Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor

Willey, Joanne M.; Santamaría, Ramón I.; Guijarro, José A.; Geistlich, Martin; Losick, Richard

doi:10.1016/0092-8674(91)90096-h

Cited by 166 publications

(233 citation statements)

References 18 publications

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“…Indeed, relatively recently a small diffusible peptide of -18 amino acids (SapB) synthesized by S. lividans and characterized in a closely related strain, Streptomyces coelicolor, has been shown to play a key role in the developmental cycle of these organisms (Willey et al, 1991). SapB as well as another chemically uncharacterized diffusible factor are needed for the erection of aerial mycelium leading to sporulation in S. coelicolor (Willey et al, 1991). One explanation presented by Willey et al was that SapB might be a pheromone-like activator of differentiation (for a review, see Grafe, 1989) known to be synthesized by many different actinomycetes.…”

Section: Resultsmentioning

confidence: 99%

Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans.

1993

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Although the antibiotic thiostrepton is best known as an inhibitor of protein synthesis, it also, at extremely low concentrations (< 10-9 M), induces the expression of a regulon of unknown function in certain Streptomyces species. Here, we report the purification of a Streptomyces lividans thiostrepton-induced transcriptional activator protein, TipAL, whose N-terminus is similar to a family of eubacterial regulatory proteins represented by MerR.TipAL was first purified from induced cultures of S.lividans as a factor which bound to and activated transcription from its own promoter. The tipAL gene was overexpressed in Escherichia coli and TipAL protein purifi'ed in a single step using a thiostrepton affinity column. Thiostrepton enhanced binding of TipAL to the promoter and catalysed specific transcription in vitro.TipAs, a second gene product of the same open reading frame consisting of the C-terminal domain of TipAL, is apparently translated using its own in-frame initiation site. Since it is produced in large molar excess relative to TipAL after induction and also binds thiostrepton, it may competitively modulate transcriptional activation.

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Section: Resultsmentioning

confidence: 99%

Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans.

1993

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“…By lowering the water surface tension of the aqueous environment from 72 to 32 mJ/m 2 , SapB enables hyphae to overcome the physical barrier posed by the medium-air interface (Tillotson et al 1998). SapB is produced on complex agar media but not on minimal media supplemented with mannitol or arabinose (Willey et al 1991). On the latter media, other molecules are expected to fulfill a role similar to that of SapB.…”

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confidence: 99%

“…This phenotype correlates with the failure to produce and secrete SapB (Willey et al 1991(Willey et al , 1993. SapB is a small peptide of 18 amino acids with a high surface activity.…”

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confidence: 99%

A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation inStreptomyces coelicolorby forming amyloid-like fibrils

Claessen¹,

Rink²,

Jong³

et al. 2003

Genes Dev.

307

399

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Streptomycetes exhibit a complex morphological differentiation. After a submerged mycelium has been formed, filaments grow into the air to septate into spores. A class of eight hydrophobic secreted proteins, ChpA-H, was shown to be instrumental in the development of Streptomyces coelicolor. Mature forms of ChpD-H are up to 63 amino acids in length, and those of ChpA-C are larger (±225 amino acids). ChpA-C contain two domains similar to ChpD-H, as well as a cell-wall sorting signal. The chp genes were expressed in submerged mycelium (chpE and chpH) as well as in aerial hyphae (chpA-H). Formation of aerial hyphae was strongly affected in a strain in which six chp genes were deleted (⌬chpABCDEH). A mixture of ChpD-H purified from cell walls of aerial hyphae complemented the ⌬chpABCDEH strain extracellularly, and it accelerated development in the wild-type strain. The protein mixture was highly surface active, and it self-assembled into amyloid-like fibrils at the water-air interface. The fibrils resembled those of a surface layer of aerial hyphae. We thus conclude that the amyloid-like fibrils of ChpD-H lower the water surface tension to allow aerial growth and cover aerial structures, rendering them hydrophobic. ChpA-C possibly bind ChpD-H to the cell wall.

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“…Recent experiments have indicated that at least one of the Saps (SapB) is required on some media for aerial hyphae to form, yet SapB is apparently absent from aerial mycelium produced on minimal medium plus mannitoi (Willey etaL, 1991). SapB is very small and abundant, and contains a high proportion of leucine residues: thus, as pointed out by Willey et at.…”

Section: How Might Bida Influence Morphological Differentiation?mentioning

confidence: 99%

The use of a rare codon specifically during development?

Leskiw

Bibb

Chater

1991

Molecular Microbiology

115

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Summary A range of circumstantial evidence suggests that in Streptomyces spp., genes required for vegetative growth do not contain the leucine codon TTA. Instead, the codon seems to be confined to a few genes necessary during differentiation, when the colonies begin to produce aerial hyphae and antibiotics. Thus, mutations in bldA, the structural gene for tRNALeuTTA, do not retard vegetative growth, but they prevent normal aerial mycelium and antibiotic production. Most of the known TTA‐containing genes specify regulatory or resistance proteins associated with antibiotic‐production clusters. Possibly the ability to translate the UUA codons in mRNA from such genes is confined to late stages of colony development. Factors that might have contributed to the evolution of this unusual situation are discussed.

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Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor

Cited by 166 publications

References 18 publications

Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans.

Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans.

A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation inStreptomyces coelicolorby forming amyloid-like fibrils

The use of a rare codon specifically during development?

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