Characterization of an Lrp/AsnC family regulator SCO3361, controlling actinorhodin production and morphological development in Streptomyces coelicolor

Appl Microbiol Biotechnol. 2017 Jul;101(14):5773-5783. doi: 10.1007/s00253-017-8339-9. Epub 2017 Jun 11.

Abstract

Lrp/AsnC family regulators have been found in many bacteria as crucial regulators controlling diverse cellular processes. By genomic alignment, we found that SCO3361, an Lrp/AsnC family protein from Streptomyces coelicolor, shared the highest similarity to the SACE_Lrp from Saccharopolyspora erythraea. Deletion of SCO3361 led to dramatic reduction in actinorhodin (Act) production and delay in aerial mycelium formation and sporulation on solid media. Dissection of the mechanism underlying the function of SCO3361 in Act production revealed that it altered the transcription of the cluster-situated regulator gene actII-ORF4 by directly binding to its promoter. SCO3361 was an auto-regulator and simultaneously activated the transcription of its adjacent divergently transcribed gene SCO3362. SCO3361 affected aerial hyphae formation and sporulation of S. coelicolor by activating the expression of amfC, whiB, and ssgB. Phenylalanine and cysteine were identified as the effector molecules of SCO3361, with phenylalanine reducing the binding affinity, whereas cysteine increasing it. Moreover, interactional regulation between SCO3361 and SACE_Lrp was discovered for binding to each other's target gene promoter in this work. Our findings indicate that SCO3361 functions as a pleiotropic regulator controlling secondary metabolism and morphological development in S. coelicolor.

Keywords: Act production; Interactional regulation; Lrp/AsnC family; Morphological development; SCO3361; Streptomyces coelicolor.

MeSH terms

  • Anthraquinones / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Carrier Proteins
  • Cysteine / metabolism
  • Gene Deletion
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial*
  • Leucine-Responsive Regulatory Protein / genetics*
  • Leucine-Responsive Regulatory Protein / metabolism
  • Multigene Family
  • Phenylalanine / metabolism
  • Promoter Regions, Genetic
  • Secondary Metabolism
  • Streptomyces coelicolor / genetics*
  • Streptomyces coelicolor / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Anthraquinones
  • Bacterial Proteins
  • Carrier Proteins
  • Transcription Factors
  • Leucine-Responsive Regulatory Protein
  • Phenylalanine
  • actinorhodin
  • Cysteine