Does efficiency sensing unify diffusion and quorum sensing?

PERSPECTIVES

OPINION

Does efficiency sensing unify diffusion and quorum sensing?

Burkhard A. Hense, Christina Kuttler, Johannes Mller, Michael Rothballer, Anton Hartmann and Jan-Ulrich Kreft

Abstract | Quorum sensing faces evolutionary problems from non-producing or over-producing cheaters. Such problems are circumvented in diffusion sensing, an alternative explanation for quorum sensing. However, both explanations face the problems of signalling in complex environments such as the rhizosphere where, for example, the spatial distribution of cells can be more important for sensing than cell density, which we show by mathematical modelling. We argue that these conflicting concepts can be unified by a new hypothesis, efficiency sensing, and that some of the problems associated with signalling in complex environments, as well as the problem of maintaining honesty in signalling, can be avoided when the signalling cells grow in microcolonies.

In a confined space, bacteria can change their environment in their favour. In an open and mixed environment, by contrast, bacteria must cooperate to carry out these functions, such as the production of a sufficient concentration of exoenzymes to digest complex organic matter1. In addition, the

cooperation of a group of cells can change the environment on a larger scale2 and enable concerted actions such as attacking self-defending host tissue3, defending against predators (protozoa or immune cells4) and fruiting-body formation5,6.

Although direct experimental support for the usefulness of cooperation often lags behind the number of postulated cases, the intriguing idea that some cooperative activities are only effectiveif a sufficient density of cells is available for coordinated action, and that cellcell

communication could be used for this coordination, has received much attention. Before we explain the conflicting hypotheses concerning the function of this type of signalling (in historical order), we will summarize the common ground of both hypotheses: the molecular mechanismsof signalling and the signal molecules involved.

Bacterial cells produce small, diffusible signalling molecules that are secreted intothe environment, from which they can leave by diffusion or advection. The producer cells respond to their own signals, which are therefore called autoinducers79. Typically, an autoinducer induces the transcription of a set of genes that includes the gene encoding the autoinducer-producing enzyme, which results in a positive feedback loop10. The autoinducer can accumulate to sufficiently high concentrations to trigger a response by the cell...