, M., Piard, J.-C., Naïtali, M., and Briandet, R. (2015). Biofilm-associated persistence of food-borne pathogens. Food Microbiol. In press. doi:10.1016/j.fm.2014.04.015.
29. Burmølle, M., Kjøller, A. H., and Sørensen, S. J. (2012). "An invisible workforce: biofilms in the soil.," in Microbial biofilms: current research and applications, eds. G. Lear and D. L. Gillian (Caister Academic Press), 61.71.
30. Burmølle, M., Webb, J. S., Rao, D., Hansen, L. H., Sørensen, S. J., and Kjelleberg, S. (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, 3916-3923. doi:10.1128/AEM.03022-05.
31. Cantón, R., and Morosini, M.-I. (2011). Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiol. Rev. 35, 977-91. doi:10.1111/j.1574- 6976.2011.00295.x.
32. Ceri, H., Olson, M. E., Stremick, C., Read, R. R., Morck, D., and Buret, A. (1999). The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37, 1771-6.
33. Cerqueira, L., Azevedo, N. F., Almeida, C., Jardim, T., Keevil, C. W., and Vieira, M. J. (2008). DNA mimics for the rapid identification of microorganisms by fluorescence in situ hybridization (FISH). Int. J. Mol. Sci. 9, 1944-60. doi:10.3390/ijms9101944.
34. Chalmers, N. I., Palmer, R. J., Cisar, J. O., and Kolenbrander, P. E. (2008). Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J. Bacteriol. 190, 8145-54. doi:10.1128/JB.00983-08.
35. Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Hammar, M., Normark, S., and Hultgren, S. J. (2008). Role of Escherichia coli Curli Operons in Directing Amyloid Fiber Formation. Science 295, 851-855. doi:10.1126/science.1067484.Role.
36. Chaves Simões, L., Simões, M., and JoãoVieira, M. (2010). Influence of the diversity of bacterial isolates from drinking water on resistance of biofilms to disinfection. Appl. Environ. Microbiol. 76, 6673-9. doi:10.1128/AEM.00872-10.
37. Chen, F., Gao, Y., Chen, X., Yu, Z., and Li, X. (2013). Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection. Int. J. Mol. Sci. 14, 17477-500. doi:10.3390/ijms140917477.
38. Chorianopoulos, N. G., Giaouris, E. D., Skandamis, P. N., Haroutounian, S. a, and Nychas, G.-J. E. (2008). Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J. Appl. Microbiol. 104, 1586-96. doi:10.1111/j.1365-2672.2007.03694.x.
39. Christensen, B. B., Sternberg, C., Andersen, J. B., Eberl, L., Moller, S., Givskov, M., and Molin, S. (1998). Establishment of new genetic traits in a microbial biofilm community. Appl. Environ. Microbiol. 64, 2247-55
40. Ciandrini, E., Campana, R., Federici, S., Manti, A., Battistelli, M., Falcieri, E., Papa, S., and Baffone, W. (2014). In vitro activity of Carvacrol against titanium-adherent oral biofilms and planktonic cultures. Clin. Oral Investig. doi:10.1007/s00784-013-1179-9.
41. Combrouse, T., Sadovskaya, I., Faille, C., Kol, O., Gu??rardel, Y., and Midelet-Bourdin, G. (2013). Quantification of the extracellular matrix of the Listeria monocytogenes biofilms of different phylogenic lineages with optimization of culture conditions. J. Appl. Microbiol. 114, 1120-1131. doi:10.1111/jam.12127.
42. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H. M. (1995). Microbial biofilms. Annu. Rev. Microbiol. 49, 711-45. doi:10.1146/annurev.mi.49.100195.003431.
43. Davin-Regli, A., and Pagès, J. M. (2012). Cross-resistance between biocides and antimicrobials: an emerging question. Rev. Sci. Tech. 31, 89-104.
44. Dige, I., Nyengaard, J. R., Kilian, M., and Nyvad, B. (2009). Application of stereological principles for quantification of bacteria in intact dental biofilms. Oral Microbiol. Immunol. 24, 69-75. doi:10.1111/j.1399-302X.2008.00482.x.
45. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and Zhang, L. H. (2001). Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813-7. doi:10.1038/35081101.
46. Dueholm, M. S., Søndergaard, M. T., Nilsson, M., Christiansen, G., Stensballe, A., Overgaard, M. T., Givskov, M., Tolker-Nielsen, T., Otzen, D. E., and Nielsen, P. H. (2013). Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen 2, 365-82. doi:10.1002/mbo3.81.
47. Egland, P. G., Palmer, R. J., and Kolenbrander, P. E. (2004). Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. U. S. A. 101, 16917-22. doi:10.1073/pnas.0407457101.
48. Elias, S., and Banin, E. (2012). Multi-species biofilms: living with friendly neighbors. FEMS Microbiol. Rev. doi:10.1111/j.1574-6976.2012.00325.x.
49. Elsholz, A. K. W., Wacker, S. a, and Losick, R. (2014). Self-regulation of exopolysaccharide production in Bacillus subtilis by a tyrosine kinase. Genes Dev. 28, 1710-20. doi:10.1101/gad.246397.114.
50. Elvers, K. T., Leeming, K., and Lappin-Scott, H. M. (2002). Binary and mixed population biofilms: time-lapse image analysis and disinfection with biocides. J. Ind. Microbiol. Biotechnol. 29, 331-8. doi:10.1038/sj.jim.7000318.
51. Epstein, A. K., Pokroy, B., Seminara, A., and Aizenberg, J. (2011). Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc. Natl. Acad. Sci. U. S. A. 108, 995-1000. doi:10.1073/pnas.1011033108.
52. Flemming, H.-C. (2011a). "Microbial Biofouling: Unsolved Problems, Insufficient Approaches, and Possible Solutions," in Biofilm Highlights, Springer Series on Biofilms 5 Springer Series on Biofilms., eds. H.-C. Flemming, J. Wingender, and U. Szewzyk (Berlin, Heidelberg: Springer Berlin Heidelberg), 81-110. doi:10.1007/978-3-642- 19940-0.
53. Flemming, H.-C. (2011b). The perfect slime. Colloids Surf. B. Biointerfaces 86, 251-9. doi:10.1016/j.colsurfb.2011.04.025.
54. Flemming, H.-C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Microbiol. 8, 623- 633. doi:10.1080/0892701031000072190.
55. Ganin, H., Danin-Poleg, Y., Kashi, Y., and Meijler, M. M. (2012). Vibrio cholerae autoinducer CAI-1 interferes with Pseudomonas aeruginosa quorum sensing and inhibits its growth. ACS Chem. Biol. 7, 659-65. doi:10.1021/cb2004675.
56. Gensberger, E. T., Sessitsch, A., and Kostic, T. (2013). Propidium monoazide-quantitative polymerase chain reaction for viable Escherichia coli and Pseudomonas aeruginosa detection from abund ant background microflora. Anal. Biochem. 441, 69-72. doi:10.1016/j.ab.2013.05.033.
57. Giaouris, E., Chorianopoulos, N., Doulgeraki, A., and Nychas, G.-J. (2013). Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLoS One 8, e77276. doi:10.1371/journal.pone.0077276.
58. Gilbert, P., Allison, D. G., and McBain, A. J. (2002). Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? J. Appl. Microbiol. 92 Suppl, 98S-110S.
59. Glover, J. R., Kowal, A. S., Schirmer, E. C., Patino, M. M., Liu, J. J., and Lindquist, S. (1997). Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell 89, 811-9.
60. Guiamet, P. S., and Gaylarde, C. C. (1996). Activity of an isothiazolone biocide against Hormoconis resinae in pure and mixed biofilms. World J. Microbiol. Biotechnol. 12, 395-7. doi:10.1007/BF00340218.
61. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108. doi:10.1038/nrmicro821.
62. Hansen, M. C., Palmer, R. J. J., Udsen, C., White, D. C., and Molin, S. (2001). Assessment of GFP fluorescence in cells of Streptococcus gordonii under conditions of low pH and low oxygen concentration. Microbiology 147, 1383-1391.
63. Hansen, S. K., Haagensen, J. a J., Gjermansen, M., Jørgensen, T. M., Tolker-Nielsen, T., and Molin, S. (2007). Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. J. Bacteriol. 189, 4932-4943. doi:10.1128/JB.00041-07.
64. Harmsen, M., Yang, L., Pamp, S. J., and Tolker-Nielsen, T. (2010). An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol. 59, 253-68. doi:10.1111/j.1574-695X.2010.00690.x.
65. Harriott, M. M., and Noverr, M. C. (2009). Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob. Agents Chemother. 53, 3914-22. doi:10.1128/AAC.00657-09.
66. Hassett, D. J., Elkins, J. G., Ma, J.-F., and McDermott, T. R. (1999). Pseudomonas aeruginosa biofilm sensitivity to biocides: Use of hydrogen peroxide as model antimicrobial agent for examining resistance mechanisms. Methods Enzymol. 310, 599-608. doi:10.1016/S0076-6879(99)10046-6.
67. Hausner, M., Lawrence, J. R., Wolfaardt, G. M., Schloter, M., Seiler, K.-P., and Hartmann, A. (2000). "The use of immunological techniques and scanning confocal laser microscopy fort he characterization of Agrobacterium tumefaciens and Pseudomonas fluorescens in atrazine-utilizing biofilms," in Biofilms:Investigate methods and Application, eds. H.-C. Flemming, U. Szewzyk, and T. Griebe (Lancaster, Basel: Technomic Publ.), 143-154.
68. Hausner, M., and Wuertz, S. (1999). High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65, 3710-3.
69. Hendricks, K. J., Burd, T. A., Anglen, J. O., Simpson, A. W., Christensen, G. D., and Gainor, B. J. (2001). Synergy between Staphylococcus aureus and Pseudomonas aeruginosa in a rat model of complex orthopaedic wounds. J. Bone Joint Surg. Am. 83-A, 855-61.
70. Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35, 322-32. doi:10.1016/j.ijantimicag.2009.12.011.
71. Huang, W. E., Stoecker, K., Griffiths, R., Newbold, L., Daims, H., Whiteley, A. S., and Wagner, M. (2007). Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9, 1878-89. doi:10.1111/j.1462-2920.2007.01352.x.
72. Irie, Y., Borlee, B. R., O'Connor, J. R., Hill, P. J., Harwood, C. S., Wozniak, D. J., and Parsek, M. R. (2012). Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 109, 20632-6. doi:10.1073/pnas.1217993109
73. Ito, A., May, T., Taniuchi, A., Kawata, K., and Okabe, S. (2009). Localized expression profiles of rpoS in Escherichia coli biofilms. Biotechnol. Bioeng. 103, 975-83. doi:10.1002/bit.22305.
74. Jahid, I. K., Han, N., Zhang, C.-Y., and Ha, S.-D. (2015). Mixed culture biofilms of Salmonella Typhimurium and cultivable indigenous microorganisms on lettuce show enhanced resistance of their sessile cells to cold oxygen plasma. Food Microbiol. 46, 383-94. doi:10.1016/j.fm.2014.08.003.
75. Jang, A., Szabo, J., Hosni, A. A., Coughlin, M., and Bishop, P. L. (2006). Measurement of chlorine dioxide penetration in dairy process pipe biofilms during disinfection. Appl. Microbiol. Biotechnol. 72, 368-76. doi:10.1007/s00253-005-0274-5.
76. Jayaraman, A., and Wood, T. K. (2008). Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu. Rev. Biomed. Eng. 10, 145-67. doi:10.1146/annurev.bioeng.10.061807.160536.
77. Kara, D., Luppens, S. B. I., and Ten Cate, J. M. (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, 58-63.
78. Kart, D., Tavernier, S., Van Acker, H., Nelis, H. J., and Coenye, T. (2014). Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling 30, 377-83. doi:10.1080/08927014.2013.878333.
79. Kim, J., Hahn, J.-S., Franklin, M. J., Stewart, P. S., and Yoon, J. (2009). Tolerance of dormant and active cells in Pseudomonas aeruginosa PA01 biofilm to antimicrobial agents. J. Antimicrob. Chemother. 63, 129-35. doi:10.1093/jac/dkn462.
80. Kindaichi, T., Ito, T., and Okabe, S. (2004). Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiography-fluorescence in situ hybridization. Appl. Environ. Microbiol. 70, 1641-50.
81. Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jørgensen, A., Molin, S., and Tolker-Nielsen, T. (2003). Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48, 1511-1524. doi:10.1046/j.1365- 2958.2003.03525.x.
82. Kobayashi, K., and Iwano, M. (2012). BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol. Microbiol. 85, 51-66. doi:10.1111/j.1365- 2958.2012.08094.x.
83. Korgaonkar, A., Trivedi, U., Rumbaugh, K. P., and Whiteley, M. (2013). Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc. Natl. Acad. Sci. U. S. A. 110, 1059-64. doi:10.1073/pnas.1214550110.
84. Kostaki, M., Chorianopoulos, N., Braxou, E., Nychas, G.-J., and Giaouris, E. (2012). Differential biofilm formation and chemical disinfection resistance of sessile cells of listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl. Environ. Microbiol. 78, 2586-95. doi:10.1128/AEM.07099- 11.
85. Kucera, J., Sojka, M., Pavlik, V., Szuszkiewicz, K., Velebny, V., and Klein, P. (2014). Multispecies biofilm in an artificial wound bed--A novel model for in vitro assessment of solid antimicrobial dressings. J. Microbiol. Methods 103, 18-24. doi:10.1016/j.mimet.2014.05.008.
86. De la Cruz, F., and Davies, J. (2000). Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 8, 128-33.
87. Lee, K. W. K., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S., and Rice, S. a (2014). Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 8, 894-907. doi:10.1038/ismej.2013.194.
88. Lee, N., Nielsen, P. H., Andreasen, K. H., Juretschko, S., Nielsen, J. L., Schleifer, K. H., and Wagner, M. (1999). Combination of fluorescent in situ hybridization and microautoradiography-a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65, 1289-97.
89. Leriche, V., Briandet, R., and 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, 64-71.
90. Leriche, V., and Carpentier, B. (1995). Viable but noncultibable Salmonella typhimurium in Single- and Binary-Species Biofilms in Response to Chlorine Treatment. J. Food Prot. 58, 1186-1191.
91. Lewis, K. (2010). Persister cells. Annu. Rev. Microbiol. 64, 357-72. doi:10.1146/annurev.micro.112408.134306.
92. Li, L., Mendis, N., Trigui, H., Oliver, J. D., and Faucher, S. P. (2014). The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol. 5, 258. doi:10.3389/fmicb.2014.00258.
93. Lindsay, D., Brözel, V. S., Mostert, J. F., and von Holy, a (2002). Differential efficacy of a chlorine dioxide-containing sanitizer against single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J. Appl. Microbiol. 92, 352-61.
94. Lopes, S. P., Ceri, H., Azevedo, N. F., and Pereira, M. O. (2012). Antibiotic resistance of mixed biofilms in cystic fibrosis: Impact of emerging microorganisms on treatment of infection. Int. J. Antimicrob. Agents 40, 260-263. doi:10.1016/j.ijantimicag.2012.04.020.
95. Løvdal, T., Hovda, M. B., Björkblom, B., and Møller, S. G. (2011). Propidium monoazide combined with real-time quantitative PCR underestimates heat-killed Listeria innocua. J. Microbiol. Methods 85, 164-9. doi:10.1016/j.mimet.2011.01.027.
96. Luppens, S. B. I., Kara, D., Bandounas, L., Jonker, M. J., Wittink, F. R. A., Bruning, O., Breit, T. M., Ten Cate, J. M., and Crielaard, W. (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, 183-9. doi:10.1111/j.1399- 302X.2007.00409.x.
97. Ma, H., and Bryers, J. D. (2010). Non-invasive method to quantify local bacterial concentrations in a mixed culture biofilm. J. Ind. Microbiol. Biotechnol. 37, 1081-9. doi:10.1007/s10295-010-0756-z.
98. Maciel, B. M., Dias, J. C. T., Romano, C. C., Sriranganathan, N., Brendel, M., and Rezende, R. P. (2011). Detection of Salmonella Enteritidis in asymptomatic carrier animals: comparison of quantitative real-time PCR and bacteriological culture methods. Genet. Mol. Res. 10, 2578-88. doi:10.4238/2011.October.24.1
99. Mack, D., Rohde, H., Harris, L. G., Davies, A. P., Horstkotte, M. A., and Knobloch, J. K.-M. (2006). Biofilm formation in medical device-related infection. Int. J. Artif. Organs 29, 343-59.
100. Maillard, J.-Y. (2002). Bacterial target sites for biocide action. J. Appl. Microbiol. 92 Suppl, 16S-27S.
101. Malic, S., Hill, K. E., Hayes, A., Percival, S. L., Thomas, D. W., and Williams, D. W. (2009). Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology 155, 2603-11. doi:10.1099/mic.0.028712-0.
102. Marsh, P. D., and Bradshaw, D. J. (1995). Dental plaque as a biofilm. J. Ind. Microbiol. 15, 169-75.
103. Martinez, J. L. (2009). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157, 2893-902. doi:10.1016/j.envpol.2009.05.051.
104. Mashburn, L. M., Jett, A. M., Akins, D. R., and Whiteley, M. (2005). Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187, 554-66. doi:10.1128/JB.187.2.554-566.2005.
105. Miller, M. B., and Bassler, B. L. (2001). Quorum Sensing in Bacteria. Annu. Rev. Genet. 55, 165-199.
106. Millezi, F. M., Pereira, M. O., Batista, N. N., Camargos, N., Auad, I., Cardoso, M. D. G., and Piccoli, R. H. (2012). Susceptibility of monospecies and dual-species biofilms of staphylococcus aureus and escherichia coli to essential oils. J. Food Saf. 32, 351-359. doi:10.1111/j.1745-4565.2012.00387.x.
107. Moellering, R. C. (2012). MRSA: the first half century. J. Antimicrob. Chemother. 67, 4-11. doi:10.1093/jac/dkr437.
108. Moons, P., Van Houdt, R., Aertsen, A., Vanoirbeek, K., Engelborghs, Y., and Michiels, C. W. (2006). Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including mixed biofilms with Escherichia coli. Appl. Environ. Microbiol. 72, 7294-300. doi:10.1128/AEM.01708-06.
109. Moormeier, D. E., Endres, J. L., Mann, E. E., Sadykov, M. R., Horswill, A. R., Rice, K. C., Fey, P. D., and Bayles, K. W. (2013). Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches. Appl. Environ. Microbiol. 79, 3413-24. doi:10.1128/AEM.00395- 13.
110. Morris, J. G., Sztein, M. B., Rice, E. W., Nataro, J. P., Losonsky, G. A., Panigrahi, P., Tacket, C. O., and Johnson, J. A. (1996). Vibrio cholerae 01 Can Assume a Chlorine-Resistant Rugose Survival Form that Is Virulent for Humans. J. Infect. Dis. 174, 1364-1368. doi:10.1093/infdis/174.6.1364.
111. Musat, N., Foster, R., Vagner, T., Adam, B., and Kuypers, M. M. M. (2012). Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol. Rev. 36, 486-511. doi:10.1111/j.1574-6976.2011.00303.x.
112. Neu, T., Swerhone, G. D., and Lawrence, J. R. (2001). Assessment of lectin-binding analysis for in situ detection of glycoconjugates in biofilm systems. Microbiology 147, 299-313.
113. Nielsen, a T., Tolker-Nielsen, T., Barken, K. B., and Molin, S. (2000). Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ. Microbiol. 2, 59-68.
114. Nielsen, J. L., and Nielsen, P. H. (2005). Advances in microscopy: microautoradiography of single cells. Methods Enzymol. 397, 237-56. doi:10.1016/S0076-6879(05)97014-6.
115. Nocker, A., Cheung, C.-Y., and Camper, A. K. (2006). Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Methods 67, 310-20. doi:10.1016/j.mimet.2006.04.015.
116. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D., and DeLong, E. F. (2001). Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484-7. doi:10.1126/science.1061338.
117. Pammi, M., Liang, R., Hicks, J., Mistretta, T.-A., and Versalovic, J. (2013). Biofilm extracellular DNA enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans. BMC Microbiol. 13, 257. doi:10.1186/1471-2180-13-257.
118. Parsek, M. R., and Greenberg, E. P. (2000). Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. U. S. A. 97, 8789-93.
119. Pastar, I., Nusbaum, A. G., Gil, J., Patel, S. B., Chen, J., Valdes, J., Stojadinovic, O., Plano, L. R., Tomic-Canic, M., and Davis, S. C. (2013). Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection. PLoS One 8, e56846. doi:10.1371/journal.pone.0056846.
120. Pathak, S., Awuh, J. A., Leversen, N. A., Flo, T. H., and Asjø, B. (2012). Counting mycobacteria in infected human cells and mouse tissue: a comparison between qPCR and CFU. PLoS One 7, e34931. doi:10.1371/journal.pone.0034931.
121. Pawar, D. M., Rossman, M. L., and Chen, J. (2005). Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J. Appl. Microbiol. 99, 418-25. doi:10.1111/j.1365-2672.2005.02499.x.
122. Pereira, C. S., Thompson, J. a, and Xavier, K. B. (2013). AI-2-mediated signalling in bacteria. FEMS Microbiol. Rev. 37, 156-81. doi:10.1111/j.1574-6976.2012.00345.x.
123. Peters, B. M., Jabra-Rizk, M. A., Scheper, M. A., Leid, J. G., Costerton, J. W., and Shirtliff, M. E. (2010). Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms. FEMS Immunol. Med. Microbiol. 59, 493-503. doi:10.1111/j.1574-695X.2010.00710.x
124. Ramsey, M. M., Rumbaugh, K. P., and Whiteley, M. (2011). Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog. 7, e1002012. doi:10.1371/journal.ppat.1002012.
125. Rao, D., Webb, J. S., and Kjelleberg, S. (2005). Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl. Environ. Microbiol. 71, 1729-36. doi:10.1128/AEM.71.4.1729-1736.2005.
126. Ren, D., Madsen, J. S., de la Cruz-Perera, C. I., Bergmark, L., Sørensen, S. J., and Burmølle, M. (2014). High-throughput screening of multispecies biofilm formation and quantitative PCR-based assessment of individual species proportions, useful for exploring interspecific bacterial interactions. Microb. Ecol. 68, 146-54. doi:10.1007/s00248-013- 0315-z.
127. Rendueles, O., and Ghigo, J.-M. (2012). Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol. Rev. 36, 972-989. doi:10.1111/j.1574-6976.2012.00328.x.
128. Rickard, A. H., Colacino, K. R., Manton, K. M., Morton, R. I., Pulcini, E., Pfeil, J., Rhoads, D., Wolcott, R. D., and James, G. (2010). Production of cell-cell signalling molecules by bacteria isolated from human chronic wounds. J. Appl. Microbiol. 108, 1509-22. doi:10.1111/j.1365-2672.2009.04554.x
129. Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E., and Handley, P. S. (2003). Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11, 94-100.
130. Robinson, C. J., Bohannan, B. J. M., and Young, V. B. (2010). From structure to function: the ecology of host-associated microbial communities. Microbiol. Mol. Biol. Rev. 74, 453- 76. doi:10.1128/MMBR.00014-10.
131. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010). Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U. S. A. 107, 2230-4. doi:10.1073/pnas.0910560107.
132. Römling, U. (2005). Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62, 1234-46. doi:10.1007/s00018-005-4557-x.
133. Rüger, M., Ackermann, M., and Reichl, U. (2014). Species-specific viability analysis of Pseudomonas aeruginosa, Burkholderia cepacia and Staphylococcus aureus in mixed culture by flow cytometry. BMC Microbiol. 14, 56. doi:10.1186/1471-2180-14-56.
134. Russell, A. D. (1999). Bacterial resistance to disinfectants: present knowledge and future problems. J. Hosp. Infect. 43 Suppl, S57-68.
135. Saá Ibusquiza, P., Herrera, J. J. R., Vázquez-Sánchez, D., and Cabo, M. L. (2012). Adherence kinetics, resistance to benzalkonium chloride and microscopic analysis of mixed biofilms formed by Listeria monocytogenes and Pseudomonas putida. Food Control 25, 202-210. doi:10.1016/j.foodcont.2011.10.002.
136. Sabaeifard, P., Abdi-Ali, A., Soudi, M. R., and Dinarvand, R. (2014). Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J. Microbiol. Methods 105, 134-40. doi:10.1016/j.mimet.2014.07.024.
137. Sánchez, M. C., Marín, M. J., Figuero, E., Llama-Palacios, A., León, R., Blanc, V., Herrera, D., and Sanz, M. (2014). Quantitative real-time PCR combined with propidium monoazide for the selective quantification of viable periodontal pathogens in an in vitro subgingival biofilm model. J. Periodontal Res. 49, 20-8. doi:10.1111/jre.12073.
138. Sanchez-Vizuete, P., Le Coq, D., Bridier, A., Herry, J.-M., Aymerich, S., and Briandet, R. (2015). Identification of ypqP as a New Bacillus subtilis Biofilm Determinant That Mediates the Protection of Staphylococcus aureus against Antimicrobial Agents in Mixed-Species Communities. Appl. Environ. Microbiol. 81, 109-118. doi:10.1128/AEM.02473-14.
139. Schertzer, J. W., Boulette, M. L., and Whiteley, M. (2009). More than a signal: non-signaling properties of quorum sensing molecules. Trends Microbiol. 17, 189-95. doi:10.1016/j.tim.2009.02.001.
140. Schwering, M., Song, J., Louie, M., Turner, R. J., and Ceri, H. (2013). Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling 29, 917-28. doi:10.1080/08927014.2013.816298.
141. Servais, P., Prats, J., Passerat, J., and Garcia-Armisen, T. (2009). Abundance of culturable versus viable Escherichia coli in freshwater. Can. J. Microbiol. 55, 905-9. doi:10.1139/w09-043.
142. Seth, A. K., Geringer, M. R., Hong, S. J., Leung, K. P., Galiano, R. D., and Mustoe, T. A. (2012). Comparative analysis of single-species and polybacterial wound biofilms using a quantitative, in vivo, rabbit ear model. PLoS One 7, e42897. doi:10.1371/journal.pone.0042897.
143. Shank, E. A., Klepac-Ceraj, V., Collado-Torres, L., Powers, G. E., Losick, R., and Kolter, R. (2011). Interspecies interactions that result in Bacillus subtilis forming biofilms are mediated mainly by members of its own genus. Proc. Natl. Acad. Sci. U. S. A. 108, E1236-43. doi:10.1073/pnas.1103630108.
144. Shirtliff, M., and Leid, J. (2009). The Role of Biofilms in Device-Related. Springer series on biofilms doi:10.1007/7142.
145. Simões, M., Simões, L. C., and Vieira, M. J. (2009). Species association increases biofilm resistance to chemical and mechanical treatments. Water Res. 43, 229-37. doi:10.1016/j.watres.2008.10.010.
146. Singh, R., Ray, P., Das, A., and Sharma, M. (2010). Enhanced production of exopolysaccharide matrix and biofilm by a menadione-auxotrophic Staphylococcus aureus small-colony variant. J. Med. Microbiol. 59, 521-7. doi:10.1099/jmm.0.017046-0.
147. Skillman, L. C., Sutherland, I. W., and Jones, M. V (1998). The role of exopolysaccharides in dual species biofilm development. J. Appl. Microbiol. 85 Suppl 1, 13S-18S. doi:10.1111/j.1365-2672.1998.tb05278.x.
148. Slimani, S., Robyns, A., Jarraud, S., Molmeret, M., Dusserre, E., Mazure, C., Facon, J. P., Lina, G., Etienne, J., and Ginevra, C. (2012). Evaluation of propidium monoazide (PMA) treatment directly on membrane filter for the enumeration of viable but non cultivable Legionella by qPCR. J. Microbiol. Methods 88, 319-21. doi:10.1016/j.mimet.2011.12.010.
149. Stacy, A., Everett, J., Jorth, P., Trivedi, U., Rumbaugh, K. P., and Whiteley, M. (2014). Bacterial fight-and-flight responses enhance virulence in a polymicrobial infection. Proc. Natl. Acad. Sci. U. S. A. 111, 7819-24. doi:10.1073/pnas.1400586111.
150. Starkey, M., Hickman, J. H., Ma, L., Zhang, N., De Long, S., Hinz, A., Palacios, S., Manoil, C., Kirisits, M. J., Starner, T. D., et al. (2009). Pseudomonas aeruginosa rugose small colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J. Bacteriol. 191, 3492-503. doi:10.1128/JB.00119-09.
151. Stender, H., Fiandaca, M., Hyldig-Nielsen, J. J., and Coull, J. (2002). PNA for rapid microbiology. J. Microbiol. Methods 48, 1-17.
152. Stewart, P. S. (2002). Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292, 107-13. doi:10.1078/1438-4221-00196.
153. Stewart, P. S., and Franklin, M. J. (2008). Ph ysiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199-210. doi:10.1038/nrmicro1838.
154. Stewart, P. S., Rayner, J., Roe, F., and Rees, W. M. (2001). Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J. Appl. Microbiol. 91, 525-532.
155. Sutherland, I. (2001). Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147, 3-9.
156. Takenaka, S., Trivedi, H. M., Corbin, A., Pitts, B., and Stewart, P. S. (2008). Direct visualization of spatial and temporal patterns of antimicrobial action within model oral biofilms. Appl. Environ. Microbiol. 74, 1869-75. doi:10.1128/AEM.02218-07.
157. Terada, A., Hibiya, K., Nagai, J., Tsuneda, S., and Hirata, A. (2003). Nitrogen removal characteristics and biofilm analysis of a membrane-aerated biofilm reactor applicable to high-strength nitrogenous wastewater treatment. J. Biosci. Bioeng. 95, 170-178. doi:10.1016/S1389-1723(03)80124-X.
158. Thurnheer, T., Gmür, R., and Guggenheim, B. (2004). Multiplex FISH analysis of a six species bacterial biofilm. J. Microbiol. Methods 56, 37-47. doi:10.1016/j.mimet.2003.09.003.
159. Tomlin, K. L., Coll, O. P., and Ceri, H. (2001). Interspecies biofilms of Pseudomonas aeruginosa and Burkholderia cepacia. Can. J. Microbiol. 47, 949-54.
160. Trejo-Hernández, A., Andrade-Domínguez, A., Hernández, M., and Encarnación, S. (2014). Interspecies competition triggers virulence and mutability in Candida albicans- Pseudomonas aeruginosa mixed biofilms. ISME J. 8, 1974-88. doi:10.1038/ismej.2014.53.
161. Trevors, J. T. (2011). Viable but non-culturable (VBNC) bacteria: Gene expression in planktonic and biofilm cells. J. Microbiol. Methods 86, 266-73. doi:10.1016/j.mimet.2011.04.018.
162. Tükel, C., Nishimori, J. H., Wilson, R. P., Winter, M. G., Keestra, A. M., van Putten, J. P. M., and Bäumler, A. J. (2010). Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell. Microbiol. 12, 1495-505. doi:10.1111/j.1462-5822.2010.01485.x.
163. Uhlich, G. A., Cooke, P. H., and Solomon, E. B. (2006). Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl. Environ. Microbiol. 72, 2564-72. doi:10.1128/AEM.72.4.2564-2572.2006.
164. Van der Veen, S., and Abee, T. (2011). Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int. J. Food Microbiol. 144, 421-31. doi:10.1016/j.ijfoodmicro.2010.10.029.
165. Wagner, M. (2009). Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu. Rev. Microbiol. 63, 411-429. doi:10.1146/annurev.micro.091208.073233.
166. Wang, R., Kalchayanand, N., Schmidt, J. W., and Harhay, D. M. (2013). Mixed biofilm formation by Shiga toxin-producing Escherichia coli and Salmonella enterica serovar Typhimurium enhanced bacterial resistance to sanitization due to extracellular polymeric substances. J. Food Prot. 76, 1513-22. doi:10.4315/0362-028X.JFP-13-077.
167. Wang, X., and Wood, T. K. (2011). Toxin- antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77, 5577-83. doi:10.1128/AEM.05068-11.
168. Wang, Y., Dai, Y., Zhang, Y., Hu, Y., Yang, B., and Chen, S. (2007). Effects of quorum sensing autoinducer degradation gene on virulence and biofilm formation of Pseudomonas aeruginosa. Sci. China. C. Life Sci. 50, 385-91. doi:10.1007/s11427-007-0044-y.
169. Wei, X., Pathak, D. T., and Wall, D. (2011). Heterologous protein transfer within structured myxobacteria biofilms. Mol. Microbiol. 81, 315-26. doi:10.1111/j.1365- 2958.2011.07710.x.
170. West, S. A., Winzer, K., Gardner, A., and Diggle, S. P. (2012). Quorum sensing and the confusion about diffusion. Trends Microbiol. 20, 586-94. doi:10.1016/j.tim.2012.09.004.
171. Whiteley, M., Ott, J. R., Weaver, E. a, and McLean, R. J. (2001). Effects of community composition and growth rate on aquifer biofilm bacteria and their susceptibility to betadine disinfection. Environ. Microbiol. 3, 43-52.
172. Wiedenbeck, J., and Cohan, F. M. (2011). Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol. Rev. 35, 957- 76. doi:10.1111/j.1574-6976.2011.00292.x.
173. Wolcott, R., Costerton, J. W., Raoult, D., and Cutler, S. J. (2013). The polymicrobial nature of biofilm infection. Clin. Microbiol. Infect. 19, 107-12. doi:10.1111/j.1469- 0691.2012.04001.x.
174. Yap, B., Zilm, P. S., Briggs, N., Rogers, A. H., and Cathro, P. C. (2014). The effect of sodium hypochlorite on Enterococcus faecalis when grown on dentine as a single- and multi species biofilm. Aust. Endod. J. 40, 101-10. doi:10.1111/aej.12073.
175. Yasunaga, A., Yoshida, A., Morikawa, K., Maki, K., Nakamura, S., Soh, I., Awano, S., and Ansai, T. (2013). Monitoring the prevalence of viable and dead cariogenic bacteria in oral specimens and in vitro biofilms by qPCR combined with propidium monoazide. BMC Microbiol. 13, 157. doi:10.1186/1471-2180-13-157.
176. Zhang, L.-H., and Dong, Y.-H. (2004). Quorum sensing and signal interference: diverse implications. Mol. Microbiol. 53, 1563-71. doi:10.1111/j.1365-2958.2004.04234.x.
177. Zhou, Y., Smith, D., Leong, B. J., Brännström, K., Almqvist, F., and Chapman, M. R. (2012). Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J. Biol. Chem. 287, 35092-103. doi:10.1074/jbc.M112.383737.