Spatial Patterns of DNA Replication, Protein Synthesis, and Oxygen Concentration within Bacterial Biofilms Reveal Diverse Physiological States

Rani, Suriani Abdul; Pitts, Betsey; Beyenal, Haluk; Veluchamy, Raaja Angathevar; Lewandowski, Zbigniew; Davison, William M.; Buckingham‐Meyer, Kelli; Stewart, Philip S.

doi:10.1128/jb.00107-07

Cited by 290 publications

(250 citation statements)

References 37 publications

Supporting

Mentioning

240

Contrasting

Order By: Relevance

“…This aspect and its mucoid appearance suggest a model where the MV uses secretions to reduce cell density and expand outwards and upwards. Moving to the surface will allow cells to gain the best access to oxygen, which is strongly growth-limiting within colonies (13)(14)(15)(16)21). We used confocal imaging to assess the spatial patterning of the MV within WT colonies.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Importance of positioning for microbial evolution

Kim

Racimo

Schluter

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

144

207

View full text Add to dashboard Cite

Microbes commonly live in dense surface-attached communities where cells layer on top of one another such that only those at the edges have unimpeded access to limiting nutrients and space. Theory predicts that this simple spatial effect, akin to plants competing for light in a forest, generates strong natural selection on microbial phenotypes. However, we require direct empirical tests of the importance of this spatial structuring. Here we show that spontaneous mutants repeatedly arise, push their way to the surface, and dominate colonies of the bacterium Pseudomonas fluorescens Pf0-1. Microscopy and modeling suggests that these mutants use secretions to expand and push themselves up to the growth surface to gain the best access to oxygen. Physically mixing the cells in the colony, or introducing space limitations, largely removes the mutant's advantage, showing a key link between fitness and the ability of the cells to position themselves in the colony. We next follow over 500 independent adaptation events and show that all occur through mutation of a single repressor of secretions, RsmE, but that the mutants differ in competitiveness. This process allows us to map the genetic basis of their adaptation at high molecular resolution and we show how evolutionary competitiveness is explained by the specific effects of each mutation. By combining population level and molecular analyses, we demonstrate how living in dense microbial communities can generate strong natural selection to reach the growing edge.bacteria | biofilm | experimental evolution | social interaction

show abstract

Section: Resultsmentioning

confidence: 99%

“…Colonies have long been considered a model laboratory system to study spatially structured microbial communities (12,(21)(22)(23), and are one of the main experimental approaches in studying biofilms (5). Here we use experimental evolution in laboratory colonies to study competition in microbial groups.…”

mentioning

confidence: 99%

Importance of positioning for microbial evolution

Kim

Racimo

Schluter

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

144

207

View full text Add to dashboard Cite

show abstract

“…It is thought that biofilm structure results in microenvironments due to gradients of nutrients, oxygen, and selfgenerated signals (Werner et al 2004;Rani et al 2007). These microenvironments, coupled with the bistable states described for many differentiation processes, have been proposed to ultimately lead to different cell types in specific regions of the biofilm (Raser and O'Shea 2005;Kolter and Greenberg 2006).…”

Section: Cells Within a Biofilm Display Spatiotemporal Organizationmentioning

confidence: 99%

Control of cell fate by the formation of an architecturally complex bacterial community

Vlamakis¹,

Aguilar²,

Losick³

et al. 2008

Genes Dev.

488

648

View full text Add to dashboard Cite

Bacteria form architecturally complex communities known as biofilms in which cells are held together by an extracellular matrix. Biofilms harbor multiple cell types, and it has been proposed that within biofilms individual cells follow different developmental pathways, resulting in heterogeneous populations. Here we demonstrate cellular differentiation within biofilms of the spore-forming bacterium Bacillus subtilis, and present evidence that formation of the biofilm governs differentiation. We show that motile, matrix-producing, and sporulating cells localize to distinct regions within the biofilm, and that the localization and percentage of each cell type is dynamic throughout development of the community. Importantly, mutants that do not produce extracellular matrix form unstructured biofilms that are deficient in sporulation. We propose that sporulation is a culminating feature of biofilm formation, and that spore formation is coupled to the formation of an architecturally complex community of cells.[Keywords: Bacillus; biofilm; cell fate; development; multicellularity] Supplemental material is available at http://www.genesdev.org.

show abstract

“…Nutrients and oxygen permeate the matrix through specific channels and the resulting gradient may generate a population of cells that differ substantially in their metabolism [26]. These cells, named 'persisters', have a low metabolic rate and live in a dormant state attributable to starvation and a low oxygen concentration in the environment, conditions that cause high tolerance to antibiotics [27].…”

Section: Biofilmmentioning

confidence: 99%