Quorum sensing in natural environments: emerging views from microbial mats

doi:10.1016/j.tim.2009.12.008

Trends in Microbiology

Volume 18, Issue 2, February 2010, Pages 73-80

https://doi.org/10.1016/j.tim.2009.12.008 Get rights and content

Much laboratory-based information exists on quorum sensing, a type of bacterial cell-to-cell communication that depends upon exchanges of molecular signals between neighboring cells. However, little is known about how this and other microbial sensing systems operate in nature. Geochemical and biological modifications of signals probably occur in extracellular environments, and these could disrupt intended communication if signals are no longer recognized. However, as we discuss here, signal alterations might result in other outcomes: if a modified signal is able to interact with a different receptor then further environmental information can be gained by the receiving cells. We also postulate that quorum sensing occurs within cell clusters, where signal dispersion might be significantly influenced by extracellular polymers. As a model system to discuss these points we use microbial mats – highly-structured biofilm communities living under sharply-defined, fluctuating geochemical gradients.

Section snippets

Introduction to quorum sensing

Quorum sensing (QS) is a density-dependent form of cell-to-cell chemical communication that uses small-molecule signals (Box 1). Over the past decades, QS has been examined in much detail under laboratory conditions and has generated an enormous literature base (reviewed in Refs 1, 2, 3). However, comparatively little is understood regarding QS and other forms of microbial sensing within the complex milieu of natural environments [4]. In QS, cells produce molecular signals that are released

Microbial mats

Microbial mats are diverse yet highly-structured biofilm communities living within the confines of sharply-defined geochemical gradients that predictably fluctuate over a diel (i.e. 24 h or diurnal) cycle (reviewed in Refs 6, 7, 8). These laminated sedimentary biofilms provide an excellent dynamic system in which to examine environmental effects on QS for the following reasons. Mats have been shown to produce a wide range of extractable QS signals 9, 10. There are extensive small-scale (e.g.

How do signals move once outside the cell?

The relative mobilities of different types of signals and the processes that might influence their movement are not well understood. The mobility of small molecules in aqueous solutions is mainly a function of their passive diffusion in water, that in turn is influenced by their spherical molecular diameter (i.e. approximate size) and surface reactivity with other molecules 15, 16. Small signal molecules (e.g. short-chain AHLs), therefore, should diffuse more rapidly than their larger

Can signals be altered by the environment?

Mats are characterized by geochemical fluctuations of parameters that can be easily measured, such as pH, concentrations of oxidants, O₂, HS⁻ and other ions, UV irradiation, water availability and temperature (Figure 2). In mats, pH values can range from 6 to 11 over a diel cycle 11, 22. This is due to the extremely high rates of photosynthesis occurring during daytime within a thin subsurface layer (under 0.5 mm thick), whereas respiration predominates during the night [23]. During peak

Complexity of natural communities

The biological and spatial heterogeneity of natural microbial communities results from, and contributes to, the diversity of chemical environments over microspatial (e.g. micrometer) scales. The highly localized diversities of species facilitate many interactions, either by chance or by self-organization [20]. These interactions will lead to exchange of signals between partners, non-intended sensing of cues, and chemical manipulation.

Physicochemical environmental conditions determine which

Conclusions and future directions

Many questions remain about how QS operates in natural environments (Box 2). The presence of signal molecules has been observed in a limited number of natural systems 10, 26, 60. Given our present understanding of the physicochemical stability of signal molecules it appears that QS in natural biofilms will be confined to relatively small patches containing clusters of cells, and this raises the additional possibility that signals are altered by natural environments. Environmental alterations

Acknowledgements

This work was supported by National Science Foundation grants under the Environmental Genomics (En-Gen), Collaborative Research in Chemistry (CRC), and Biocomplexity (BE) Programs. We thank reviewers for their very helpful suggestions on many points mentioned in the manuscript.

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Trends in Microbiology

OpinionQuorum sensing in natural environments: emerging views from microbial mats

Section snippets

Introduction to quorum sensing

Microbial mats

How do signals move once outside the cell?

Can signals be altered by the environment?

Complexity of natural communities

Conclusions and future directions

Acknowledgements

Cell

Mar. Geol.

Trends Microbiol.

Paleogeogr. Paleoclimatol. Palaeoecol.

Sed. Geol.

Trends Microbiol.

FEMS Microbiol. Ecol.

Trends Plant Sci.

Curr. Opin. Microbiol.

Trends Microbiol.

FEMS Microbiol. Rev.

FEMS Microbiol. Lett.

Peptides

Listening in on bacteria: acyl-homoserine lactone signaling

Nat. Rev. Mol. Cell Biol.

Quorum sensing: cell-to-cell communication in bacteria

Annu. Rev. Cell Dev. Biol.

The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities

Anal. Bioanal. Chem.

Bacterial small-molecule signaling pathways

Science

Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere

Biol. Bull.

Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH

Environ. Microbiol.

Microelectrode studies of the photosynthesis, and O2, H2S and pH profiles of a microbial mat

Limnol. Oceanogr.

Photosynthesis and structure of benthic microbial mats: microelectrode and SEM studies of four cyanobacterial communities

Limnol. Oceanogr.

Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat

Appl. Environ. Microbiol.

Diffusive mass transfer by nonequilibrium fluctuations: Fick's Law revisited

Phys. Rev. E

Liquid flow in biofilm systems

Appl. Environ. Microbiol.

Membrane vesicles traffic signals and facilitate group activities in a prokaryote

Nature

In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots

FEMS Microbiol. Ecol.

Does efficiency sensing unify diffusion and quorum sensing?

Nat. Rev. Microbiol.

Communication in bacteria: an ecological and evolutionary perspective

Nat. Rev. Microbiol.

Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat

FEMS Microbiol. Ecol.

Microscale observations of sulfate reduction: evidence of microbial activity forming lithified micritic laminae in modern marine stromatolites

Geology

N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa

Infect. Immun.

Kinetic constraints on acylated homoserine lactone-based quorum sensing in marine environments

Aquat. Microb. Ecol.

Dimethyl sulfide and methanethiol formation in microbial mats: potential pathways for biogenic signatures

Environ. Microbiol.

Opinion
Quorum sensing in natural environments: emerging views from microbial mats

Microelectrode studies of the photosynthesis, and O₂, H₂S and pH profiles of a microbial mat