Growth dependence of conjugation explains limited plasmid invasion in biofilms: An individual-based modelling study

Environmental Microbiology

Volumn 13, Issue 9, 2011, Pages 2435-2452

  Merkey, Brian V ^a,b   Lardon, Laurent A ^b,c   Seoane, Jose M ^b   Kreft, Jan Ulrich ^d   Smets, Barth F ^b  

^a Northwestern University   (United States)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c LABORATOIRE DE BIOTECHNOLOGIE DE L ENVIRONNEMENT   (France)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM; BACTERIUM CONJUGATION; BIOFILM; BIOLOGICAL MODEL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLASMID;

BACTERIA; BIOFILMS; CONJUGATION, GENETIC; MODELS, BIOLOGICAL; PLASMIDS;

EID: 80052630416     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02535.x     Document Type: Article

References (67)

1. Andrup, L., and Andersen, K. (1999) A comparison of the kinetics of plasmid transfer in the conjugation systems encoded by the F plasmid from Escherichia coli and plasmid pCF10 from Enterococcus faecalis. Microbiology 145: 2001-2009.
2. Andrup, L., Smidt, L., Andersen, K., and Boe, L. (1998) Kinetics of conjugative transfer: a study of the plasmid pXO16 from Bacillus thuringiensis subsp. israelensis. Plasmid 40: 30-43.
3. Angles, M.L., Marshall, K.C., and Goodman, A.E. (1993) Plasmid transfer between marine bacteria in the aqueous phase and biofilms in reactor microcosms. Appl Environ Microbiol 59: 843-850.
4. Arango Pinedo, C., and Smets, B.F. (2005) Conjugal TOL transfer from Pseudomonas putida to Pseudomonas aeruginosa: effects of restriction proficiency, toxicant exposure, cell density ratios, and conjugation detection method on observed transfer efficiencies. Appl Environ Microbiol 71: 51-57.
5. Babic, A., Lindner, A.B., Vulic, M., Stewart, E.J., and Radman, M. (2008) Direct visualization of horizontal gene transfer. Science 319: 1533-1536.
6. Barkay, T., and Smets, B.F. (2005) Horizontal gene flow in microbial communities. ASM News 71: 412-419.
7. Bradley, D.E., and Williams, P.A. (1982) The TOL plasmid is naturally derepressed for transfer. J Gen Microbiol 128(12): 3019-3024.
8. Brownlie, L., Stephenson, J.R., and Cole, J.A. (1990) Effect of growth rate on plasmid maintenance by Escherichia coli HB101 (pAT153). Microbiology 136: 2471-2480.
9. Brun, R., Reichert, P., and Kuensch, H.R. (2001) Practical identifiability analysis of large environmental simulation models. Water Resour Res 37: 1015-1030.
10. Characklis, W.G., and Marshall, K.C. (1990) Biofilms. New York, USA: John Wiley & Sons.
11. 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: 2247-2255.
12. Clarke, M., Maddera, L., Harris, R.L., and Silverman, P.M. (2008) F-pili dynamics by live-cell imaging. Proc Natl Acad Sci USA 105: 17978-17981.
13. Clewlow, L.J., Cresswell, N., and Wellington, E.M.H. (1990) Mathematical model of plasmid transfer between strains of streptomycetes in soil microcosms. Appl Environ Microbiol 56: 3139-3145.
14. Dahlberg, C., Bergstrom, M., and Hermansson, M. (1998) In situ detection of high levels of horizontal plasmid transfer in marine bacterial communities. Appl Environ Microbiol 64: 2670-2675.
15. De Gelder, L., Ponciano, J.M., Joyce, P., and Top, E.M. (2007) Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153: 452-463.
16. Ebersbach, G., and Gerdes, K. (2005) Plasmid segregation mechanisms. Annu Rev Genet 39: 453-479.
17. Elsas, J.D.v., and Bailey, M.J. (2002) The ecology of transfer of mobile genetic elements. FEMS Microbiol Ecol 42: 187-197.
18. Fernandez-Astorga, A., Muela, A., Cisterna, R., Iriberri, J., and Barcina, I. (1992) Biotic and abiotic factors affecting plasmid transfer in Escherichia coli strains. Appl Environ Microbiol 58: 392-398.
19. Fox, R.E., Zhong, X., Krone, S.M., and Top, E.M. (2008) Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations. ISME J 2: 1024-1039.
20. Garcillán-Barcia, M.P., and de la Cruz, F. (2008) Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60: 1-18.
21. Grimm, V., Revilla, E., Berger, U., Jeltsch, F., Mooij, W.M., Railsback, S.F., etal. (2005) Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310: 987-991.
22. Grimm, V., Berger, U., Bastiansen, F., Eliassen, S., Ginot, V., Giske, J., etal. (2006) A standard protocol for describing individual-based and agent-based models. Ecol Model 198: 115-126.
23. Harrington, L.C., and Rogerson, A.C. (1990) The F pilus of Escherichia coli appears to support stable DNA transfer in the absence of wall-to-wall contact between cells. J Bacteriol 172: 7263-7264.
24. Hausner, M., and Wuertz, S. (1999) High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl Environ Microbiol 65: 3710-3713.
25. Hellweger, F.L., and Bucci, V. (2008) A bunch of tiny individuals - individual-based modeling for microbes. Ecol Model 220: 8-22.
26. Heuer, H., Abdo, Z., and Smalla, K. (2008) Patchy distribution of flexible genetic elements in bacterial populations mediates robustness to environmental uncertainty. FEMS Microbiol Ecol 65: 361-371.
27. Joshi, H., Dave, R., and Venugopalan, V.P. (2009) Competition triggers plasmid-mediated enhancement of substrate utilisation in Pseudomonas putida. PLoS ONE 4: e6065.
28. Knudsen, G.R., Walter, M.V., Porteous, L.A., Prince, V.J., Armstrong, J.L., and Seidler, R.J. (1988) Predictive model of conjugative plasmid transfer in the rhizosphere and phyllosphere. Appl Environ Microbiol 54: 343-347.
29. Kreft, J.-U. (2004a) Biofilms promote altruism. Microbiology 150: 2751-2760.
30. Kreft, J.-U. (2004b) Conflicts of interest in biofilms. Biofilms 1: 265-276.
31. Kreft, J.-U., Booth, G., and Wimpenny, J.W.T. (1998) BacSim, a simulator for individual-based modelling of bacterial colony growth. Microbiology 144: 3275-3287.
32. Kreft, J.-U., Picioreanu, C., Wimpenny, J.W.T., and van Loosdrecht, M.C.M. (2001) Individual-based modelling of biofilms. Microbiology 147: 2897-2912.
33. Krone, S.M., Lu, R., Fox, R., Suzuki, H., and Top, E.M. (2007) Modelling the spatial dynamics of plasmid transfer and persistence. Microbiology 153: 2803-2816.
34. Lagido, C., Wilson, I.J., Glover, L.A., and Prosser, J.I. (2003) A model for bacterial conjugal gene transfer on solid surfaces. FEMS Microbiol Ecol 44: 67-78.
35. Lardon, L., Merkey, B.V., Martins, S., Dötsch, A., Picioreanu, C., Kreft, J.-U., and Smets, B.F. (2011) iDynoMiCS: next-generation individual-based modeling of biofilms. Environ Microbiol 13: 2416-2434.
36. Levin, B.R., Stewart, F.M., and Rice, V.A. (1979) The kinetics of conjugative plasmid transmission: fit of a simple mass action model. Plasmid 2: 247-260.
37. Licht, T.R., Christensen, B.B., Krogfelt, K.A., and Molin, S. (1999) Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Environ Microbiol 145: 2615-2622.
38. Massoudieh, A., Mathew, A., Lambertini, E., Nelson, K.E., and Ginn, T.R. (2007) Horizontal gene transfer on surfaces in natural porous media: conjugation and kinetics. Vadose Zone J 6: 306-325.
39. Nadell, C.D., Xavier, J., Levin, S.A., and Foster, K.R. (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6: 171-179.
40. Nordstrom, K., and Austin, S.J. (1989) Mechanisms that contribute to the stable segregation of plasmids. Annu Rev Genet 23: 37-69.
41. Normander, B., Christensen, B.B., Molin, S., and Kroer, N. (1998) Effect of bacterial distribution and activity on conjugal gene transfer on the phylloplane of the bush bean (Phaseolus vulgaris). Appl Environ Microbiol 64: 1902-1909.
42. Pedersen, A.R., Møller, S., Molin, S., and Arvin, E. (1997) Activity of toluene-degrading Pseudomonas putida in the early growth phase of a biofilm for waste gas treatment. Biotechnol Bioeng 54: 131-141.
43. Picioreanu, C., Kreft, J.-U., and van Loosdrecht, M.C.M. (2004) Particle-based multidimensional multispecies biofilm model. Appl Environ Microbiol 70: 3024-3040.
44. Picioreanu, C., Batstone, D.J., and van Loosdrecht, M.C.M. (2005) Multidimensional modelling of anaerobic granules. Water Sci Technol 52: 501-507.
45. Picioreanu, C., Head, I.M., Katuri, K.P., van Loosdrecht, M.C.M., and Scott, K. (2007) A computational model for biofilm-based microbial fuel cells. Water Res 41: 2921-2940.
46. Prosser, J.I.C., Lagido, G., and Glover, L.A. (2000) Gene transfer in microbial biofilms. In Microbial Biosystems: New Frontiers. Bell, C.R., Brylinsky, M., and Johnson-Green, P. (eds). Kentville, NS, Canada: Atlantic Canada Society for Microbial Ecology, pp. 925-930.
47. Seoane, J.M., Sin, G., Lardon, L., Gernaey, K., and Smets, B.F. (2010) A new extant respirometric assay to estimate intrinsic growth parameters applied to study plasmid metabolic burden. Biotechnol Bioeng 105: 141-149.
48. Seoane, J.M., Yankelevich, T., Dechesne, A., Merkey, B.V., Sternberg, C., and Smets, B.F. (2011) An individual-based approach to explain plasmid invasion in bacterial populations. FEMS Microbiol Ecol 75: 17-27.
49. Shu, A.C., Wu, C.C., Chen, Y.Y., Peng, H.L., Chang, H.Y., and Yew, T.R. (2008) Evidence of DNA transfer through F-pilus channels during Escherichia coli conjugation. Langmuir 24: 6796-6802.
50. Simonsen, L. (1990) Dynamics of plasmid transfer on surfaces. J Gen Microbiol 136: 1001-1007.
51. Simonsen, L., Gordon, D.M., Stewart, F.M., and Levin, B.R. (1990) Estimating the rate of plasmid transfer: an end-point method. J Gen Microbiol 136: 2319-2325.
52. Sin, G., and Vanrolleghem, P.A. (2007) Extensions to modeling aerobic carbon degradation using combined respirometric-titrimetric measurements in view of activated sludge model calibration. Water Res 41: 3345-3358.
53. Skerker, J.M., and Berg, H.C. (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 98: 6901-6904.
54. Slater, F.R., Bailey, M.J., Tett, A.J., and Turner, S.L. (2008) Progress towards understanding the fate of plasmids in bacterial communities. FEMS Microbiol Ecol 66: 3-13.
55. Smets, B.F., Rittmann, B.E., and Stahl, D.A. (1993) The specific growth rate of Pseudomonas putida PAW1 influences the conjugal transfer rate of the TOL plasmid. Appl Environ Microbiol 59: 3430-3437.
56. Smets, B.F., Rittmann, B.E., and Stahl, D.A. (1994) Stability and conjugal transfer kinetics of a TOL plasmid in Pseudomonas aeruginosa PAO 1162. FEMS Microbiol Ecol 15: 337-350.
57. Smets, B.F., Rittmann, B.E., and Stahl, D.A. (1995) Quantification of the effect of substrate concentration on the conjugal transfer rate of the TOL plasmid in short-term batch mating experiments. Lett Appl Microbiol 21: 167-172.
58. Sørensen, S.J., Bailey, M., Hansen, L.H., Kroer, N., and Wuertz, S. (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3: 700-710.
59. Stewart, F.M., and Levin, B.R. (1977) The population biology of bacterial plasmids: a priori conditions for the existence of conjugationally transmitted factors. Genetics 87: 209-228.
60. Stewart, P.S., Camper, A.K., Handran, S.D., Huang, C., and Warnecke, M. (1997) Spatial distribution and coexistence of Klebsiella pneumoniae and Pseudomonas aeruginosa in biofilms. Microb Ecol 33: 2-10.
61. Sudarshana, P., and Knudsen, G.R. (1995) Effect of parental growth on dynamics of conjugative plasmid transfer in the pea spermosphere. Appl Environ Microbiol 61: 3136-3141.
62. Thomas, C.M., and Nielsen, K.M. (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3: 711-721.
63. Watnick, P., and Kolter, R. (2000) Biofilm, city of microbes. J Bacteriol 182: 2675-2679.
64. Williams, D.R., and Thomas, C.M. (1992) Active partitioning of bacterial plasmids. Microbiology 138: 1-16.
65. Williams, P.A., Taylor, S.D., and Gibb, L.E. (1988) Loss of the toluene-xylene catabolic genes of TOL plasmid pWWO during growth of Pseudomonas putida on benzoate is due to a selective growth advantage of 'cured' segregants. Microbiology 134: 2039-2048.
66. Xavier, J., and Foster, K.R. (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104: 876-881.
67. Xavier, J., de Kreuk, M.K., Picioreanu, C., and van Loosdrecht, M.C.M. (2007) Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ Sci Technol 41: 6410-6417.