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Applied and Environmental Microbiology, November 2006, p. 7324-7330, Vol. 72, No. 11
0099-2240/06/$08.00+0     doi:10.1128/AEM.01163-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Spatiometabolic Stratification of Shewanella oneidensis Biofilms{triangledown} ,{dagger}

Tracy K. Teal,1 Douglas P. Lies,2,3 Barbara J. Wold,1 and Dianne K. Newman1,2,3*

Division of Biological Sciences,1 Division of Geological and Planetary Sciences, California Institute of Technology,2 Howard Hughes Medical Institute, Pasadena, California 911253

Received 19 May 2006/ Accepted 19 August 2006

Biofilms, or surface-attached microbial communities, are both ubiquitous and resilient in the environment. Although much is known about how biofilms form, develop, and detach, very little is understood about how these events are related to metabolism and its dynamics. It is commonly thought that large subpopulations of cells within biofilms are not actively producing proteins or generating energy and are therefore dead. An alternative hypothesis is that within the growth-inactive domains of biofilms, significant populations of living cells persist and retain the capacity to dynamically regulate their metabolism. To test this, we employed unstable fluorescent reporters to measure growth activity and protein synthesis in vivo over the course of biofilm development and created a quantitative routine to compare domains of activity in independently grown biofilms. Here we report that Shewanella oneidensis biofilm structures reproducibly stratify with respect to growth activity and metabolism as a function of size. Within domains of growth-inactive cells, genes typically upregulated under anaerobic conditions are expressed well after growth has ceased. These findings reveal that, far from being dead, the majority of cells in mature S. oneidensis biofilms have actively turned-on metabolic programs appropriate to their local microenvironment and developmental stage.

* Corresponding author. Mailing address: 1200 E. California Blvd., Mailcode 100-23, Pasadena, CA 91125. Phone: (626) 395-6790. Fax: (626) 683-0621. E-mail: dkn{at}gps.caltech.edu.

{triangledown} Published ahead of print on 25 August 2006.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, November 2006, p. 7324-7330, Vol. 72, No. 11
0099-2240/06/$08.00+0     doi:10.1128/AEM.01163-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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