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  • Review Article
  • Published:

A functional perspective on phenotypic heterogeneity in microorganisms

Nature Reviews Microbiology volume 13, pages 497–508 (2015)Cite this article

Subjects

Key Points

  • The phenotype of an individual microbial cell is not determined by genes and environment alone. Rather, a number of cellular mechanisms produce phenotypic differences between genetically identical cells grown in homogeneous environments; these differences are referred to as phenotypic heterogeneity.

  • The degree of heterogeneity that arises in a given trait is influenced by the biochemical properties of molecules and by the architecture of gene-regulatory networks. Mutations and other genetic changes can therefore influence the degree of phenotypic heterogeneity.

  • As a consequence, phenotypic heterogeneity is an evolvable trait that can be shaped by natural selection. Increased levels of heterogeneity in specific phenotypic traits can evolve if this provides organisms with benefits in terms of increased survival and growth.

  • One possible benefit is that phenotypic heterogeneity can help organisms to cope with fluctuating environments. This effect is known as bet hedging.

  • Another possible benefit arises through division of labour. Individual cells with different phenotypic traits can specialize in different activities and behaviours and can engage in beneficial interactions.

  • Phenotypic heterogeneity is a potentially important component of biological diversity; it arises at the level of individual microbial cells and provides groups of microorganisms with added functionality.

Abstract

Most microbial communities consist of a genetically diverse assembly of different organisms, and the level of genetic diversity plays an important part in community properties and functions. However, biological diversity also arises at a lower level of biological organization, between genetically identical cells that reside in the same microenvironment. In this Review, I outline the molecular mechanisms responsible for phenotypic heterogeneity and discuss how phenotypic heterogeneity allows genotypes to persist in fluctuating environments. I also describe how it promotes interactions between phenotypic subpopulations in clonal groups, providing microbial groups with new functionality.

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Figure 1: Phenotypic heterogeneity.
Figure 2: Molecular mechanisms of phenotypic heterogeneity.
Figure 3: Different functions of phenotypic heterogeneity.

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Acknowledgements

The author gratefully acknowledges fruitful collaborations and important discussions with current and former members of the research group, and with a number of colleagues (in particular W.-D. Hardt and M. Doebeli). The author also thanks the referees and S. van Vliet for helpful comments on the manuscript. This work was supported by the Swiss National Science Foundation, the Swiss Federal Institute of Technology Zurich (ETH Zürich), the Swiss Federal Institute of Aquatic Science and Technology (Eawag) and the Marie Curie Program of the European Commission.

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  1. Institute of Biogeochemistry and Pollutant Dynamics, Swiss Federal Institute of Technology Zurich (ETH Zürich), ETH Zentrum CHN H70.3, Universitätsstrasse 16, Zürich, 8092, Switzerland

    Martin Ackermann

  2. Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Ueberlandstrasse 133, Dübendorf, 8600, Switzerland

    Martin Ackermann

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Correspondence to Martin Ackermann.

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PowerPoint slides

Glossary

Quantitative biology

The use of mathematical tools and principles to analyse experimental data in order to test existing theories and develop new theories.

Division of labour

The division of a biological task into several different subtasks that are each executed by specialized individuals.

Gene amplification

The generation of multiple copies of a genetic region, resulting from a duplication event and subsequent homologous recombination of the duplicated region.

Stochastic gene expression

Fluctuations in the rate of mRNA and/or protein production over time. These fluctuations are a consequence of the low copy numbers of molecules in microbial cells and the burst-like nature of transcription.

Periodic oscillations

Changes in phenotypic traits that occur at regular time intervals.

Cellular age

The age of a cell as measured by the time since synthesis of particular subcellular structures. During cell division, these structures can be asymmetrically segregated into the daughter cells, resulting in two cells of different cellular ages.

Quorum sensing

The regulation of gene expression in response to changes in bacterial population density. Quorum sensing is mediated by intercellular chemical signalling.

Persisters

Cells that are phenotypically tolerant to antibiotics without being genetically resistant.

HipA

An intracellular bacterial toxin that is part of the toxin–antitoxin module hipBA.

Metabolic flux

The rate at which molecules flow through a metabolic pathway.

Type three secretion system 1

(ttss-1). The genetic locus encoding a multiprotein secretion apparatus that some Gram-negative bacteria use to translocate effector proteins into host cells.

Cheaters

Individuals that contribute less than others to a collectively produced public good but still benefit from that good.

Biofilms

Microbial communities that are attached to surfaces. Biofilms provide spatial structure by limiting the movement of microorganisms and the diffusion of molecules.

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Ackermann, M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol 13, 497–508 (2015). https://doi.org/10.1038/nrmicro3491

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