Abstract
Extracytoplasmic function (ECF) sigma factors are key transcriptional regulators that prokaryotes have evolved to respond to environmental challenges. Streptomyces tsukubaensis harbours 42 ECFs to reprogram stress-responsive gene expression. Among them, SigG1 features a minimal conserved ECF σ2–σ4 architecture and an additional C-terminal extension that encodes a SnoaL_2 domain, which is characteristic for ECF σ factors of group ECF56. Although proteins with such domain organisation are widely found among Actinobacteria, the functional role of ECFs with a fused SnoaL_2 domain remains unknown. Our results show that in addition to predicted self-regulatory intramolecular amino acid interactions between the SnoaL_2 domain and the ECF core, SigG1 activity is controlled by the cognate anti-sigma protein RsfG, encoded by a co-transcribed sigG1-neighbouring gene. Characterisation of ∆sigG1 and ∆rsfG strains combined with RNA-seq and ChIP-seq experiments, suggests the involvement of SigG1 in the morphological differentiation programme of S. tsukubaensis. SigG1 regulates the expression of alanine dehydrogenase, ald and the WhiB-like regulator, wblC required for differentiation, in addition to iron and copper trafficking systems. Overall, our work establishes a model in which the activity of a σ factor of group ECF56, regulates morphogenesis and metal-ions homeostasis during development to ensure the timely progression of multicellular differentiation.
Highlights
Streptomycetes are unique soil-dwelling bacteria with a prolific biosynthetic capacity responsible for hundreds of widely used bioactive compounds
The presence of the CT SnoaL_2 domain in extracytoplasmic function (ECF) sigma factors is distributed among different p hyla[17,18]. They are predominantly found in the Actinobacteria and Firmicutes and, in particular, they are included within groups ECF41, ECF56, ECF205, ECF294 and ECF295 of the general ECF group classification (Supplementary Fig. S1)[17]
Besides STSU_11560, we identified three additional ECFs with a SnoaL_2 extension in the S. tsukubaensis genome: STSU_14518 and STSU_17474, that belong to the ECF41 group; and STSU_12530, a closer homologue to STSU_11560
Summary
Streptomycetes are unique soil-dwelling bacteria with a prolific biosynthetic capacity responsible for hundreds of widely used bioactive compounds. We illustrated that the transition from first mycelium stage (MI) to secondary metabolite producing differentiated mycelium (MII) is preceded by phenomena of cell death in the vegetative mycelia, which reroutes nutrients to differentiate MII hyphae into nascent aerial mycelium. Pivotal to this substrate to aerial mycelium transition is the production of a hydrophobic coat. The process of differentiation in the Streptomyces genus has been largely studied in strains used as model organisms such as S. coelicolor and S. venezuelae It is strictly dependent on gene networks which are controlled by the Bld (bald) and the Whi (white) family of r egulators[4,5,6]. They do not seem to play a direct role in RNAP b inding[14,15,16]
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