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Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies

Nature Reviews Microbiology volume 12, pages 115–124 (2014)Cite this article

Subjects

Key Points

  • Bacterial multicellularity takes several phenotypically diverse forms and has independently evolved in different species.

  • Simple bacterial multicellularity can rapidly evolve as a result of mutations that prevent cells from separating after division or that cause independent cells to co-aggregate.

  • Hallmark features of bacterial multicellularity include morphological differentiation, programmed cell death and a well-defined and reproducible multicellular shape (known as patterning).

  • The benefits of bacterial multicellularity include predation- and stress-resistance and improved resource acquisition and dispersal.

  • Bacterial multicellular structures that arise via aggregation — for example, in Myxobacteria spp. — are susceptible to the emergence of cheater cells that exploit other cooperative cells.

  • Experimental evolution offers exciting possibilities for understanding the mechanisms and dynamics of the de novo evolution of bacterial multicellularity under defined laboratory conditions.

Abstract

Although bacteria frequently live as unicellular organisms, many spend at least part of their lives in complex communities, and some have adopted truly multicellular lifestyles and have abandoned unicellular growth. These transitions to multicellularity have occurred independently several times for various ecological reasons, resulting in a broad range of phenotypes. In this Review, we discuss the strategies that are used by bacteria to form and grow in multicellular structures that have hallmark features of multicellularity, including morphological differentiation, programmed cell death and patterning. In addition, we examine the evolutionary and ecological factors that lead to the wide range of coordinated multicellular behaviours that are observed in bacteria.

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Figure 1: Bacterial manifestations of multicellularity.
Figure 2: Evolution of multicellular clusters.
Figure 3: Different strategies that lead to the development of bacterial multicellularity.

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Acknowledgements

The authors are grateful to E. Flores, J. E. Frías, J. Kirby and S. Müller for kindly providing images. The work was supported by Vidi and Vici grants from the Dutch Applied Research Council (to D.C. and G.P.vW., respectively) and a UK Biotechnology and Biological Sciences Research Council (BBSRC) grant (D.E.R.).

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Author notes

  1. Dennis Claessen and Daniel E. Rozen: These authors contributed equally to this work.

Authors and Affiliations

  1. Molecular Biotechnology, Institute of Biology Leiden, Leiden University, Sylviusweg 72, P.O. Box 9502, Leiden, 2300 RA, The Netherlands

    Dennis Claessen, Daniel E. Rozen & Gilles P. van Wezel

  2. Department of Molecular Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Linnaeusborg, Nijenborgh 7, Groningen, 9747 AG, The Netherlands

    Oscar P. Kuipers

  3. Kluyver Center for Genomics of Industrial Fermentation, Nijenborgh 7, Groningen, 9747 AG, The Netherlands

    Oscar P. Kuipers

  4. Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse 10, Marburg, 35043, Germany

    Lotte Søgaard-Andersen

Authors
  1. Dennis Claessen
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  2. Daniel E. Rozen
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  4. Lotte Søgaard-Andersen
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  5. Gilles P. van Wezel
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Corresponding authors

Correspondence to Lotte Søgaard-Andersen or Gilles P. van Wezel.

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PowerPoint slides

Glossary

Swarming

The coordinated movement of a group of bacterial cells across a surface.

Irreversible differentiation

A process by which cells become irreversibly specialized in form and function.

Syncytial filaments

Filaments that have a multinucleated cytoplasm that is not separated into individual cells.

Germ–soma division

The distinction in animals and plants between cells that are reproductively competent (known as germ cells) and those that contribute only to growth and structural maintenance (soma).

Propagules

Materials that enable dispersal and promote continued growth, such as a spore or cluster of cells.

Sessile

A term used to describe cells that grow while they are attached to a surface substrate.

Planktonic

A term used to describe unattached cells that grow in the bulk liquid of a medium.

Pellicles

Biofilms that form at the water–air interface.

Sporulation

The process of generating spores that are resistant to environmental stresses, such as dessication and starvation.

Kin selection

The evolutionary theory that explains why altruistic behaviours are directed towards individuals that are highly genetically related.

Desmosomes

Eukaryotic cell structures that are specialized for cell–cell adhesion and molecular exchange.

S-layer

A cell envelope layer that is composed of proteins, which encloses the cell surface of many bacteria and archaea, and occasionally divides cells.

Stringent response

A bacterial stress response that is induced during unfavourable growth conditions (such as lack of amino acids), which creates a negative-feedback loop that shuts down macromolecule biosynthesis and other metabolic activity.

(p)ppGpp

(Guanosine pentaphosphate or tetraphosphate). An alarmone molecule that signals the stringent response.

Allorecognition

The process by which organisms are able to distinguish self from non-self.

Bacteriocin

A narrow- or broad-spectrum antimicrobial peptide, which is ribosomally synthesized by bacteria and is able to kill other bacteria by different mechanisms.

Paralogue

A term used to describe evolutionarily related genes that have duplicated and reside in different locations within the same genome.

Sporangia

Specialized structures in which spores are formed and contained.

Min system

A system that ensures the correct localization of the septum during cell division by directing polymerization of the cell division scaffold protein FtsZ away from the cell poles and towards midcell.

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Claessen, D., Rozen, D., Kuipers, O. et al. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12, 115–124 (2014). https://doi.org/10.1038/nrmicro3178

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