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Does efficiency sensing unify diffusion and quorum sensing?

Nature Reviews Microbiology volume 5, pages 230–239 (2007)Cite this article

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.

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Figure 1: What cells sense.
Figure 2: The rhizosphere as an example of a complex habitat.
Figure 3: The geometric relationship of DS and QS as extreme cases of ES.
Figure 4: Spatial distribution and cell density.

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Acknowledgements

We thank Dieter Haas for discussing the fitness effects of signal-blind and other mutants. We apologize to the authors of the many interesting studies that we could not discuss due to space limitations. We thank the Deutsche Forschungsgemeinschaft (DFG) for financial support through the collaborative research centre on 'Singular Phenomena and Scaling in Mathematical Models' and the GSF - National Research Center for Environment and Health for supporting the project network 'Molecular Interactions in the Rhizosphere'.

Author information

Authors and Affiliations

  1. Burkhard A. Hense, Christina Kuttler and Johannes Müller are at the Institute of Biomathematics and Biometry, GSF-National Research Center for Environment and Health, Ingolstaedter Landstrasse 1, D85764 Neuherberg/Munich, Germany.,

    Burkhard A. Hense, Christina Kuttler & Johannes Müller

  2. Johannes Müller is also at the Centre for Mathematical Sciences, Unit M12, Technical University Munich, Boltzmannstrasse 3, D-85748 Garching/Munich, Germany.,

    Johannes Müller

  3. Michael Rothballer and Anton Hartmann are at the Department of Microbe–Plant Interactions, GSF-National Research Center for Environment and Health.,

    Michael Rothballer & Anton Hartmann

  4. Jan-Ulrich Kreft is at Theoretical Biology, IZMB, University of Bonn, Kirschallee 1, D-53115 Bonn, Germany.,

    Jan-Ulrich Kreft

Authors
  1. Burkhard A. Hense
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  2. Christina Kuttler
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  3. Johannes Müller
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  4. Michael Rothballer
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  5. Anton Hartmann
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  6. Jan-Ulrich Kreft
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Corresponding authors

Correspondence to Burkhard A. Hense or Jan-Ulrich Kreft.

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DATABASES

Entrez Genome Project

Porphyromonas gingivalis

Pseudomonas putida

Staphylococcus aureus

Vibrio harveyi

FURTHER INFORMATION

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Jan Kreft's homepage

Molecular interactions in the rhizosphere project

Glossary

Accounting cost

Accounting cost represents the total amount of money spent on buying or producing something.

Advection

The transport of material with the flow of, for example, water or wind; more generally, the motion of a conserved quantity in a velocity field.

AHL

N-acyl-L-homoserine lactone. A class of small autoinducers produced by a considerable number of Proteobacteria, consisting of a homoserine lactone ring with a Nlinked acyl side chain of variable length (C4–C20) and functional groups (mostly hydroxyl- or oxo- groups at the C3 position).

AI-2

Autoinducer 2. Derived from the methyl-donor S-adenosylmethionine, which forms S-adenosylhomocysteine after the transfer of the methyl group. In some bacteria this is converted to S-ribosylhomocysteine, which is converted by the enzyme LuxS to homocysteine and 4,5-dihydroxy-2,3-pentanedione, which spontaneously cyclizes into several furanones in chemical equilibrium, collectively referred to as AI-2.

Autoinducer

A molecule secreted by a bacterial population that accumulates in the growth medium and induces genes in that same bacterial population.

Cheater

An individual who obtains more benefits from a collectively produced public good relative to its own contribution.

Chemical manipulation

If the chemical is produced for the purpose of changing the behaviour of the receiver but this change is detrimental for the receiver, this is chemical manipulation.

Coincidence detection

A situation involving two independent inputs and an output that is activated only when signals are received at the same time at both inputs.

Communication

True communication or signalling requires that the sender, having incurred costs in signal production, benefits from the response of the receiver and that the receiver in turn benefits from its own costly response to the signal. Otherwise, it is not a signal, but a cue or chemical manipulation.

Cooperation

A proportional contribution by individuals to a collectively produced public good.

Cue

If bacteria use the information from chemicals produced for purposes other than communication, the chemical is not a signal but a cue.

Diffusion

The movement of particles from a higher to lower concentration, in which the net flux of the particles is equal to their diffusivity multiplied by the negative concentration gradient.

Diffusion sensing

Determines whether secreted molecules move rapidly away from the cell, allowing cells to regulate the secretion of degradative enzymes and other effectors to minimize losses owing to extracellular diffusion and mixing.

Direct fitness

The component of fitness that is gained through reproduction in contrast to indirect fitness, which is the component of fitness that is gained from aiding the reproduction of non-descendant relatives.

Effector

A substance that is produced and released into the environment for its ultimate effect, such as exoenzymes, siderophores, antibiotics, biosurfactants and virulence factors. Signals that lead to the production of such compounds are not themselves effectors.

Honesty

An honest signal is one that does not misrepresent the world. If the sender has an incentive to convey wrong information, dishonest signals might evolve that manipulate the receivers behaviour to benefit the sender.

Interference

A costly activity with a negative effect on the competitor, which does not act indirectly through resources.

Kin discrimination

When behaviours are directed towards individuals depending on their relatedness to the actor.

Kin selection

Favours traits because of their beneficial effects on the fitness of relatives.

Occam's razor

A principle stating that the explanation of any phenomenon should make as few assumptions as possible. When multiple competing theories have equal predictive powers, the principle recommends selecting the explanation that makes the fewest assumptions and postulates the fewest hypothetical entities.

Opportunity cost

Opportunity cost, also referred to as economic cost, is the cost of something in terms of an opportunity forgone. For example, if a city decides to build a hospital on vacant land that it owns, the opportunity cost is the best other thing that could have been done with the land and construction funds instead.

Pheromone

A chemical produced by an organism to transmit a message to other members of the same species, affecting their behaviour or physiology.

Phylloplane

Aerial plant surfaces, such as the stem, leaves and flowers.

Public good

Any fitness-enhancing resource that is accessible to multiple individuals within a local group.

Quorum sensing

Determines whether a sufficient cell density has been reached to switch a set of behaviours of a whole population, and synchronizes this switching among all individuals of the population.

Rhizosphere

The rhizosphere is the root surface (also known as the rhizoplane) and the surrounding soil influenced by plant roots, as opposed to the bulk soil.

Signal

Any act, structure or chemical emission that elicits a response from the receiver and that evolved because of this effect and is effective because the receiver's response has also evolved. Note that the diffusible signals typically used by bacteria blur the distinction between emitter and receiver. In diffusion sensing, the signal will even be received only by the sender. As such 'self-signalling' does not preclude an evolved response, we use signal and signalling in a broader sense in this article that includes 'self-signalling'.

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Hense, B., Kuttler, C., Müller, J. et al. Does efficiency sensing unify diffusion and quorum sensing?. Nat Rev Microbiol 5, 230–239 (2007). https://doi.org/10.1038/nrmicro1600

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