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  • Review Article
  • Published:

Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium

Nature Reviews Microbiology volume 7, pages 36–49 (2009)Cite this article

Key Points

  • This Review analyses recent advances in our understanding of the cell biology and genetics of Streptomyces growth and developmental morphogenesis, focusing mainly on Streptomyces coelicolor as a model organism. The major topics discussed are:

  • The molecular basis of the apical growth and branching of hyphae.

  • The morphogenetic processes that allow hyphae to break surface tension and grow into the air.

  • The role of the hormone-like γ-butyrolactone signalling molecule, A-factor, in the regulation of aerial mycelium formation and its integration with secondary metabolism in Streptomyces griseus.

  • The developmental reorganization of cytoskeletal elements, cell division, chromosome segregation and peptidoglycan assembly that leads to the conversion of aerial hyphae into mature spores, and what is known about the regulation of these processes.

  • Recent advances in the study of cell type-specific gene expression in Streptomyces, and new tools and systems that will facilitate the investigation of Streptomyces developmental biology.

Abstract

During the life cycle of the filamentous bacteria Streptomyces, morphological differentiation is closely integrated with fundamental growth and cell-cycle processes, as well as with truly complex multicellular behaviour that involves hormone-like extracellular signalling and coordination with an extraordinarily diverse secondary metabolism. Not only are the bacterial cytoskeleton and the machineries for cell-wall assembly, cell division and chromosome segregation reorganized during sporulation, but the developmental programme of these fascinating organisms also has many unusual elements, including the formation of a sporulating aerial mycelium and the production of a surfactant peptide and a hydrophobic sheath that allow cells to escape from the surface tension of the growth medium.

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Figure 1: Developmental life cycle of Streptomyces coelicolor.
Figure 2: Model for the biosynthesis of the lantibiotic-like surfactant peptide SapB.
Figure 3: Model for the role of the chaplins and SapB in morphogenesis.
Figure 4: The A-factor signalling cascade triggers morphological differentiation and secondary metabolism in Streptomyces griseus.
Figure 5: Reorganization of cell biological processes during differentiation of aerial hyphae into spores.
Figure 6: Patterns of cell type-specific gene expression in sporulating aerial hyphae.

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Acknowledgements

We thank M. Elliot, J. Willey, D. Claessen, G. Kelemen, M. Bibb, Y. Ohnishi, G. Muth, J. Errington and K. Chater for their comments on the manuscript, and M. Hempel and A. Hempel for helping with the figures. We apologize to colleagues whose work has not been cited owing to space constraints.

Author information

Authors and Affiliations

  1. Department of Cell and Organism Biology, Lund University, Sölvegatan 35, Lund, SE-223 62, Sweden

    Klas Flärdh

  2. Department of Molecular Microbiology, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

    Mark J. Buttner

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Correspondence to Mark J. Buttner.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Caulobacter crescentus

Corynebacterium glutamicum

Escherichia coli

Mycobacterium smegmatis

Mycobacterium tuberculosis

Streptomyces avermitilis

Streptomyces coelicolor

Streptomyces griseus

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Glossary

Vegetative mycelium

The dense, branching network of hyphae that arises in the medium after spore germination (also called the substrate mycelium).

Saprophyte

An organism that degrades and feeds on dead organisms or decaying organic material, especially in soil.

Germ tube

The vegetative hypha that emerges from spores during germination.

Vancomycin

An antibiotic that inhibits cell-wall biosynthesis by binding to peptidoglycan precursor lipid II when lipid II is exposed on the external face of the cytoplasmic membrane.

FtsK family

A family of ATP-dependent DNA translocases that are important in chromosome segregation and intercellular DNA transfer.

γ-butyrolactones

A class of hormone-like signalling molecules made by streptomycetes. γ-butyrolactones are similar in structure to the homoserine lactones that are involved in quorum sensing in Gram-negative bacteria.

Grixazone

A yellow secondary metabolite that contains a phenoxazinone chromophore made by Streptomyces griseus.

Hexahydroxyperyl-enequinone

(HPQ). A polyketide secondary metabolite made by Streptomyces griseus that readily autopolymerizes to form HPQ melanin.

Hyphal cross-wall

An infrequent vegetative septum observed in substrate hyphae and occasionally in aerial hyphae. Hyphal cross-walls are not associated with constriction and cell separation (in contrast to sporulation septa).

σB-like stress response sigma factor

A sigma factor that is closely related, phylogenetically and functionally, to σB, which controls the general stress response in Bacillus subtilis.

Z ring

A ring of the cytoskeletal tubulin-like protein FtsZ that is formed at the beginning of cytokinesis and defines the site of cell division.

Walker A cytoskeletal ATPase

A group of Walker ATPases that possess a distinct version of the Walker A motif that deviates from the universal consensus. These proteins share structural similarity with P-loop GTPases and are recognized as members of the GTPase superfamily.

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Flärdh, K., Buttner, M. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7, 36–49 (2009). https://doi.org/10.1038/nrmicro1968

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