Streptomycete Spores

Marie A Elliot, McMaster University, Hamilton, ON, Canada
Klas Flärdh, Lund University, Lund, Sweden

Published online: August 2012

DOI: 10.1002/9780470015902.a0000308.pub2

Gram‐positive bacteria of the genus Streptomyces are major inhabitants of soil and grow as branching hyphae, strikingly like the filamentous fungi. Whereas their mycelium is multicellular, dispersal and long‐term survival are achieved by unicellular spores. Spore formation is part of a complex developmental cycle involving dedicated reproductive aerial hyphae. The long apical cells of the aerial hyphae are divided into chains of tens of prespore compartments, which in turn mature into thick‐walled spores with condensed nucleoids and low metabolic activity, primed for dispersal and survival. Aerial hyphae and spore surfaces are coated with a proteinaceous fibrous sheath. This highly hydrophobic sheath is required for aerial hyphal emergence, and may aid spore dispersal and interaction with various interfaces. When exposed to appropriate environmental conditions, spores rehydrate and swell. Cell polarisation is required for the emergence of a germ tube, which develops into a mycelium by apical growth and side‐branch formation.

Key Concepts:

  • Streptomyces spores are distinctly different from bacterial endospores.
  • Spores develop from dedicated reproductive structures called aerial hyphae.
  • Streptomyces spores are formed by division of long, multigenomic hyphal cells into unigenomic compartments.
  • A thick spore wall is assembled from within the maturing spore and contributes to quiescence and resilience.
  • Spores are dehydrated, accumulate trehalose and have condensed nucleoids.
  • An outer fibrous sheath confers surface hydrophobicity to aerial hyphae and spores.
  • Germination involves rehydration, symmetrical swelling and establishment of polar growth leading to germ tube emergence.

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

Figure 1. Schematic view of spore formation in Streptomyces. The vegetative mycelium is represented by hyphae growing down in the medium. On the surface of the colony, aerial branches emerge and extend away from the medium and into the air. Initially, the aerial hyphae form occasional crosswalls, similar to the crosswalls observed in vegetative hyphae. After extension into the air has ceased, the apical cell of the aerial hyphae is segmented into prespores by multiple and regularly spaced sporulation septa. Maturation and rounding up of the prespores result in the final 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 and (b) 500 nm.
Figure 3. Schematic view of sporulation septation and spore wall formation. (a) Aerial hyphae are encased within a fibrous sheath (FS), outside of the hyphal wall (HW). (b) Sporulation septa (SS) grow inwards and have a double annular appearance. (c) Thickening of the wall at the sporulation septa is the first stage of spore wall (SW) formation. (d) A uniformly thick spore wall is assembled on the inside of the original hyphal wall. (e) Spore maturation includes rounding up to an ovoid shape and detaching from each other. The fibrous sheath and the original hyphal wall tend to break up to release the spores. Some studies have reported a separation of the spore wall into distinct layers, as indicated in panel (e), but the significance of this observation remain unclear. Redrawn from Wildermuth and Hopwood (1970).
Figure 4. Micrographs showing different stages of spore germination in S. coelicolor. 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 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. Reproduced with permission from Flärdh (2003).
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 References
    Bruton CJ, Plaskitt KA and Chater KF (1995) Tissue‐specific glycogen branching isoenzymes in a multicellular prokaryote, Streptomyces coelicolor A3(2). Molecular Microbiology 18: 89–99.
    Capstick DS, Jomaa A, Hanke C, Ortega J and Elliot MA (2011) Dual amyloid domains promote differential functioning of the chaplin proteins during Streptomyces aerial morphogenesis. Proceedings of the National Academy of Sciences of the USA 108: 9821–9826.
    Capstick DS, Willey JM, Buttner MJ and Elliot MA (2007) SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Molecular Microbiology 64: 602–613.
    Challis GL (2008) Mining microbial genomes for new natural products and biosynthetic pathways. Microbiology 154: 1555–1569.
    book 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. Norfolk, UK: Caister Academic Press.
    Chater KF, Biro S, Lee KJ, Palmer T and Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiology Reviews 34: 171–198.
    Claessen D, Rink R, de Jong W et al. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid‐like fibrils. Genes & Development 17: 1714–1726.
    Claessen D, Stokroos I, Deelstra HJ et al. (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Molecular Microbiology 53: 433–443.
    Davis NK and Chater KF (1990) Spore colour in Streptomyces coelicolor A3(2) involves the developmentally regulated synthesis of a compound biosynthetically related to polyketide antibiotics. Molecular Microbiology 4: 1679–1691.
    Dedrick RM, Wildschutte H and McCormick JR (2009) Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. Journal of Bacteriology 191: 320–332.
    Derouaux A, Halici S, Nothaft H et al. (2004) Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. Journal of Bacteriology 186: 1893–1897.
    Ditkowski B, Troć P, Ginda K et al. (2010) The actinobacterial signature protein ParJ (SCO1662) regulates ParA polymerization and affects chromosome segregation and cell division during Streptomyces sporulation. Molecular Microbiology 78: 1403–1415.
    Eaton D and Ensign JC (1980) Streptomyces viridochromogenes spore germination initiated by calcium ions. Journal of Bacteriology 143: 377–382.
    Elliot MA, Karoonuthaisiri N, Huang J et al. (2003) The chaplins: a family of hydrophobic cell‐surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes & Development 17: 1727–1740.
    Ensign JC (1978) Formation, properties, and germination of actinomycete spores. Annual Reviews of Microbiology 32: 185–219.
    Facey PD, Hitchings MD, Saavedra‐Garcia P et al. (2009) Streptomyces coelicolor Dps‐like proteins: differential dual roles in response to stress during vegetative growth and in nucleoid condensation during reproductive cell division. Molecular Microbiology 73: 1186–1202.
    Flärdh K (2003) Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Molecular Microbiology 49: 1523–1536.
    Flärdh K, Leibovitz E, Buttner MJ and Chater KF (2000) Generation of a non‐sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Molecular Microbiology 38: 737–749.
    Funa N, Funabashi M, Ohnishi Y and Horinouchi S (2005) Biosynthesis of hexahydroxyperylenequinone melanin via oxidative aryl coupling by cytochrome P‐450 in Streptomyces griseus. Journal of Bacteriology 187: 8149–8155.
    Grantcharova N, Lustig U and Flärdh K (2005) Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2). Journal of Bacteriology 187: 3227–3237.
    Grund AD and Ensign JC (1985) Properties of the germination inhibitor of Streptomyces viridochromogenes spores. Journal of General Microbiology 131: 833–847.
    Haiser HJ, Yousef MR and Elliot MA (2009) Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. Journal of Bacteriology 191: 6501–6512.
    Hardisson C, Manzanal MB, Salas JA and Suarez JE (1978) Fine structure, physiology and biochemistry of arthrospore germination in Streptomyces antibioticus. Journal of General Microbiology 105: 203–214.
    Heichlinger A, Ammelburg M, Kleinschnitz EM et al. (2011) The MreB‐like protein Mbl of S. coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis. Journal of Bacteriology 193: 1533–1542.
    den Hengst CD, Tran NT, Bibb MJ et al. (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Molecular Microbiology 78: 361–379.
    Hirsch CF and Ensign JC (1978) Some properties of Streptomyces viridochromogenes spores. Journal of Bacteriology 134: 1056–1063.
    Jakimowicz D, Mouz S, Zakrzewska‐Czerwińska J and Chater KF (2006) Developmental control of a parAB promoter leads to formation of sporulation‐associated ParB complexes in Streptomyces coelicolor. Journal of Bacteriology 188: 1710–1720.
    Jakimowicz D, Zydek P, Kois A, Zakrzewska‐Czerwińska J and Chater KF (2007) Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Molecular Microbiology 65: 625–641.
    de Jong W, Wösten HA, Dijkhuizen L and Claessen D (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Molecular Microbiology 73: 1128–1140.
    Kelemen GH, Brian P, Flärdh K et al. (1998) Developmental regulation of transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3(2). Journal of Bacteriology 180: 2515–2521.
    Kleinschnitz EM, Heichlinger A, Schirner K et al. (2011) Proteins encoded by the mre gene cluster in Streptomyces coelicolor A3(2) cooperate in spore wall synthesis. Molecular Microbiology 79: 1367–1379.
    Kodani S, Hudson ME, Durrant MC et al. (2004) The SapB morphogen is a lantibiotic‐like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proceedings of the National Academy of Sciences of the USA 101: 11448–11453.
    Kois A, Swiatek M, Jakimowicz D and Zakrzewska‐Czerwińska J (2009) SMC protein‐dependent chromosome condensation during aerial hyphal development in Streptomyces. Journal of Bacteriology 191: 310–319.
    Mazza P, Noens EE, Schirner K et al. (2006) MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Molecular Microbiology 60: 838–852.
    McBride MJ and Ensign JC (1987) Effects of intracellular trehalose content on Streptomyces griseus spores. Journal of Bacteriology 169: 4995–5001.
    McBride MJ and Ensign JC (1990) Regulation of trehalose metabolism by Streptomyces griseus spores. Journal of Bacteriology 172: 3637–3643.
    McCormick JR and Flärdh K (2012) Signals and regulators that govern Streptomyces development. FEMS Microbiology Reviews 36: 206–231.
    McCormick JR, Su EP, Driks A and Losick R (1994) Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Molecular Microbiology 14: 243–254.
    Rueda B, Miguelez EM, Hardisson C and Manzanal MB (2001) Changes in glycogen and trehalose content of Streptomyces brasiliensis hyphae during growth in liquid cultures under sporulating and non‐sporulating conditions. FEMS Microbiology Letters 194: 181–185.
    Salerno P, Larsson J, Bucca G et al. (2009) One of the two genes encoding nucleoid‐associated HU proteins in Streptomyces coelicolor is developmentally regulated and specifically involved in spore maturation. Journal of Bacteriology 191: 6489–6500.
    Schneider D, Bruton CJ and Chater KF (2000) Duplicated gene clusters suggest an interplay of glycogen and trehalose metabolism during sequential stages of aerial mycelium development in Streptomyces coelicolor A3(2). Molecular and General Genetics 263: 543–553.
    Sharples GP and Williams ST (1976) Fine structure of spore germination in actinomycetes. Journal of General Microbiology 96: 323–332.
    Süsstrunk U, Pidoux J, Taubert S, Ullmann A and Thompson CJ (1998) Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Molecular Microbiology 30: 33–46.
    Wang L, Yu Y, He X et al. (2007) Role of an FtsK‐like protein in genetic stability in Streptomyces coelicolor A3(2). Journal of Bacteriology 189: 2310–2318.
    Wildermuth H (1970) Surface structure of streptomycete spores as revealed by negative staining and freeze‐etching. Journal of Bacteriology 101: 318–322.
    Wildermuth H (1972) Morphological surface characteristics of Streptomyces glaucescens and S. acrimycini, two streptomycetes with “hairy” spores. Archives of Microbiology 81: 321–332.
    Wildermuth H and Hopwood DA (1970) Septation during sporulation in Streptomyces coelicolor. Journal of General Microbiology 60: 57–59.
    Willemse J, Borst JW, de Waal E, Bisseling T and van Wezel GP (2011) Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes & Development 25: 89–99.
    Willemse J, Mommaas AM and van Wezel GP (2012) Constitutive expression of ftsZ overrides the whi developmental genes to initiate sporulation of Streptomyces coelicolor. Antonie van Leeuwenhoek 101: 619–632.
    Yu T‐W and Hopwood DA (1995) Ectopic expression of the Streptomyces coelicolor whiE genes for polyketide spore pigment synthesis and their interaction with the act genes for actinorhodin biosynthesis. Microbiology 141: 2779–2791.
 Further Reading
    Chater KF and Chandra G (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiology Reviews 30: 651–672.
    book Dyson P (ed.) (2011) Streptomyces. Molecular Biology and Biotechnology. Norfolk, UK: Caister Academic Press.
    book Elliot MA, Buttner MJ and Nodwell JR (2008) "Multicellular development of Streptomyces". In: Whitworth DE (ed.) Myxobacteria: Multicellularity and Differentiation, pp. 419–438. Herndon, VA: ASM Press.
    Flärdh K (2010) Cell polarity and the control of apical growth in Streptomyces. Current Opinion in Microbiology 13: 758–765.
    Flärdh K and Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nature Reviews Microbiology 7: 36–49.
    Hopwood DA (2006) Soil to genomics: the Streptomyces chromosome. Annual Reviews of Genetics 40: 1–23.
    book Hopwood DA (2007) Streptomyces in Nature and Medicine. The Antibiotic Makers. New York: Oxford University Press.
    Horinouchi S (2007) Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Bioscience, Biotechnology, and Biochemistry 71: 283–299.
    McCormick JR (2009) Cell division is dispensible but not irrelevant in Streptomyces. Current Opinion in Microbiology 12: 689–698.
    book Swiercz JP and Elliot MA (2012) "Streptomyces sporulation". In: Abel‐Santos E (ed.) Bacterial Spores: Current Research and Applications. Norfolk, UK: Caister Academic Press.

Related Sub-Topics:

Composition and Structure of Microbial Cells | Bacteria | Bacterial Culture, Growth and Development
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Article Title: Streptomycete Spores
 
How to Cite close
Elliot, Marie A, and Flärdh, Klas(Aug 2012) Streptomycete Spores. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000308.pub2]