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Biofilms as complex fluids

Published online by Cambridge University Press:  18 May 2011

James N. Wilking ,
Thomas E. Angelini ,
Agnese Seminara ,
Michael P. Brenner  and
David A. Weitz
James N. Wilking
Affiliation:
Harvard University, Cambridge, MA 02139, USA; [email protected]
Thomas E. Angelini
Affiliation:
University of Florida; [email protected]
Agnese Seminara
Affiliation:
Harvard University, Cambridge, MA 02139, USA; [email protected]
Michael P. Brenner
Affiliation:
Harvard University, Cambridge, MA 02139, USA; [email protected]
David A. Weitz
Affiliation:
Harvard University, Cambridge, MA 02139, USA; [email protected]
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Abstract

Bacterial biofilms are interface-associated colonies of bacteria embedded in an extracellular matrix that is composed primarily of polymers and proteins. They can be viewed in the context of soft matter physics: the rigid bacteria are analogous to colloids, and the extracellular matrix is a cross-linked polymer gel. This perspective is beneficial for understanding the structure, mechanics, and dynamics of the biofilm. Bacteria regulate the water content of the biofilm by controlling the composition of the extracellular matrix, and thereby controlling the mechanical properties. The mechanics of well-defined soft materials can provide insight into the mechanics of biofilms and, in particular, the viscoelasticity. Furthermore, spatial heterogeneities in gene expression create heterogeneities in polymer and surfactant production. The resulting concentration gradients generate forces within the biofilm that are relevant for biofilm spreading and survival.

Keywords

Biomaterialcolloidpolymerviscoelasticityfilm
Type
Research Article
Information
MRS Bulletin , Volume 36 , Issue 5: All together now: Integrating biofilm research across disciplines , May 2011 , pp. 385 - 391
Copyright
Copyright © Materials Research Society 2011

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References

1.Ghannoum, M., O’Toole, G.A., Eds., Microbial Biofilms, (ASM Press, Washington, DC, 2004).CrossRefGoogle Scholar
2.O’Toole, G., Kaplan, H.B., Kolter, R., Annu. Rev. Microbiol. 54, 49 (2000).CrossRefGoogle Scholar
3.Sutherland, I.W., Microbiology 147, 3 (2001).CrossRefGoogle Scholar
4.Branda, S.S., Vik, A., Friedman, L., Kolter, R., Trends Microbiol. 13, 20 (2005).CrossRefGoogle Scholar
5.Whitman, W.B., Coleman, D.C., Wiebe, W.J., Proc. Natl. Acad. Sci. U.S.A. 95, 6578 (1998).CrossRefGoogle Scholar
6.Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappinscott, H.M., Annu. Rev. Microbiol. 49, 711 (1995).CrossRefGoogle Scholar
7.Rittmann, B.E., McCarty, P.L., Environmental Biotechnology: Principles and Applications (McGraw-Hill Book Co., New York, NY, 2001).Google Scholar
8.Kolenbrander, P.E., Annu. Rev. Microbiol. 54, 413 (2000).CrossRefGoogle Scholar
9.Kolenbrander, P.E., Andersen, R.N., Blehert, D.S., Egland, P.G., Foster, J.S., Palmer, R.J., Microbiol. Mol. Biol. Rev. 66, 486 (2002).CrossRefGoogle Scholar
10.Gristina, A.G., Science 237, 1588 (1987).CrossRefGoogle Scholar
11.del Pozo, J.L., Patel, R., Clin. Pharmacol. Ther. 82, 204 (2007).CrossRefGoogle Scholar
12.Frank, K.L., del Pozo, J.L., Patel, R., Clin. Microbiol. Rev. 21, 111 (2008).CrossRefGoogle Scholar
13.Costerton, J.W., Cheng, K.J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M., Marrie, T.J., Annu. Rev. Microbiol. 41, 435 (1987).CrossRefGoogle Scholar
14.Daniels, R., Reynaert, S., Hoekstra, H., Verreth, C., Janssens, J., Braeken, K., Fauvart, M., Beullens, S., Heusdens, C., Lambrichts, I., De Vos, D.E., Vanderleyden, J., Vermant, J., Michiels, J., Proc. Natl. Acad. Sci. 103, 14965 (2006).CrossRefGoogle Scholar
15.Angelini, T.E., Roper, M., Kolter, R., Weitz, D.A., Brenner, M.P., Proc. Natl. Acad. Sci. 106, 18109 (2009).CrossRefGoogle Scholar
16.Rubinstein, M., Colby, R.H., Polymer Physics (Oxford University Press, NY, 2003).CrossRefGoogle Scholar
17.Cerf, A., Cau, J.C., Vieu, C., Dague, E., Langmuir 25, 5731 (2009).CrossRefGoogle Scholar
18.Francius, G., Domenech, O., Mingeot-Leclercq, M.P., Dufrene, Y.F., J. Bacteriol. 190, 7904 (2008).CrossRefGoogle Scholar
19.Arnoldi, M., Fritz, M., Bauerlein, E., Radmacher, M., Sackmann, E., Boulbitch, A., Phys. Rev. E 62, 1034 (2000).CrossRefGoogle Scholar
20.Kasza, K.E., Rowat, A.C., Liu, J.Y., Angelini, T.E., Brangwynne, C.P., Koenderink, G.H., Weitz, D.A., Curr. Opin. Cell Biol. 19, 101 (2007).CrossRefGoogle Scholar
21.Vlamakis, H., Aguilar, C., Losick, R., Kolter, R., Genes Dev. 22, 945 (2008).CrossRefGoogle Scholar
22.Romero, D., Aguilar, C., Losick, R., Kolter, R., Proc. Natl. Acad. Sci. U.S.A. 107, 2230 (2010).CrossRefGoogle Scholar
23.Lahaye, E., Aubry, T., Kervarec, N., Douzenel, P., Sire, O., Biomacromolecules 8, 1218 (2007).CrossRefGoogle Scholar
24.Klapper, I., Dockery, J., SIAM Rev. 52, 221 (2010).CrossRefGoogle Scholar
25.Boyd, A., Chakrabarty, A.M., Appl. Environ. Microbiol. 60, 2355 (1994).CrossRefGoogle Scholar
26.Kolodkin-Gal, I., Romero, D., Cao, S.G., Clardy, J., Kolter, R., Losick, R., Science 328, 627 (2010).CrossRefGoogle Scholar
27.Aguilar, C., Vlamakis, H., Losick, R., Kolter, R., Curr. Opin. Microbiol. 10, 638 (2007).CrossRefGoogle Scholar
28.Branda, S.S., Gonzalez-Pastor, J.E., Dervyn, E., Ehrlich, S.D., Losick, R., Kolter, R., J. Bacteriol. 186, 3970 (2004).CrossRefGoogle Scholar
29.Branda, S.S., Chu, F., Kearns, D.B., Losick, R., Kolter, R., Mol. Microbiol. 59, 1229 (2006).CrossRefGoogle Scholar
30.Kearns, D.B., Chu, F., Branda, S.S., Kolter, R., Losick, R., Mol. Microbiol. 55, 739 (2005).CrossRefGoogle Scholar
31.Danese, P.N., Pratt, L.A., Kolter, R., J. Bacteriol. 182, 3593 (2000).CrossRefGoogle Scholar
32.Pratt, L.A., Kolter, R., Mol. Microbiol. 30, 285 (1998).CrossRefGoogle Scholar
33.O’Toole, G.A., Kolter, R., Mol. Microbiol. 30, 295 (1998).CrossRefGoogle Scholar
34.Branda, S.S., Gonzalez-Pastor, J.E., Ben-Yehuda, S., Losick, R., Kolter, R., Proc. Natl. Acad. Sci. U.S.A. 98, 11621 (2001).CrossRefGoogle Scholar
35.Epstein, A., Pokroy, B., Seminara, A., Aizenberg, J., Proc. Natl. Acad. Sci. U.S.A. (2010).Google Scholar
36.Larson, R.G., The Structure and Rheology of Complex Fluids (Oxford University Press, New York City, 1999).Google Scholar
37.Characklis, W.G., Biofilm development and destruction. Final report. (Electric Power Research Institute, Palo Alto, CA, 1979).Google Scholar
38.Flemming, H.C., Schaule, G., Werkst. Korros.-Mater. Corros. 45, 29 (1994).CrossRefGoogle Scholar
39.Stoodley, P., Lewandowski, Z., Boyle, J.D., Lappin-Scott, H.M., Biotechnol. Bioeng. 65, 83 (1999).3.0.CO;2-B>CrossRefGoogle Scholar
40.Picologlou, B.F., Zelver, N., Characklis, W.G., J. Hydraulics Div., ASCE 106, 733 (1980).CrossRefGoogle Scholar
41.Yoon, S.S., Hennigan, R.F., Hilliar, G.M., Ochsner, U.A., Parvatiyar, K., Kamani, M.C., Allen, H.L., DeKievit, T.R., Gardner, P.R., Schwab, U., Rowe, J.J., Iglewski, B.H., McDermott, T.R., Mason, R.P., Wozniak, D.J., Hancock, R.E.W., Parsek, M.R., Noah, T.L., Boucher, R.C., Hassett, D.J., Dev. Cell 3, 593 (2002).CrossRefGoogle Scholar
42.de Gennes, P.-G., Scaling Concepts in Polymer Physics (Cornell University Press, Ithaca, NY, 1979).Google Scholar
43.Rogers, S.S., van der Walle, C., Waigh, T.A., Langmuir 24, 13549 (2008).CrossRefGoogle Scholar
44.Donev, A., Cisse, I., Sachs, D., Variano, E., Stillinger, F.H., Connelly, R., Torquato, S., Chaikin, P.M., Science 303, 990 (2004).CrossRefGoogle Scholar
45.Hohne, D.N., Younger, J.G., Solomon, M.J., Langmuir 25, 7743 (2009).CrossRefGoogle Scholar
46.Stoodley, P., Cargo, R., Rupp, C.J., Wilson, S., Klapper, I., J. Ind. Microbiol. Biotechnol. 29, 361 (2002).CrossRefGoogle Scholar
47.Storm, C., Pastore, J.J., MacKintosh, F.C., Lubensky, T.C., Janmey, P.A., Nature 435, 191 (2005).CrossRefGoogle Scholar
48.Matsui, H., Wagner, V.E., Hill, D.B., Schwab, U.E., Rogers, T.D., Button, B., Taylor, R.M., Superfine, R., Rubinstein, M., Iglewski, B.H., Boucher, R.C., Proc. Natl. Acad. Sci. U.S.A. 103, 18131 (2006).CrossRefGoogle Scholar
49.Mason, T.G., Weitz, D.A., Phys. Rev. Lett. 74, 1250 (1995).CrossRefGoogle Scholar
50.Squires, T.M., Mason, T.G., Annu. Rev. Fluid Mech. 42, 413 (2010).CrossRefGoogle Scholar
51.Mizuno, D., Head, D.A., MacKintosh, F.C., Schmidt, C.F., Macromolecules 41, 7194 (2008).CrossRefGoogle Scholar
52.Lau, P.C.Y., Dutcher, J.R., Beveridge, T.J., Lam, J.S., Biophys. J. 96, 2935 (2009).CrossRefGoogle Scholar
53.Aggarwal, S., Hozalski, R.M., Biofouling 26, 479 (2010).CrossRefGoogle Scholar
54.Aggarwal, S., Poppele, E.H., Hozalski, R.M., Biotechnol. Bioeng. 105, 924 (2010).CrossRefGoogle Scholar
55.Klein, B., Bouriat, P., Goulas, P., Grimaud, R., Biotechnol. Bioeng. 105, 461 (2010).CrossRefGoogle Scholar
56.Henrichs, J., Bacteriol. Rev. 36, 478 (1972).CrossRefGoogle Scholar
57.Harshey, R.M., Annu. Rev. Microbiol. 57, 249 (2003).CrossRefGoogle Scholar
58.McBride, M.J., Annu. Rev. Microbiol. 55, 49 (2001).CrossRefGoogle Scholar
59.Brown, I.I., Hase, C.C., J. Bacteriol. 183, 3784 (2001).CrossRefGoogle Scholar
60.Recht, J., Kolter, R., J. Bacteriol. 183, 5718 (2001).CrossRefGoogle Scholar
61.Recht, J., Martinez, A., Torello, S., Kolter, R., J. Bacteriol. 182, 4348 (2000).CrossRefGoogle Scholar
62.Huang, T.P., Wong, A.C.L., Res. Microbiol. 158, 702 (2007).CrossRefGoogle Scholar
63.Mukherjee, S., Das, P., Sen, R., Trends Biotechnol. 24, 509 (2006).CrossRefGoogle Scholar
64.Agusti, G., Astola, O., Rodriguez-Guell, E., Julian, E., Luquin, M., J. Bacteriol. 190, 6894 (2008).CrossRefGoogle Scholar
65.Bodour, A.A., Guerrero-Barajas, C., Jiorle, B.V., Malcomson, M.E., Paull, A.K., Somogyi, A., Trinh, L.N., Bates, R.B., Maier, R.M., Appl. Environ. Microbiol. 70, 114 (2004).CrossRefGoogle Scholar
66.Stewart, C.R., Rossier, O., Cianciotto, N.P., J. Bacteriol. 191, 1537 (2009).CrossRefGoogle Scholar
67.Scriven, L.E., Sternling, C.V., Nature 187, 186 (1960).CrossRefGoogle Scholar
68.Kinsinger, R.F., Shirk, M.C., Fall, R., J. Bacteriol. 185, 5627 (2003).CrossRefGoogle Scholar
69.Kinsinger, R.F., Kearns, D.B., Hale, M., Fall, R., J. Bacteriol. 187, 8462 (2005).CrossRefGoogle Scholar
70.Be’er, A., Smith, R.S., Zhang, H.P., Florin, E.-L., Payne, S.M., Swinney, H.L., J. Bacteriol. 191, 5758 (2009).CrossRefGoogle Scholar
71.Matar, O.K., Troian, S.M., Phys. Fluids 11, 3232 (1999).CrossRefGoogle Scholar
72.Ben-Jacob, E., Schochet, O., Tenenbaum, A., Cohen, I., Czirok, A., Vicsek, T., Nature 368, 46 (1994).CrossRefGoogle Scholar
73.Derda, R., Laromaine, A., Mammoto, A., Tang, S.K.Y., Mammoto, T., Ingber, D.E., Whitesides, G.M., Proc. Natl. Acad. Sci. U.S.A. 106, 18457 (2009).CrossRefGoogle Scholar
74.Stewart, P.S., Franklin, M.J., Nat. Rev. Microbiol. 6, 199 (2008).CrossRefGoogle Scholar
75.White, A.P., Weljie, A.M., Apel, D., Zhang, P., Shaykhutdinov, R., Vogel, H.J., Surette, M.G., PLoS One 5 (2010).Google Scholar
76.Seymour, J.D., Codd, S.L., Gjersing, E.L., Stewart, P.S., J. Magn. Reson. 167, 322 (2004).CrossRefGoogle Scholar
77.Rani, S.A., Pitts, B., Beyenal, H., Veluchamy, R.A., Lewandowski, Z., Davison, W.M., Buckingham-Meyer, K., Stewart, P.S., J. Bacteriol. 189, 4223 (2007).CrossRefGoogle Scholar
78.Zhang, T.C., Fu, Y.C., Bishop, P.L., Water Environ. Res. 67, 992 (1995).CrossRefGoogle Scholar