Trends in Microbiology
Volume 13, Issue 1, January 2005, Pages 27-33
Journal home page for Trends in Microbiology

Sociomicrobiology: the connections between quorum sensing and biofilms

https://doi.org/10.1016/j.tim.2004.11.007Get rights and content

In the past decade, significant debate has surrounded the relative contributions of genetic determinants versus environmental conditions to certain types of human behavior. While this debate goes on, it is with a certain degree of irony that microbiologists studying aspects of bacterial community behavior face the same questions. Information regarding two social phenomena exhibited by bacteria, quorum sensing and biofilm development, is reviewed here. These two topics have been inextricably linked, possibly because biofilms and quorum sensing represent two areas in which microbiologists focus on social aspects of bacteria. We will examine what is known about this linkage and discuss areas that might be developed. In addition, we believe that these two aspects of bacterial behavior represent a small part of the social repertoire of bacteria. Bacteria exhibit many social activities and they represent a model for dissecting social behavior at the genetic level. Therefore, we introduce the term ‘sociomicrobiology’.

Introduction

In general, biofilm cells encounter much higher local cell-densities than free-floating, planktonic cell populations. An obvious consequence of this is the elevated levels of metabolic by-products, secondary metabolites and other secreted or excreted microbial factors that biofilm cells encounter. Of particular interest are intercellular signaling or quorum-sensing molecules. Because biofilms generally consist of aggregates of cells, one could argue that they represent an environmentally relevant context for quorum sensing. For some species, there is evidence that quorum sensing is important for the construction and/or dissolution of biofilm communities. In this review, we will begin with a discussion of what is known about the role quorum sensing plays in biofilm development in different systems. We will then focus specifically on Pseudomonas aeruginosa as a model system and, finally, consider quorum sensing in the context of a biofilm. Because this review focuses on the intersection of two fields of microbiology that involve social activity of bacteria, we introduce the term sociomicrobiology, meaning ‘investigations of any group-behaviors of microbes’. This is particularly fitting because we discuss controversial areas where the relative contributions of genetic and environmental influences that govern biofilm formation are not clear. This is reminiscent of discussions that continue in the general areas of sociobiology and sociology.

Section snippets

Common molecular schemes used for quorum sensing in bacteria

Quorum sensing is a term used to describe intercellular signaling in bacteria. Although several quorum-sensing systems are known, perhaps the two most thoroughly described systems are the acyl-homoserine lactone (acyl-HSL) systems of many Gram-negative species and the peptide-based signaling systems of many Gram-positive species 1, 2, 3. We will also briefly discuss the widespread AI-2 system that is found in several Gram-positive and Gram-negative species [1]. Before discussing these systems

A survey of quorum-sensing-related biofilm phenotypes

Many groups have examined whether quorum sensing controls biofilm formation. In some cases, quorum sensing does not appear to be involved in biofilm formation. However, quorum sensing has been shown to influence biofilm development for several species.

Pseudomonas aeruginosa as a case study

In 1998, a report in Science described the role of the P. aeruginosa las quorum sensing in biofilm formation [43]. In this first study on the connection between quorum sensing and biofilm formation, lasI mutants deficient in the synthesis of 3-oxododecanoyl-HSL formed biofilms that were flat, densely packed, and homogenous relative to the highly structured, heterogeneous biofilms of the wild-type parent PAO1. In contrast to the wild-type strain, the biofilms formed by the mutants were also

How might quorum sensing function in a biofilm?

To date, all of the quorum-sensing mechanisms that have been described in detail have been studied in the context of planktonic cultures. This is understandable because it simplifies the signaling process. In shaken liquid culture, all bacteria are presumed to be physiologically similar, are producing signal molecules at the same rate, and are exposed to the same concentration of signal molecule. Any degree of heterogeneity in the population can be dismissed because the researcher is measuring

Do all cells in a biofilm produce signal molecules at the same rate?

Regardless of the quorum-sensing system being studied, the substrates for signal production are derived from general metabolites, the composition of which reflects the overall physiologic state of the bacterium. In the case of acyl-HSLs, the substrates for signal synthesis are S-adenosyl methionine (SAM) and acylated acyl carrier protein (acyl-ACP) 4, 6. The availability, and in the case of acyl-ACP, the composition of the substrate pool will depend upon the metabolic state of the cell [60].

Where is quorum sensing first induced in a biofilm?

This is a question that has been previously addressed experimentally. De Kievit et al. [61] used lasI and rhlI transcriptional fusions to the gene coding for the green fluorescent protein (GFP) to monitor quorum-sensing-regulated gene expression in P. aeruginosa biofilms. They found that gene expression occurred primarily at the substratum, within the depths of the biofilm. Yarwood et al. [62] took a similar approach using an RNAIII-GFP fusion in S. aureus to monitor expression of a gene

Summary

Investigations of the role quorum sensing plays in biofilm systems for different organisms and how quorum sensing works mechanistically in a biofilm community remain in their infancy. A clear challenge facing the field is to determine what parameters of a biofilm community influence the onset of quorum sensing and subsequent patterns of gene expression. Another key challenge is to determine the functional consequences of quorum sensing in a biofilm community. Does induction of quorum sensing

Acknowledgements

We would like to thank David L. Chopp for help in figure preparation. Matthew R. Parsek is supported by NSF, NIH and CFF. E.P. Greenberg is supported by NIH and the Keck foundation.

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