Impact of Mycobacterial Biofilms on Public Health

  • Anil K. OjhaEmail author
Part of the Advances in Environmental Microbiology book series (AEM, volume 5)


The genus Mycobacterium represents over 150 bacterial species of the actinomycetes family, inhabiting a wide range of ecological niches—from soil and aquatic environments to intracellular phagosomes in human bodies. Mycobacterium tuberculosis (Mtb), the etiological agent of tuberculosis in human, is the predominant mycobacterial pathogen that resides in an estimated one-third of the world’s human population, causing disease in hundreds of millions and killing over a million people every year. In addition, several environmental mycobacteria including Mycobacterium avium and Mycobacterium abscessus are opportunistic pathogens that can establish infection in immunocompromised individuals. A common characteristic of all mycobacterial infections, regardless of the species, is their extraordinary recalcitrance to antibiotic regimens, although the underlying basis of drug resistance remains unclear. Recent studies suggest a possible linkage between mycobacterial tolerance to antibiotics and their propensity to grow as organized multicellular aggregates, called biofilms. This chapter describes the linkage and its implication in controlling mycobacterial infections in humans.


Mycobacteria Tuberculosis Biofilms Nontuberculous 


Compliance with Ethical Standards


This study was funded by the National Institute of Health (Grant # AI132422).

Conflict of Interest

Anil K. Ojha declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by the author.


  1. Absalon C, Van Dellen K, Watnick PI (2011) A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS Pathog 7:e1002210. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adam B, Baillie GS, Douglas LJ (2002) Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344–349. CrossRefPubMedGoogle Scholar
  3. Allison DG, Ruiz B, SanJose C, Jaspe A, Gilbert P (1998) Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol Lett 167:179–184CrossRefPubMedGoogle Scholar
  4. Baty AM 3rd, Eastburn CC, Techkarnjanaruk S, Goodman AE, Geesey GG (2000) Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microbiol 66:3574–3585CrossRefPubMedPubMedCentralGoogle Scholar
  5. Benedict MI, Wulff LM, White RB (1992) Current parental stress in maltreating and nonmaltreating families of children with multiple disabilities. Child Abuse Negl 16:155–163CrossRefPubMedGoogle Scholar
  6. Benwill JL, Wallace RJ Jr (2014) Mycobacterium abscessus: challenges in diagnosis and treatment. Curr Opin Infect Dis 27:506–510. CrossRefPubMedGoogle Scholar
  7. Bernut A, Herrmann JL, Kissa K, Dubremetz JF, Gaillard JL, Lutfalla G, Kremer L (2014) Mycobacterium abscessus cording prevents phagocytosis and promotes abscess formation. Proc Natl Acad Sci USA 111:E943–E952. CrossRefPubMedGoogle Scholar
  8. Boles BR, Thoendel M, Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223. CrossRefPubMedGoogle Scholar
  9. Branda SS, Vik S, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13:20–26CrossRefPubMedGoogle Scholar
  10. Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63. CrossRefPubMedGoogle Scholar
  11. Caiazza NC, O’Toole GA (2004) SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186:4476–4485. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Catherinot E et al (2007) Hypervirulence of a rough variant of the Mycobacterium abscessus type strain. Infect Immun 75:1055–1058. CrossRefPubMedGoogle Scholar
  14. Chai Y, Chu F, Kolter R, Losick R (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67:254–263. CrossRefPubMedGoogle Scholar
  15. Chamberlin W et al (2001) Review article: Mycobacterium avium subsp. paratuberculosis as one cause of Crohn’s disease. Aliment Pharmacol Ther 15:337–346CrossRefPubMedGoogle Scholar
  16. Conrady DG, Brescia CC, Horii K, Weiss AA, Hassett DJ, Herr AB (2008) A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci USA 105:19456–19461. CrossRefPubMedGoogle Scholar
  17. Costerton JW, Irvin RT, Cheng KJ (1981) The role of bacterial surface structures in pathogenesis. Crit Rev Microbiol 8:303–338CrossRefPubMedGoogle Scholar
  18. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427–5433PubMedPubMedCentralGoogle Scholar
  19. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cugini C, Calfee MW, Farrow JM 3rd, Morales DK, Pesci EC, Hogan DA (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65:896–906. CrossRefPubMedGoogle Scholar
  21. de Beer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43:1131–1138. CrossRefPubMedGoogle Scholar
  22. Delaquis PJ, Caldwell DE, Lawrence JR, McCurdy AR (1989) Detachment of Pseudomonas fluorescens from biofilms on glass surfaces in response to nutrient stress. Microb Ecol 18:199–210. CrossRefPubMedGoogle Scholar
  23. Desai M, Buhler T, Weller PH, Brown MR (1998) Increasing resistance of planktonic and biofilm cultures of Burkholderia cepacia to ciprofloxacin and ceftazidime during exponential growth. J Antimicrob Chemother 42:153–160CrossRefPubMedGoogle Scholar
  24. Dubos RJ, Middlebrook G (1948) The effect of wetting agents on the growth of tubercle bacilli. J Exp Med 88:81–88CrossRefPubMedPubMedCentralGoogle Scholar
  25. Duguid IG, Evans E, Brown MR, Gilbert P (1992) Growth-rate-independent killing by ciprofloxacin of biofilm-derived Staphylococcus epidermidis; evidence for cell-cycle dependency. J Antimicrob Chemother 30:791–802CrossRefPubMedGoogle Scholar
  26. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990–1004. CrossRefPubMedGoogle Scholar
  27. Falkinham JO 3rd (2007) Growth in catheter biofilms and antibiotic resistance of Mycobacterium avium. J Med Microbiol 56:250–254. CrossRefPubMedGoogle Scholar
  28. Feazel LM, Baumgartner LK, Peterson KL, Frank DN, Harris JK, Pace NR (2009) Opportunistic pathogens enriched in showerhead biofilms. Proc Natl Acad Sci USA 106:16393–16399. CrossRefPubMedGoogle Scholar
  29. Field SK, Fisher D, Cowie RL (2004) Mycobacterium avium complex pulmonary disease in patients without HIV infection. Chest 126:566–581. CrossRefPubMedGoogle Scholar
  30. Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34–40. CrossRefPubMedGoogle Scholar
  31. Garchitorena A, Guegan JF, Leger L, Eyangoh S, Marsollier L, Roche B (2015) Mycobacterium ulcerans dynamics in aquatic ecosystems are driven by a complex interplay of abiotic and biotic factors. elife 4:e07616. CrossRefPubMedPubMedCentralGoogle Scholar
  32. George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J, Lee R, Small PL (1999) Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854–857CrossRefGoogle Scholar
  33. Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker-Nielsen T (2005) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7:894–906. CrossRefPubMedGoogle Scholar
  34. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75:815–826. CrossRefPubMedGoogle Scholar
  35. Gonzalez-Santiago TM, Drage LA (2015) Nontuberculous mycobacteria: skin and soft tissue infections. Dermatol Clin 33:563–577. CrossRefPubMedGoogle Scholar
  36. Hall-Stoodley L, Stoodley P (2002) Developmental regulation of microbial biofilms. Curr Opin Biotechnol 13:228–233CrossRefPubMedGoogle Scholar
  37. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108CrossRefPubMedGoogle Scholar
  38. Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101–104CrossRefPubMedGoogle Scholar
  39. Han XY, Tarrand JJ, Infante R, Jacobson KL, Truong M (2005) Clinical significance and epidemiologic analyses of Mycobacterium avium and Mycobacterium intracellulare among patients without AIDS. J Clin Microbiol 43:4407–4412. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091CrossRefPubMedGoogle Scholar
  41. Henrici AT (1933) Studies of freshwater bacteria: I. A direct microscopic technique. J Bacteriol 25:277–287PubMedPubMedCentralGoogle Scholar
  42. Hinsa SM, Espinosa-Urgel M, Ramos JL, O’Toole GA (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49:905–918CrossRefPubMedGoogle Scholar
  43. Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:2229–2232. CrossRefPubMedGoogle Scholar
  44. Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212–1223CrossRefPubMedGoogle Scholar
  45. Holcombe LJ et al (2010) Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. Microbiology 156:1476–1486. CrossRefPubMedGoogle Scholar
  46. Hunter RL, Olsen MR, Jagannath C, Actor JK (2006) Multiple roles of cord factor in the pathogenesis of primary, secondary, and cavitary tuberculosis, including a revised description of the pathology of secondary disease. Ann Clin Lab Sci 36:371–386PubMedGoogle Scholar
  47. Islam MS, Richards JP, Ojha AK (2012) Targeting drug tolerance in mycobacteria: a perspective from mycobacterial biofilms. Expert Rev Anti-Infect Ther 10:1055–1066. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Iwase T et al (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–349. CrossRefPubMedGoogle Scholar
  49. Jindani A, Dore CJ, Mitchison DA (2003) Bactericidal and sterilizing activities of antituberculosis drugs during the first 14 days. Am J Respir Crit Care Med 167:1348–1354CrossRefPubMedGoogle Scholar
  50. Jones AC (1896) On the so-called Tubercle Bacilli Report of the sixty-sixth meeting of the British Association for the Advancements of Science 1015–1016Google Scholar
  51. Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N (2004) Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48:2633–2636. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Karakousis PC, Moore RD, Chaisson RE (2004) Mycobacterium avium complex in patients with HIV infection in the era of highly active antiretroviral therapy. Lancet Infect Dis 4:557–565. CrossRefPubMedGoogle Scholar
  53. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302CrossRefPubMedGoogle Scholar
  55. Kolter R, Losick R (1998) One for all and all for one. Science 280:226–227CrossRefPubMedGoogle Scholar
  56. Kuboniwa M et al (2006) Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol Microbiol 60:121–139. CrossRefPubMedGoogle Scholar
  57. Lewis K (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322:107–131PubMedGoogle Scholar
  58. Mah TF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39CrossRefPubMedGoogle Scholar
  59. Mann EE et al (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4:e5822. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Marrie TJ, Nelligan J, Costerton JW (1982) A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66:1339–1341CrossRefPubMedGoogle Scholar
  61. Marsollier L et al (2005) Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell Microbiol 7:935–943CrossRefPubMedGoogle Scholar
  62. McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S (2012) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10:39–50. CrossRefGoogle Scholar
  63. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS, Lamont RJ (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185:274–284CrossRefPubMedPubMedCentralGoogle Scholar
  64. Medjahed H, Reyrat JM (2009) Construction of Mycobacterium abscessus defined glycopeptidolipid mutants: comparison of genetic tools. Appl Environ Microbiol 75:1331–1338. CrossRefPubMedGoogle Scholar
  65. Medjahed H, Singh AK (2010) Genetic manipulation of Mycobacterium abscessus. Curr Protoc Microbiol Chapter 10:Unit 10D 12.
  66. Mireles JR 2nd, Toguchi A, Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183:5848–5854. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Nessar R, Reyrat JM, Davidson LB, Byrd TF (2011) Deletion of the mmpL4b gene in the Mycobacterium abscessus glycopeptidolipid biosynthetic pathway results in loss of surface colonization capability, but enhanced ability to replicate in human macrophages and stimulate their innate immune response. Microbiology 157:1187–1195. CrossRefPubMedGoogle Scholar
  68. Nickel JC, Ruseska I, Wright JB, Costerton JW (1985) Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 27:619–624CrossRefPubMedPubMedCentralGoogle Scholar
  69. Nijland R, Hall MJ, Burgess JG (2010) Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS One 5:e15668. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ojha A, Hatfull GF (2007) The role of iron in Mycobacterium smegmatis biofilm formation: the exochelin siderophore is essential in limiting iron conditions for biofilm formation but not for planktonic growth. Mol Microbiol 66:468–483CrossRefPubMedPubMedCentralGoogle Scholar
  71. Ojha A, Anand M, Bhatt A, Kremer L, Jacobs WR Jr, Hatfull GF (2005) GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123:861–873CrossRefPubMedGoogle Scholar
  72. Ojha AK et al (2008) Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol 69:164–174CrossRefPubMedPubMedCentralGoogle Scholar
  73. Ojha AK, Hatfull GF, Jacobs WR Jr (2015) Genetic dissection of mycobacterial biofilms. In: Parish T, Roberts D (eds) Mycobacteria protocols. Springer, New YorkGoogle Scholar
  74. Parrish NM, Dick JD, Bishai WR (1998) Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 6:107–112CrossRefPubMedGoogle Scholar
  75. Periasamy S, Kolenbrander PE (2010) Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J Bacteriol 192:2965–2972. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Petrova OE, Sauer K (2016) Escaping the biofilm in more than one way: desorption, detachment or dispersion. Curr Opin Microbiol 30:67–78. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Pierce ES (2009) Possible transmission of Mycobacterium avium subspecies paratuberculosis through potable water: lessons from an urban cluster of Crohn’s disease. Gut Pathog 1:17. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Purevdorj-Gage B, Costerton WJ, Stoodley P (2005) Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151:1569–1576. CrossRefPubMedGoogle Scholar
  79. Rani SA et al (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189:4223–4233. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Rendueles O, Ghigo JM (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36:972–989. CrossRefPubMedGoogle Scholar
  81. Richards JP, Ojha AK (2014) Mycobacterial biofilms. Microbiol Spectr 2(5).
  82. Rose SJ, Bermudez LE (2014) Mycobacterium avium biofilm attenuates mononuclear phagocyte function by triggering hyperstimulation and apoptosis during early infection. Infect Immun 82:405–412. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Rose SJ, Babrak LM, Bermudez LE (2015) Mycobacterium avium possesses extracellular DNA that contributes to biofilm formation, structural integrity, and tolerance to antibiotics. PLoS One 10:e0128772. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Sambandan D et al (2013) Keto-mycolic acid-dependent pellicle formation confers tolerance to drug-sensitive Mycobacterium tuberculosis. MBio 4:e00222-00213. CrossRefGoogle Scholar
  85. Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Senadheera D, Cvitkovitch DG (2008) Quorum sensing and biofilm formation by Streptococcus mutans. Adv Exp Med Biol 631:178–188. CrossRefPubMedGoogle Scholar
  87. Serra DO, Richter AM, Klauck G, Mika F, Hengge R (2013) Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBio 4:e00103-00113. CrossRefGoogle Scholar
  88. Silva CL, Ekizlerian SM, Fazioli RA (1985) Role of cord factor in the modulation of infection caused by mycobacteria. Am J Pathol 118:238–247PubMedPubMedCentralGoogle Scholar
  89. Simoes LC, Simoes M, Vieira MJ (2008) Intergeneric coaggregation among drinking water bacteria: evidence of a role for Acinetobacter calcoaceticus as a bridging bacterium. Appl Environ Microbiol 74:1259–1263. CrossRefPubMedGoogle Scholar
  90. Steed KA, Falkinham JO 3rd (2006) Effect of growth in biofilms on chlorine susceptibility of Mycobacterium avium and Mycobacterium intracellulare. Appl Environ Microbiol 72:4007–4011. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209CrossRefPubMedGoogle Scholar
  92. Stout JE, Koh WJ, Yew WW (2016) Update on pulmonary disease due to non-tuberculous mycobacteria. Int J Infect Dis 45:123–134. CrossRefPubMedGoogle Scholar
  93. Sugita Y, Ishii N, Katsuno M, Yamada R, Nakajima H (2000) Familial cluster of cutaneous Mycobacterium avium infection resulting from use of a circulating, constantly heated bath water system. Br J Dermatol 142:789–793CrossRefPubMedGoogle Scholar
  94. Takayama K, Wang C, Besra GS (2005) Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev 18:81–101CrossRefPubMedPubMedCentralGoogle Scholar
  95. Tsai SH, Lai HC, Hu ST (2015) Subinhibitory doses of aminoglycoside antibiotics induce changes in the phenotype of Mycobacterium abscessus. Antimicrob Agents Chemother 59:6161–6169. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, Ghigo JM (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103:12558–12563. CrossRefPubMedGoogle Scholar
  97. Van Acker H, Van Dijck P, Coenye T (2014) Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22(6):326–333. CrossRefPubMedGoogle Scholar
  98. van Ingen J, Boeree MJ, Dekhuijzen PN, van Soolingen D (2009) Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect 15:888–893. CrossRefPubMedGoogle Scholar
  99. von Ohle C, Gieseke A, Nistico L, Decker EM, DeBeer D, Stoodley P (2010) Real-time microsensor measurement of local metabolic activities in ex vivo dental biofilms exposed to sucrose and treated with chlorhexidine. Appl Environ Microbiol 76:2326–2334. CrossRefGoogle Scholar
  100. Waters CM, Lu W, Rabinowitz JD, Bassler BL (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190:2527–2536. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Werner E et al (2004) Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70:6188–6196. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Whiley H, Keegan A, Giglio S, Bentham R (2012) Mycobacterium avium complex – the role of potable water in disease transmission. J Appl Microbiol 113:223–232. CrossRefPubMedGoogle Scholar
  103. WHO (2012) The burden of diseases caused by TB Global Tuberculosis Report:8–28Google Scholar
  104. Williams MM, Santo Domingo JW, Meckes MC (2005) Population diversity in model potable water biofilms receiving chlorine or chloramine residual. Biofouling 21:279–288. CrossRefPubMedGoogle Scholar
  105. Wimpenny J, Manz W, Szewzyk U (2000) Heterogeneity in biofilms. FEMS Microbiol Rev 24:661–671CrossRefGoogle Scholar
  106. Yamada M, Ikegami A, Kuramitsu HK (2005) Synergistic biofilm formation by Treponema denticola and Porphyromonas gingivalis. FEMS Microbiol Lett 250:271–277. CrossRefPubMedGoogle Scholar
  107. Yamazaki Y et al (2006a) The ability to form biofilm influences Mycobacterium avium invasion and translocation of bronchial epithelial cells. Cell Microbiol 8:806–814. CrossRefPubMedGoogle Scholar
  108. Yamazaki Y, Danelishvili L, Wu M, Macnab M, Bermudez LE (2006b) Mycobacterium avium genes associated with the ability to form a biofilm. Appl Environ Microbiol 72:819–825. CrossRefPubMedPubMedCentralGoogle Scholar
  109. Yang Y, Thomas J, Li Y, Vilcheze C, Derbyshire KM, Jacobs WR Jr, Ojha AK (2017) Defining a temporal order of genetic requirements for development of mycobacterial biofilms. Mol Microbiol 105:794–809. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Yotsu RR, Murase C, Sugawara M, Suzuki K, Nakanaga K, Ishii N, Asiedu K (2015) Revisiting Buruli ulcer. J Dermatol 42:1033–1041. CrossRefPubMedGoogle Scholar
  111. Zobell CE (1943) The effect of solid surfaces upon bacterial activity. J Bacteriol 46:39–56PubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.NY State Department of HealthWadsworth CenterNew YorkUSA
  2. 2.Department of Biomedical SciencesUniversity at AlbanyNew YorkUSA

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