Role of multicellular aggregates in biofilm formation

mBio

Volumn 7, Issue 2, 2016, Pages

  Kragh, Kasper N ^a   Hutchison, Jaime B ^c   Melaugh, Gavin ^d   Rodesney, Chris ^c   Roberts, Aled E L ^e   Irie, Yasuhiko ^f   Jensen, Peter Ø ^b   Diggle, Stephen P ^e   Allen, Rosalind J ^d   Gordon, Vernita ^c,g   Bjarnsholt, Thomas ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c University of Texas at Austin   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f University of Bath   (United Kingdom)

^g UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOFILM; CELL ADHESION; CELL AGGREGATION; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; IMMUNE RESPONSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PSEUDOMONAS AERUGINOSA; COMPUTER SIMULATION; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY;

BIOFILMS; CELL ADHESION; COMPUTER SIMULATION; PSEUDOMONAS AERUGINOSA;

EID: 84965137983     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00237-16     Document Type: Article

References (48)

1. Costerton JW, Lewandowski Z, DeBeer D, Caldwell D, Korber D, James G. 1994. Biofilms, the customized microniche. J Bacteriol 176:2137–2142.
2. Lenz AP, Williamson KS, Pitts B, Stewart PS, Franklin MJ. 2008. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74:4463-4471. http://dx.doi.org/10.1128/AEM.00710-08.
3. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890. http://dx.doi.org/10.3201/eid0809.020063.
4. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210. http://dx.doi.org/10.1038/nrmicro1838.
5. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu Rev Microbiol 49:711–745. http://dx.doi.org/10.1146/annurev.mi.49.100195.003431.
6. Davey ME, O’Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867. http://dx.doi.org/10.1128/MMBR.64.4.847-867.2000.
7. 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. http://dx.doi.org/10.1099/mic.0.27536-0.
8. Stoodley P, Hall-Stoodley L, Lappin-Scott HM. 2001. Detachment, surface migration, and other dynamic behavior in bacterial biofilms revealed by digital time-lapse imaging. Methods Enzymol 337:306–319.
9. Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS. 2004. Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microbiol 70:7418–7425. http://dx.doi.org/10.1128/AEM.70.12.7418-7425.2004.
10. Bar-Zeev E, Berman-Frank I, Girshevitz O, Berman T. 2012. Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles. Proc Natl Acad Sci U S A 109:9119–9124. http://dx.doi.org/10.1073/pnas.1203708109.
11. Häussler S, Ziegler I, Löttel A, von Götz F, Rohde M, Wehmhöhner D, Saravanamuthu S, Tümmler B, Steinmetz I. 2003. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52:295–301. http://dx.doi.org/10.1099/jmm.0.05069-0.
12. Déziel E, Comeau Y, Villemur R. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183:1195–1204. http://dx.doi.org/10.1128/JB.183.4.1195-1204.2001.
13. Schleheck D, Barraud N, Klebensberger J, Webb JS, McDougald D, Rice SA, Kjelleberg S. 2009. Pseudomonas aeruginosa PAO1 preferentially grows as aggregates in liquid batch cultures and disperses upon starvation. PLoS One 4:e5513. http://dx.doi.org/10.1371/journal.pone.0005513.
14. Melaugh G, Hutchison J, Kragh KN, Irie Y, Roberts AEL, Bjarnsholt T, Diggle SP, Gordon VD, Allen RJ. 2015. Shaping the growth behaviour of bacterial aggregates in biofilms. arXiv arXiv:1506.08168v2. [physics. bio-ph]
15. Alhede M, Kragh KN, Qvortrup K, Allesen-Holm M, van Gennip M, Christensen LD, Jensen PØ, Nielsen AK, Parsek M, Wozniak D, Molin S, Tolker-Nielsen T, Høiby N, Givskov M, Bjarnsholt T. 2011. Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One 6:e27943. http://dx.doi.org/10.1371/journal.pone.0027943.
16. Wessel AK, Arshad TA, Fitzpatrick M, Connell JL, Bonnecaze RT, Shear JB, Whiteley M. 2014. Oxygen limitation within a bacterial aggregate. mBio 5:e00992-14. http://dx.doi.org/10.1128/mBio.00992-14.
17. Hamilton WD. 1964. The genetical evolution of social behaviour. I. J Theor Biol 7:1–16. http://dx.doi.org/10.1016/0022-5193(64)90038-4.
18. West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol 4:597-607. http://dx.doi.org/10.1038/nrmicro1461.
19. Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci U S A 104:876–881. http://dx.doi.org/10.1073/pnas.0607651104.
20. Bjarnsholt T, Jensen PØ, Fiandaca MJ, Pedersen J, Hansen CR, Andersen CB, Pressler T, Givskov M, Høiby N. 2009. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547–558. http://dx.doi.org/10.1002/ppul.21011.
21. Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sørensen SR, Moser C, Kühl M, Jensen PØ, Høiby N. 2013. The in vivo biofilm. Trends Microbiol 21:466–474. http://dx.doi.org/10.1016/j.tim.2013.06.002.
22. Hall-Stoodley L, Stoodley P. 2005. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 13:7–10. http://dx.doi.org/10.1016/j.tim.2004.11.004.
23. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332. http://dx.doi.org/10.1016/j.ijantimicag.2009.12.011.
24. Bester E, Wolfaardt GM, Aznaveh NB, Greener J. 2013. Biofilms’ role in planktonic cell proliferation. Int J Mol Sci 14:21965–21982. http://dx.doi.org/10.3390/ijms141121965.
25. 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. http://dx.doi.org/10.1038/nrmicro2695.
26. Fazli M, Bjarnsholt T, Kirketerp-Møller K, Jørgensen B, Andersen AS, Krogfelt KA, Givskov M, Tolker-Nielsen T. 2009. Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47:4084-4089. http://dx.doi.org/10.1128/JCM.01395-09.
27. Kragh KN, Alhede M, Jensen PØ, Moser C, Scheike T, Jacobsen CS, Seier S, Eickhardt-Sørensen SR, Trøstrup H, Christoffersen L, Hougen H-P, Rickelt LF, Kühl M, Høiby N, Bjarnsholt T. 2014. Polymorphonuclear leukocytes restrict the growth of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Infect Immun 82:4477-4486. http://dx.doi.org/10.1128/IAI.01969-14.
28. Homøe P, Bjarnsholt T, Wessman M, Sørensen HCF, Johansen HK. 2009. Morphological evidence of biofilm formation in Greenlanders with chronic suppurative otitis media. Eur Arch Otorhinolaryngol 266: 1533–1538. http://dx.doi.org/10.1007/s00405-009-0940-9.
29. Hutchison JB, Rodesney CA, Kaushik KS, Le HH, Hurwitz DA, Irie Y, Gordon VD. 2014. Single-cell control of initial spatial structure in biofilm development using laser trapping. Langmuir 30:4522-4530. http://dx.doi.org/10.1021/la500128y.
30. Tolker-Nielsen T, Sternberg C. 2011. Growing and analyzing biofilms in flow chambers. Curr Protoc Microbiol Chapter 1:Unit 1B.2. http://dx.doi.org/10.1002/9780471729259.mc01b02s21.
31. Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jørgensen A, Molin S, Tolker-Nielsen T. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524. http://dx.doi.org/10.1046/j.1365-2958.2003.03525.x.
32. Bjarnsholt T, Jensen PØ, Burmølle M, Hentzer M, Haagensen JAJ, Hougen HP, Calum H, Madsen KG, Moser C, Molin S, Høiby N, Givskov M. 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383. http://dx.doi.org/10.1099/mic.0.27463-0.
33. Heydorn A, Givskov M, Hentzer M, Ersbøll BK, Sternberg C, Nielsen AT, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395–2407. http://dx.doi.org/10.1099/00221287-146-10-2395.
34. Orr HA. 2009. Fitness and its role in evolutionary genetics. Nat Rev Genet 10:531–539. http://dx.doi.org/10.1038/nrg2603.
35. Lardon LA, Merkey BV, Martins S, Dötsch A, Picioreanu C, Kreft J-U, Smets BF. 2011. iDynoMiCS: next-generation individual-based modelling of biofilms. Environ Microbiol 13:2416–2434. http://dx.doi.org/10.1111/j.1462-2920.2011.02414.x.
36. Hermanowicz SW. 2001. A simple 2D biofilm model yields a variety of morphological features. Math Biosci 169:1–14. http://dx.doi.org/10.1016/S0025-5564(00)00049-3.
37. Stewart PS. 2003. Diffusion in biofilms. J Bacteriol 185:1485–1491. http://dx.doi.org/10.1128/JB.185.5.1485-1491.2003.
38. Dockery J, Klapper I. 2001. Finger formation in biofilm layers. SIAM J Appl Math 62:853–869.
39. Nadell CD, Foster KR, Xavier JB. 2010. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 6:e1000716. http://dx.doi.org/10.1371/journal.pcbi.1000716.
40. Xavier JB, Picioreanu C, van Loosdrecht MCM. 2005. A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ Microbiol 7:1085–1103. http://dx.doi.org/10.1111/j.1462 -2920.2005.00787.x.
41. Picioreanu C, Kreft J-U, van Loosdrecht MCM. 2004. Particle-based multidimensional multispecies biofilm model. Appl Environ Microbiol 70:3024–3040. http://dx.doi.org/10.1128/AEM.70.5.3024-3040.2004.
42. Estrela S, Brown SP. 2013. Metabolic and demographic feedbacks shape the emergent spatial structure and function of microbial communities. PLoS Comput Biol 9:e1003398. http://dx.doi.org/10.1371/journal.pcbi.1003398.
43. Kreft J-U, Picioreanu C, Wimpenny JWT, van Loosdrecht MCM. 2001. Individual-based modelling of biofilms. Microbiology 147:2897–2912. http://dx.doi.org/10.1099/00221287-147-11-2897.
44. Battino R, Rettich TR, Tominaga T. 1983. The solubility of oxygen and ozone in liquids. J Phys Chem Ref Data 12:163–178.
45. Beyenal H, Chen SN, Lewandowski Z. 2003. The double substrate growth kinetics of Pseudomonas aeruginosa. Enzyme Microb Technol 32:92–98. http://dx.doi.org/10.1016/S0141-0229(02)00246-6.
46. Characklis WG, Marshall KC. 1990. Biofilms. Wiley Interscience, New York, NY.
47. Alpkvist E, Picioreanu C, van Loosdrecht MCM, Heyden A. 2006. Three-dimensional biofilm model with individual cells and continuum EPS matrix. Biotechnol Bioeng 94:961–979. http://dx.doi.org/10.1002/bit.20917.
48. Picioreanu C, van Loosdrecht MCM, Heijnen JJ. 1998. Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58:101–116. http://dx.doi.org/10.1002/(SICI)1097-0290(19980405)58:1_101::AID-BIT11_3.0.CO;2-M.