Hostname: page-component-797576ffbb-tx785 Total loading time: 0 Render date: 2023-12-11T05:39:22.287Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "useRatesEcommerce": true } hasContentIssue false

Biofilms as complex fluids

Published online by Cambridge University Press:  18 May 2011

James N. Wilking
Affiliation:
Harvard University, Cambridge, MA 02139, USA; jwilking@seas.harvard.edu
Thomas E. Angelini
Affiliation:
University of Florida; t.e.angelini@ufl.edu
Agnese Seminara
Affiliation:
Harvard University, Cambridge, MA 02139, USA; Agnese.seminara@gmail.com
Michael P. Brenner
Affiliation:
Harvard University, Cambridge, MA 02139, USA; Brenner@seas.harvard.edu
David A. Weitz
Affiliation:
Harvard University, Cambridge, MA 02139, USA; weitz@seas.harvard.edu
Get access

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.

Type
Research Article
Copyright
Copyright © Materials Research Society 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Ghannoum, M., O’Toole, G.A., Eds., Microbial Biofilms, (ASM Press, Washington, DC, 2004).Google Scholar
2.O’Toole, G., Kaplan, H.B., Kolter, R., Annu. Rev. Microbiol. 54, 49 (2000).Google Scholar
3.Sutherland, I.W., Microbiology 147, 3 (2001).Google Scholar
4.Branda, S.S., Vik, A., Friedman, L., Kolter, R., Trends Microbiol. 13, 20 (2005).Google Scholar
5.Whitman, W.B., Coleman, D.C., Wiebe, W.J., Proc. Natl. Acad. Sci. U.S.A. 95, 6578 (1998).Google Scholar
6.Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappinscott, H.M., Annu. Rev. Microbiol. 49, 711 (1995).Google 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).Google 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).Google Scholar
10.Gristina, A.G., Science 237, 1588 (1987).Google Scholar
11.del Pozo, J.L., Patel, R., Clin. Pharmacol. Ther. 82, 204 (2007).Google Scholar
12.Frank, K.L., del Pozo, J.L., Patel, R., Clin. Microbiol. Rev. 21, 111 (2008).Google 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).Google 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).Google Scholar
15.Angelini, T.E., Roper, M., Kolter, R., Weitz, D.A., Brenner, M.P., Proc. Natl. Acad. Sci. 106, 18109 (2009).Google Scholar
16.Rubinstein, M., Colby, R.H., Polymer Physics (Oxford University Press, NY, 2003).Google Scholar
17.Cerf, A., Cau, J.C., Vieu, C., Dague, E., Langmuir 25, 5731 (2009).Google Scholar
18.Francius, G., Domenech, O., Mingeot-Leclercq, M.P., Dufrene, Y.F., J. Bacteriol. 190, 7904 (2008).Google Scholar
19.Arnoldi, M., Fritz, M., Bauerlein, E., Radmacher, M., Sackmann, E., Boulbitch, A., Phys. Rev. E 62, 1034 (2000).Google 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).Google Scholar
21.Vlamakis, H., Aguilar, C., Losick, R., Kolter, R., Genes Dev. 22, 945 (2008).Google Scholar
22.Romero, D., Aguilar, C., Losick, R., Kolter, R., Proc. Natl. Acad. Sci. U.S.A. 107, 2230 (2010).Google Scholar
23.Lahaye, E., Aubry, T., Kervarec, N., Douzenel, P., Sire, O., Biomacromolecules 8, 1218 (2007).Google Scholar
24.Klapper, I., Dockery, J., SIAM Rev. 52, 221 (2010).Google Scholar
25.Boyd, A., Chakrabarty, A.M., Appl. Environ. Microbiol. 60, 2355 (1994).Google Scholar
26.Kolodkin-Gal, I., Romero, D., Cao, S.G., Clardy, J., Kolter, R., Losick, R., Science 328, 627 (2010).Google Scholar
27.Aguilar, C., Vlamakis, H., Losick, R., Kolter, R., Curr. Opin. Microbiol. 10, 638 (2007).Google Scholar
28.Branda, S.S., Gonzalez-Pastor, J.E., Dervyn, E., Ehrlich, S.D., Losick, R., Kolter, R., J. Bacteriol. 186, 3970 (2004).Google Scholar
29.Branda, S.S., Chu, F., Kearns, D.B., Losick, R., Kolter, R., Mol. Microbiol. 59, 1229 (2006).Google Scholar
30.Kearns, D.B., Chu, F., Branda, S.S., Kolter, R., Losick, R., Mol. Microbiol. 55, 739 (2005).Google Scholar
31.Danese, P.N., Pratt, L.A., Kolter, R., J. Bacteriol. 182, 3593 (2000).Google Scholar
32.Pratt, L.A., Kolter, R., Mol. Microbiol. 30, 285 (1998).Google Scholar
33.O’Toole, G.A., Kolter, R., Mol. Microbiol. 30, 295 (1998).Google 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).Google 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).Google Scholar
39.Stoodley, P., Lewandowski, Z., Boyle, J.D., Lappin-Scott, H.M., Biotechnol. Bioeng. 65, 83 (1999).Google Scholar
40.Picologlou, B.F., Zelver, N., Characklis, W.G., J. Hydraulics Div., ASCE 106, 733 (1980).Google 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).Google 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).Google Scholar
44.Donev, A., Cisse, I., Sachs, D., Variano, E., Stillinger, F.H., Connelly, R., Torquato, S., Chaikin, P.M., Science 303, 990 (2004).Google Scholar
45.Hohne, D.N., Younger, J.G., Solomon, M.J., Langmuir 25, 7743 (2009).Google Scholar
46.Stoodley, P., Cargo, R., Rupp, C.J., Wilson, S., Klapper, I., J. Ind. Microbiol. Biotechnol. 29, 361 (2002).Google Scholar
47.Storm, C., Pastore, J.J., MacKintosh, F.C., Lubensky, T.C., Janmey, P.A., Nature 435, 191 (2005).Google 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).Google Scholar
49.Mason, T.G., Weitz, D.A., Phys. Rev. Lett. 74, 1250 (1995).Google Scholar
50.Squires, T.M., Mason, T.G., Annu. Rev. Fluid Mech. 42, 413 (2010).Google Scholar
51.Mizuno, D., Head, D.A., MacKintosh, F.C., Schmidt, C.F., Macromolecules 41, 7194 (2008).Google Scholar
52.Lau, P.C.Y., Dutcher, J.R., Beveridge, T.J., Lam, J.S., Biophys. J. 96, 2935 (2009).Google Scholar
53.Aggarwal, S., Hozalski, R.M., Biofouling 26, 479 (2010).Google Scholar
54.Aggarwal, S., Poppele, E.H., Hozalski, R.M., Biotechnol. Bioeng. 105, 924 (2010).Google Scholar
55.Klein, B., Bouriat, P., Goulas, P., Grimaud, R., Biotechnol. Bioeng. 105, 461 (2010).Google Scholar
56.Henrichs, J., Bacteriol. Rev. 36, 478 (1972).Google Scholar
57.Harshey, R.M., Annu. Rev. Microbiol. 57, 249 (2003).Google Scholar
58.McBride, M.J., Annu. Rev. Microbiol. 55, 49 (2001).Google Scholar
59.Brown, I.I., Hase, C.C., J. Bacteriol. 183, 3784 (2001).Google Scholar
60.Recht, J., Kolter, R., J. Bacteriol. 183, 5718 (2001).Google Scholar
61.Recht, J., Martinez, A., Torello, S., Kolter, R., J. Bacteriol. 182, 4348 (2000).Google Scholar
62.Huang, T.P., Wong, A.C.L., Res. Microbiol. 158, 702 (2007).Google Scholar
63.Mukherjee, S., Das, P., Sen, R., Trends Biotechnol. 24, 509 (2006).Google Scholar
64.Agusti, G., Astola, O., Rodriguez-Guell, E., Julian, E., Luquin, M., J. Bacteriol. 190, 6894 (2008).Google 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).Google Scholar
66.Stewart, C.R., Rossier, O., Cianciotto, N.P., J. Bacteriol. 191, 1537 (2009).Google Scholar
67.Scriven, L.E., Sternling, C.V., Nature 187, 186 (1960).Google Scholar
68.Kinsinger, R.F., Shirk, M.C., Fall, R., J. Bacteriol. 185, 5627 (2003).Google Scholar
69.Kinsinger, R.F., Kearns, D.B., Hale, M., Fall, R., J. Bacteriol. 187, 8462 (2005).Google 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).Google Scholar
71.Matar, O.K., Troian, S.M., Phys. Fluids 11, 3232 (1999).Google Scholar
72.Ben-Jacob, E., Schochet, O., Tenenbaum, A., Cohen, I., Czirok, A., Vicsek, T., Nature 368, 46 (1994).Google 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).Google Scholar
74.Stewart, P.S., Franklin, M.J., Nat. Rev. Microbiol. 6, 199 (2008).Google 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).Google 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).Google Scholar
78.Zhang, T.C., Fu, Y.C., Bishop, P.L., Water Environ. Res. 67, 992 (1995).Google Scholar