Streptomycete Spores

Abstract

The Gram‐positive Streptomyces bacteria are major inhabitants of soil, and, unusually for bacteria, they have a complex, multicellular life cycle that looks remarkably fungal‐like. Vegetative growth involves the extension of multicellular, branching hyphae, while reproductive growth involves the emergence of nonbranching hyphae into the air, away from the branching vegetative hyphal mass. These aerial hyphae are converted into chains of prespore compartments by coordinated cell division and chromosome segregation. Prespores then mature into thick‐walled spores that have condensed nucleoids, low metabolic activity and are primed for dispersal and survival. Aerial hyphae and spore surfaces are coated with a hydrophobic, proteinaceous fibrous sheath that aids in aerial growth and may help to promote subsequent spore dispersal and interaction with various interfaces. When exposed to appropriate environmental conditions, spores re‐establish metabolic activity, initiate germination and begin the vegetative phase of their life cycle anew.

Key Concepts

  • Streptomyces spores are distinctly different from bacterial endospores and may be regarded as a type of exospore.
  • Spores develop from dedicated reproductive structures called aerial hyphae.
  • Streptomyces spores are formed by partitioning long, multigenomic hyphal cells into unigenomic prespore compartments, through developmentally regulated cell division and chromosome segregation events.
  • An outer fibrous sheath, containing the lanthionine peptide SapB, the chaplins and the rodlins, confers surface hydrophobicity to aerial hyphae and spores.
  • A dedicated ‘Streptomyces spore wall synthesis complex’ directs the development of a thick spore wall that contributes to mature spore quiescence and resilience.
  • Spores have reduced metabolic activity, accumulate trehalose and have condensed nucleoids.
  • Germination involves rehydration, symmetrical swelling and establishment of polar growth, leading to germ tube emergence and vegetative hyphal outgrowth.

Keywords: differentiation; sporulation; germination; cell division; chromosome segregation; cell wall; hyphae; bacteria

Figure 1. Schematic view of spore formation in Streptomyces. The vegetative mycelium is represented by hyphae growing down into the growth medium. On the surface of the colony, aerial hyphae emerge and extend into the air, away from the growth medium and vegetative mycelium. Initially, the aerial hyphae form occasional crosswalls, similar to the crosswalls observed in vegetative hyphae. After extension into the air has ceased, the apical compartment of each aerial hypha is segmented into prespores by multiple, regularly spaced sporulation septa. Maturation and rounding up of the prespores yield a chain of spores, ready for dispersal in the environment.
Figure 2. Streptomyces spores. (a) Scanning electron micrograph of S. coelicolor spores (foreground) and aerial hyphae (background), encased within a fibrous sheath having a striking paired‐rodlet architecture. (b) Transmission electron micrographs of mature spore chain cross sections. The chains are held together by the fibrous sheath (indicated by arrows), which presumably ruptures to release free spores. Scale bars: (a), 200 nm; (b), 500 nm.
Figure 3. Schematic overview of regulatory pathways controlling aerial mycelium formation and sporulation in streptomycetes. The figure summarises insights gained from studies of S. venezuelae, S. coelicolor and S. griseus. The figure does not distinguish between transcriptional and posttranscriptional regulation. Descriptions of the regulators are provided in the main text, together with key references. It should be noted that some of the regulators control large regulons of >100 genes, and not all interactions are displayed in the figure.
Figure 4. Micrographs showing different stages of spore germination in S. coelicolor. Fluorescence microscopy images (in green) are overlaid on grey‐scale phase‐contrast images. From left to right, the images show a phase‐bright spore, a spore that has become phase dark and partially swollen, a swollen spore in which the cell polarity determinant DivIVA (here visualised in green using a DivIVA‐EGFP fusion protein) has assembled at a specific location and finally, a spore with emerging germ tube with DivIVA‐EGFP at the apex. Scale bar: 2 μm. Flärdh (). Reproduced with permission from John Wiley & Sons.
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Further Reading

Bush MJ, Tschowri N, Schlimpert S, Flärdh K and Buttner MJ (2015) c‐di‐GMP signalling and the regulation of developmental transitions in streptomycetes. Nature Reviews Microbiology 13 (12): 749–760.

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Chater KF (2011) Differentiation in Streptomyces: the properties and programming of diverse cell‐types. In: Dyson P (ed.) Streptomyces: Molecular Biology and Biotechnology, pp 43–86. Caister Academic Press: Norfolk, UK.

Chater KF (2016) Recent advances in understanding Streptomyces. F1000Research 5: 2795.

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Hopwood DA (2007) Streptomyces in Nature and Medicine. The Antibiotic Makers. Oxford University Press: New York.

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Swiercz JP and Elliot MA (2012) Streptomyces sporulation. In: Abel‐Santos E (ed.) Bacterial Spores: Current Research and Applications. Caister Academic Press: Norfolk, UK.

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Elliot, Marie A, and Flärdh, Klas(May 2020) Streptomycete Spores. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000308.pub3]