Korean Journal of Microbiology (미생물학회지)

The Microbiological Society of Korea (한국미생물학회)
권호 표지
DOI QR코드

DOI QR Code

Biofilm modeling systems

생물막 모델 시스템

  • Kim, Soo-Kyoung (Department of Pharmacy, College of Pharmacy, Pusan National University) ;
  • Lee, Joon-Hee (Department of Pharmacy, College of Pharmacy, Pusan National University)
  • 김수경 (부산대학교 약학대학 약학과) ;
  • 이준희 (부산대학교 약학대학 약학과)
  • Received : 2016.05.09
  • Accepted : 2016.06.01
  • Published : 2016.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Biofilms are considered a complexly structured community of microorganisms derived from their attached growth to abiotic and biotic surfaces. In human life, they mediate serious infections and cause many problems in civil and industrial facilities. While it is of huge interest for scientists to understand biofilms, it has been very hard to directly analyze the various biofilms in nature. A variety of biofilm models have been suggested for laboratory-scale biofilm formation and many methods based on these models are widely used for the biofilm researches. These biofilm models mimic characteristics of environmental biofilms with different advantages and disadvantages. In this review, we will introduce these currently used biofilm model systems and explain their relative merits.

생물막은 미생물들의 표면 부착 성장으로부터 유래된 복잡하게 구조화된 미생물들의 군집이다. 인간의 삶속에서 생물막은 다양한 감염을 매개하고 여러 사회, 문화, 산업 시설물들에서 많은 문제를 일으킨다. 생물막에 대한 이해가 과학자들에게 큰 관심을 끌고 있기는 하지만, 자연계에 존재하는 다양한 생물막을 직접 연구하는 것은 매우 어렵다. 따라서 다양한 연구실에서 생물막을 형성하기 위한 다양한 모델 시스템들이 제안되어 왔으며, 이들 모델에 기반한 많은 생물막 연구 방법들이 실제 생물막 연구에 쓰이고 있다. 이러한 생물막 모델들은 실제 환경속의 생물막들의 특징들을 모사하고 있지만 각기 나름대로의 장단점들을 가지고 있다. 본 리뷰에서는 현재 사용되고 있는 생물막 모델 시스템들을 소개하고, 그들의 장단점들을 설명하고자 한다.

Keywords

References

  1. Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I., and Dewhirst, F.E. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43, 5721-5732. https://doi.org/10.1128/JCM.43.11.5721-5732.2005
  2. Adetunji, V.O. and Odetokun, I.A. 2012. Assessment of biofilm in E. coli O157:H7 and Salmonella strains: Influence of cultural conditions. Am. J. Food Technol. 7, 582-595. https://doi.org/10.3923/ajft.2012.582.595
  3. Al-Ahmad, A., Wunder, A., Auschill, T.M., Follo, M., Braun, G., Hellwig, E., and Arweiler, N.B. 2007. The in vivo dynamics of Streptococcus spp., Actinomyces naeslundii, Fusobacterium nucleatum and Veillonella spp. in dental plaque biofilm as analysed by fivecolour multiplex fluorescence in situ hybridization. J. Med. Microbiol. 56, 681-687. https://doi.org/10.1099/jmm.0.47094-0
  4. Ali, A., Khambaty, F., and Diachenko, G. 2006. Investigating the suitability of the Calgary Biofilm Device for assessing the antimicrobial efficacy of new agents. Bioresour. Technol. 97, 1887-1893. https://doi.org/10.1016/j.biortech.2005.08.025
  5. Allesen-Holm, M., Barken, K.B., Yang, L., Klausen, M., Webb, J.S., Kjelleberg, S., Molin, S., Givskov, M., and Tolker-Nielsen, T. 2006. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114-1128. https://doi.org/10.1111/j.1365-2958.2005.05008.x
  6. Amorena, B., Gracia, E., Monzon, M., Leiva, J., Oteiza, C., Perez, M., Alabart, J.L., and Hernandez-Yago, J. 1999. Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J. Antimicrob. Chemother. 44, 43-55. https://doi.org/10.1093/jac/44.1.43
  7. Anderl, J.N., Franklin, M.J., and Stewart, P.S. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44, 1818-1824. https://doi.org/10.1128/AAC.44.7.1818-1824.2000
  8. Anderson, G.G., Palermo, J.J., Schilling, J.D., Roth, R., Heuser, J., and Hultgren, S.J. 2003. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301, 105-107. https://doi.org/10.1126/science.1084550
  9. Benoit, M.R., Conant, C.G., Ionescu-Zanetti, C., Schwarz, M., and Matin, A. 2010. New device for high-throughput viability screening of flow biofilms. Appl. Environ. Microbiol. 76, 4136-4142. https://doi.org/10.1128/AEM.03065-09
  10. Bjarnsholt, T., Jensen, P.O., Fiandaca, M.J., Pedersen, J., Hansen, C.R., Andersen, C.B., Pressler, T., Givskov, M., and Hoiby, N. 2009. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 44, 547-558. https://doi.org/10.1002/ppul.21011
  11. Boulos, L., Prevost, M., Barbeau, B., Coallier, J., and Desjardins, R. 1999. LIVE/DEAD BacLight : application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37, 77-86. https://doi.org/10.1016/S0167-7012(99)00048-2
  12. Buckingham-Meyer, K., Goeres, D.M., and Hamilton, M.A. 2007. Comparative evaluation of biofilm disinfectant efficacy tests. J. Microbiol. Methods 70, 236-244. https://doi.org/10.1016/j.mimet.2007.04.010
  13. Buckingham-Meyer, K., Heersink, J., Pitts, B., Rayner, J., and Werner, E. 2003. Alternative biofilm growth reactors. In Hamilton, M., Heersink, J., Buckingham-Meyer, K., and Goeres, D. (eds.), The biofilm laboratory: Step-by-step protocols for experimental design, analysis, and data interpretation, pp. 31-51. Cytergy Publishing, Bozeman, USA.
  14. Chalfie, M., Tu, Y., Euskirchen, G., and Ward, W.W. 1994. Green fluorescent protein as a marker for gene expression. Science 263, 802-805. https://doi.org/10.1126/science.8303295
  15. Chandra, J., Kuhn, D.M., Mukherjee, P.K., Hoyer, L.L., McCormick, T., and Ghannoum, M.A. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. J. Bacteriol. 183, 5385-5394. https://doi.org/10.1128/JB.183.18.5385-5394.2001
  16. Cloete, T.E., Brozel, V.S., and Von Holy, A. 1992. Practical aspects of biofouling control in industrial water systems. Int. Biodeterior. Biodegrad. 29, 299-341. https://doi.org/10.1016/0964-8305(92)90050-X
  17. Colvin, K.M., Gordon, V.D., Murakami, K., Borlee, B.R., Wozniak, D.J., Wong, G.C.L., and Parsek, M.R. 2011. The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog. 7, e1001264. https://doi.org/10.1371/journal.ppat.1001264
  18. Conant, C.G., Schwartz, M.A., and Ionescu-Zanetti, C. 2010. Well plate-coupled microfluidic devices designed for facile image-based cell adhesion and transmigration assays. J. Biomol. Screen 15, 102-106. https://doi.org/10.1177/1087057109353789
  19. De La Fuente, L., Montanes, E., Meng, Y., Li, Y., Burr, T.J., Hoch, H.C., and Wu, M. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 73, 2690-2696. https://doi.org/10.1128/AEM.02649-06
  20. De Prijck, K., De Smet, N., Rymarczyk-Machal, M., Van Driessche, G., Devreese, B., Coenye, T., Schacht, E., and Nelis, H.J. 2010. Candida albicans biofilm formation on peptide functionalized polydimethylsiloxane. Biofouling 26, 269-275. https://doi.org/10.1080/08927010903501908
  21. De Prijck, K., Nelis, H., and Coenye, T. 2007. Efficacy of silver-releasing rubber for the prevention of Pseudomonas aeruginosa biofilm formation in water. Biofouling 23, 405-411. https://doi.org/10.1080/08927010701647861
  22. Diaz, P.I., Chalmers, N.I., Rickard, A.H., Kong, C., Milburn, C.L., Palmer, R.J.Jr., and Kolenbrander, P.E. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72, 2837-2848. https://doi.org/10.1128/AEM.72.4.2837-2848.2006
  23. Dietrich, L.E., Price-Whelan, A., Petersen, A., Whiteley, M., and Newman, D.K. 2006. The phenazine pyocyanin is a terminal signaling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61, 1308-1321. https://doi.org/10.1111/j.1365-2958.2006.05306.x
  24. Dige, I., Nilsson, H., Kilian, M., and Nyvad, B. 2007. In situ identification of streptococci and other bacteria in initial dental biofilm by confocal laser scanning microscopy and fluorescence in situ hybridization. Eur. J. Oral Sci. 115, 459-467. https://doi.org/10.1111/j.1600-0722.2007.00494.x
  25. Dige, I., Raarup, M.K., Nyengaard, J.R., Kilian, M., and Nyvad, B. 2009. Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155, 2116-2126. https://doi.org/10.1099/mic.0.027706-0
  26. Donlan, R.M. and Costerton, J.W. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167-193. https://doi.org/10.1128/CMR.15.2.167-193.2002
  27. Donlan, R.M., Piede, J.A., Heyes, C.D., Sanii, L., Murga, R., Edmonds, P., El-Sayed, I., and El-Sayed, M.A. 2004. Model system for growing and quantifying Streptococcus pneumoniae biofilms in situ and in real time. Appl. Environ. Microbiol. 708, 4980-4988.
  28. Elkins, J.G., Hassett, D.J., Stewart, P.S., Schweizer, H.P., and McDermott, T.R. 1999. Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65, 4594-4600.
  29. Eun, Y.J. and Weibel, D.B. 2009. Fabrication of microbial biofilm arrays by geometric control of cell adhesion. Langmuir 25, 4643-4654. https://doi.org/10.1021/la803985a
  30. Freitas, A.I., Vasconcelos, C., Vilanova, M., and Cerca, N. 2013. Optimization of an automatic counting system for the quantification of Staphylococcus epidermidis cells in biofilms. J. Basic Microbiol. 54, 750-757.
  31. Friedman, L. and Kolter, R. 2004a. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51, 675-690.
  32. Friedman, L. and Kolter, R. 2004b. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186, 4457-4465. https://doi.org/10.1128/JB.186.14.4457-4465.2004
  33. Fux, C.A., Costerton, J.W., Stewart, P.S., and Stoodley, P. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13, 34-40. https://doi.org/10.1016/j.tim.2004.11.010
  34. Goeres, D.M., Hamilton, M.A., Beck, N.A., Buckingham-Meyer, K., Hilyard, J.D., Loetterle, L.R., Lorenz, L.A., Walker, D.K., and Stewart, P.S. 2009. A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nat. Protoc. 4, 783-788. https://doi.org/10.1038/nprot.2009.59
  35. Goeres, D.M., Loetterle, L.R., Hamilton, M.A., Murga, R., Kirby, D.W., and Donlan, R.M. 2005. Statistical assessment of a laboratory method for growing biofilms. Microbiology 151, 757-762. https://doi.org/10.1099/mic.0.27709-0
  36. Hadi, R., Vickery, K., Deva, A., and Charlton, T. 2010. Biofilmremoval bymedical device cleaners: comparison of two bioreactor detection assays. J. Hosp. Infect. 74, 160-167. https://doi.org/10.1016/j.jhin.2009.10.023
  37. 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. https://doi.org/10.1038/nrmicro821
  38. Hannig, C., Hannig, M., Rehmer, O., Braun, G., Hellwig, E., and Al-Ahmad, A. 2007. Fluorescence microscopic visualization and quantification of initial bacterial colonization on enamel in situ. Arch. Oral Biol. 52, 1048-1056. https://doi.org/10.1016/j.archoralbio.2007.05.006
  39. Hans-Curt, F. and Jost, W. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8, 623-633. https://doi.org/10.1038/nrmicro2415
  40. Heersink, J. and Goeres, D. 2003. Reactor design considerations. In Hamilton, M., Heersink, J., Buckingham-Meyer, K., and Goeres, D. (eds.), The Biofilm Laboratory: Step-by-step Protocols for Experimental Design, Analysis, and Data Interpretation, pp. 13-15. Cytergy Publishing, Bozeman, USA.
  41. Heilmann, C., Gerke, C., Perdreau-Remington, F., and Gotz, F. 1996. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun. 64, 277-282.
  42. Heydorn, A., Ersboll, B.K., Hentzer, M., Parsek, M.R., Givskov, M., and Molin, S. 2000a. Experimental reproducibility in flowchamber biofilms. Microbiology 146, 2409-2415. https://doi.org/10.1099/00221287-146-10-2409
  43. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersboll, B.K., and Molin, S. 2000b. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146, 2395-2407. https://doi.org/10.1099/00221287-146-10-2395
  44. Im, S.J. 2011. Differential regulation of genes in Pseudomonas aeruginosa biofilm depending on spatial structure. Master thesis, Pusan National University.
  45. Janakiraman, V., Englert, D., Jayaraman, A., and Baskaran, H. 2009. Modeling growth and quorum sensing in biofilms grown in microfluidic chambers. Ann. Biomed. Eng. 37, 1206-1216. https://doi.org/10.1007/s10439-009-9671-8
  46. Jung, Y.G., Choi, J., Kim, S.K., Lee, J.H., and Kwon, S. 2015. Embedded biofilm, a ne biofilm model based on the embedded growth of bacteria. Appl. Environ. Microbiol. 81, 211-219. https://doi.org/10.1128/AEM.02311-14
  47. Kim, J., Park, H.J., Lee, J.H., Hahn, J.S., Gu, M.B., and Yoon, J. 2009. Differential effect of chlorine on the oxidative stress generation in dormant and active cells within colony biofilm. Water Res. 43, 5252-5859. https://doi.org/10.1016/j.watres.2009.08.044
  48. Krom, B.P., Cohen, J.B., McElhaney Feser, G.E., and Cihlar, R.L. 2007. Optimized candida biofilm microtiter assay. J. Microbiol. Methods 68, 421-423. https://doi.org/10.1016/j.mimet.2006.08.003
  49. Kwok, W.K., Picioreanu, C., Ong, S.L., van Loosdrecht, M.C.M., Ng, W.J., and Heijnen, J.J. 1998. Influence of biomass production and detachment force on biofilm structures in a biofilm airlift suspension reactor. Biotechnol. Bioeng. 58, 400-407. https://doi.org/10.1002/(SICI)1097-0290(19980520)58:4<400::AID-BIT7>3.0.CO;2-N
  50. Lambertsen, L., Sternberg, C., and Molin, S. 2004. Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ. Microbiol. 6, 726-732. https://doi.org/10.1111/j.1462-2920.2004.00605.x
  51. Lawrence, J.R., Neu, T.R., and Swerhone, G.D.W. 1998. Application of multiple parameter imaging for the quantification of algal, bacterial and exopolymer components of microbial biofilms. J. Microbiol. Methods 32, 253-261. https://doi.org/10.1016/S0167-7012(98)00027-X
  52. Lazarova, V.Z., Capdeville, B., and Nikolov, L. 1992. Biofilm performance of a fluidized bed biofilm reactor for drinking water denitrification. Water Sci. Technol. 26, 555-666.
  53. Lee, J.H., Kaplan, J.B., and Lee, W.Y. 2008. Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms. Biomed. Microdevices 10, 489-498. https://doi.org/10.1007/s10544-007-9157-0
  54. Mittelman, M.W., Nivens, D.E., Low, C., and White, D.C. 1990. Differential adhesion, activity and carbohydrate: protein ratios of Pseudomonas atlantica monocultures attaching to stainless steel in a linear shear gradient. Microb. Ecol. 19, 269-278. https://doi.org/10.1007/BF02017171
  55. Moller, S., Korber, D.R., Wolfaardt, G.M., Molin, S., and Caldwell, D.E. 1997. Impact of nutrient composition on a degradative biofilm community. Appl. Environ. Microbiol. 63, 2432-2438.
  56. Niu, C. and Gilbert, E.S. 2004. Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl. Environ. Microbiol. 70, 6951-6956. https://doi.org/10.1128/AEM.70.12.6951-6956.2004
  57. O'Toole, G.A. 2011. Microtiter dish biofilm formation assay. J. Vis. Exp. 30, 2437.
  58. O'Toole, G.A. and Kolter, R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295-304. https://doi.org/10.1046/j.1365-2958.1998.01062.x
  59. O'Toole, G., Kaplan, H.B., and Kolter, R. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49-79. https://doi.org/10.1146/annurev.micro.54.1.49
  60. Palmer, R.J.Jr. 2010. Supragingival and subgingival plaque: paradigm of biofilms. Compend. Contin. Educ. Dent. 31, 104-106.
  61. Pamp, S.J., Sternberg, C., and Tolker-Nielsen, T. 2009. Insight into the microbial multicellular lifestyle via flow-cell technology and confocal microscopy. Cytometry A 75, 90-103.
  62. Peeters, E., Nelis, H.J., and Coenye, T. 2008. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods 72, 157-165. https://doi.org/10.1016/j.mimet.2007.11.010
  63. Pitts, B., Hamilton, M.A., Zelver, N., and Stewart, P.S. 2003. A microtiter-plate screening method for biofilm disinfection and removal. J. Microbiol. Methods 54, 269-276. https://doi.org/10.1016/S0167-7012(03)00034-4
  64. Quave, C.L., Plano, L.R.W., Pantuso, T., and Bennett, B.C. 2008. Effects of extracts from Italian medicinal plants on planktonic growth, biofilm formation and adherence of methicillin-resistant Staphylococcus aureus. J. Ethnopharmacol. 118, 418-428. https://doi.org/10.1016/j.jep.2008.05.005
  65. Rice, K.C., Mann, E.E., Enders, J.L., Weiss, E.C., Cassat, J.E., Smeltzer, M.S., and Bayles, K.W. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104, 8113-8118. https://doi.org/10.1073/pnas.0610226104
  66. Richter, L., Stepper, C., Mak, A., Reinthaler, A., Heer, R., Kast, M., Bruckl, H., and Ertl, P. 2007. Development of a microfluidic biochip for online monitoring of fungal biofilm dynamics. Lab Chip 7, 1723-1731. https://doi.org/10.1039/b708236c
  67. Schaudinn, C., Carr, G., Gorur, A., Jaramillo, D., Costerton, J.W., and Webster, P. 2009. Imaging of endodontic biofilms by combined microscopy (FISH/cLSM - SEM). J. Microsc. 235, 124-127. https://doi.org/10.1111/j.1365-2818.2009.03201.x
  68. Shapiro, J.A. 1984. The use of Mudlac transposons as tools for vital staining to visualize clonal and non-clonal patterns of organization in bacterial growth on agar surfaces. J. Gen. Microbiol. 130, 1169-1181.
  69. Shen, Y., Stojicic, S., and Haapasalo, M. 2010. Bacterial viability in starved and revitalized biofilms: comparison of viability staining and direct culture. J. Endod. 36, 1820-1823. https://doi.org/10.1016/j.joen.2010.08.029
  70. Stepanovic, S., Djukic, V., Djordjevic, V., and Djukic, S. 2003. Influence of the incubation atmosphere on the production of biofilm by staphylococci. Clin. Microbiol. Infect. 9, 955-958. https://doi.org/10.1046/j.1469-0691.2003.00676.x
  71. Sternberg, C., Christensen, B.B., Johansen, T., Toftgaard Nielsen, A., Andersen, J.B., Givskov, M., and Molin, S. 1999. Distribution of bacterial growth activity in flow-chamber biofilms. Appl. Environ. Microbiol. 65, 4108-4117.
  72. Stewart, P.S. and Franklin, M.J. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6, 199-210. https://doi.org/10.1038/nrmicro1838
  73. Stewart, P.S., Murga, R., Srinivasan, R., and de Beer, D. 1995. Biofilm structural heterogenecity visualized by three microscopic methods. Water Res. 8, 2006-2009.
  74. 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. https://doi.org/10.1046/j.1365-2672.2001.01413.x
  75. Strathmann, M., Wingender, J., and Flemming, H.C. 2002. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. J. Microbiol. Methods 50, 237-248. https://doi.org/10.1016/S0167-7012(02)00032-5
  76. Van den Driessche, F., Rigole, P., Brackman, G., and Coenye, T. 2014. Optimization of resazurin-based viability staining for quantification of microbial biofilms. J. Microbiol. Methods 98, 31-34. https://doi.org/10.1016/j.mimet.2013.12.011
  77. Van Loosdrecht, M.C.M., Eikelboom, D., Gjaltema, A., Mulder, A., Tijhuis, L., and Heijnen, J.J. 1995. Biofilm structures. Water Sci. Technol. 32, 35-43.
  78. Vieira, M.J., Melo, L.F., and Phinheiro, M.M. 1993. Biofilm formation: hydrodynamic effects on internal diffusion and structure. Biofouling 7, 67-80. https://doi.org/10.1080/08927019309386244
  79. Wolfaardt, G.M., Lawrence, J.R., Robarts, R.D., Caldwell, S.J., and Caldwell, D.E. 1994. Multicellular organization in a degradative biofilm community. Appl. Environ. Microbiol. 60, 434-446.
  80. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K.C., Birrer, P., Bellon, G., Berger, J., Weiss, T., et al. 2002. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109, 317-325. https://doi.org/10.1172/JCI0213870
  81. Wotton, R.S. and Preston, T.M. 2005. Surface films: areas of water bodies that are often overlooked. Bioscience 55, 137-145. https://doi.org/10.1641/0006-3568(2005)055[0137:SFAOWB]2.0.CO;2
  82. Yamamoto, K., Arai, H., Ishii, M., and Igarashi, Y. 2011. Trade-off between oxygen and iron acquisition in bacterial cells at the air-liquid interface. FEMS Microbiol. Ecol. 77, 83-94. https://doi.org/10.1111/j.1574-6941.2011.01087.x
  83. Yang, L., Haagensen, J.A.J., Jelsbak, L., Johansen, H.K., Sternberg, C., Hoiby, N., and Molin, S. 2008. In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J. Bacteriol. 190, 2767-2776. https://doi.org/10.1128/JB.01581-07
  84. Zelver, N., Hamilton, M., Pitts, B., Goeres, D., Walker, D., Sturman, P., and Heersink, J. 1999. Measuring antimicrobial effects on biofilm bacteria: from laboratory to field. Methods Enzymol. 310, 608-628. https://doi.org/10.1016/S0076-6879(99)10047-8

Cited by

  1. Effectiveness of poultry litter amendments on bacterial survival and Eimeria oocyst sporulation pp.09728988, 2018, https://doi.org/10.14202/vetworld.2018.1064-1073
  2. Preventive antimicrobial action and tissue architecture ameliorations of Bacillus subtilis in challenged broilers vol.14, pp.2, 2016, https://doi.org/10.14202/vetworld.2021.523-536