Constitutive expression of ftsZ overrides the whi developmental genes to initiate sporulation of Streptomyces coelicolor

Antonie Van Leeuwenhoek. 2012 Mar;101(3):619-32. doi: 10.1007/s10482-011-9678-7. Epub 2011 Nov 24.

Abstract

The filamentous soil bacteria Streptomyces undergo a highly complex developmental programme. Before streptomycetes commit themselves to sporulation, distinct morphological checkpoints are passed in the aerial hyphae that are subject to multi-level control by the whi sporulation genes. Here we show that whi-independent expression of FtsZ restores sporulation to the early sporulation mutants whiA, whiB, whiG, whiH, whiI and whiJ. Viability, stress resistance and high-resolution electron microscopy underlined that viable spores were formed. However, spores from sporulation-restored whiA and whiG mutants showed defects in DNA segregation/condensation, while spores from the complemented whiB mutant had increased stress sensitivity, perhaps as a result of changes in the spore sheath. In contrast to the whi mutants, normal sporulation of ssgB null mutants-which fail to properly localise FtsZ-could not be restored by enhancing FtsZ protein levels, forming spore-like bodies that lack spore walls. Our data strongly suggest that the whi genes control a decisive event towards sporulation of streptomycetes, namely the correct timing of developmental ftsZ transcription. The biological significance may be to ensure that sporulation-specific cell division will only start once sufficient aerial mycelium biomass has been generated. Our data shed new light on the longstanding question as to how whi genes control sporulation, which has intrigued scientists for four decades.

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / physiology*
  • Cell Division
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / physiology*
  • DNA-Binding Proteins / genetics
  • Gene Expression Regulation, Bacterial*
  • Gene Expression Regulation, Developmental*
  • Genes, Bacterial
  • Genetic Complementation Test
  • Microscopy, Electron, Scanning
  • Repressor Proteins / genetics
  • Sigma Factor / genetics
  • Spores, Bacterial
  • Streptomyces coelicolor / genetics
  • Streptomyces coelicolor / physiology*
  • Streptomyces coelicolor / ultrastructure
  • Transcription Factors / genetics
  • Transcription Factors / physiology*
  • Transcription, Genetic

Substances

  • Bacterial Proteins
  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • FtsZ protein, Bacteria
  • Repressor Proteins
  • Sigma Factor
  • Transcription Factors
  • WhiA protein, Streptomyces coelicolor
  • whiB protein, Streptomyces
  • whiH protein, Streptomyces
  • whiG protein, Streptomyces coelicolor