Intermediate Filament-Like Proteins in Bacteria and a Cytoskeletal Function in Streptomyces

Mol Microbiol. 2008 Nov;70(4):1037-50. doi: 10.1111/j.1365-2958.2008.06473.x. Epub 2008 Oct 2.

Abstract

Actin and tubulin cytoskeletons are conserved and widespread in bacteria. A strikingly intermediate filament (IF)-like cytoskeleton, composed of crescentin, is also present in Caulobacter crescentus and determines its specific cell shape. However, the broader significance of this finding remained obscure, because crescentin appeared to be unique to Caulobacter. Here we demonstrate that IF-like function is probably a more widespread phenomenon in bacteria. First, we show that 21 genomes of 26 phylogenetically diverse species encoded uncharacterized proteins with a central segmented coiled coil rod domain, which we regarded as a key structural feature of IF proteins and crescentin. Experimental studies of three in silico predicted candidates from Mycobacterium and other actinomycetes revealed a common IF-like property to spontaneously assemble into filaments in vitro. Furthermore, the IF-like protein FilP formed cytoskeletal structures in the model actinomycete Streptomyces coelicolor and was needed for normal growth and morphogenesis. Atomic force microscopy of living cells revealed that the FilP cytoskeleton contributed to mechanical fitness of the hyphae, thus closely resembling the function of metazoan IF. Together, the bioinformatic and experimental data suggest that an IF-like protein architecture is a versatile design that is generally present in bacteria and utilized to perform diverse cytoskeletal tasks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / genetics
  • Bacterial Proteins / physiology*
  • Conserved Sequence
  • DNA, Bacterial / genetics
  • Evolution, Molecular
  • Genes, Bacterial
  • Genome, Bacterial
  • Intermediate Filament Proteins / genetics
  • Intermediate Filament Proteins / physiology*
  • Intermediate Filaments / genetics
  • Intermediate Filaments / ultrastructure*
  • Microscopy, Atomic Force
  • Microscopy, Electron
  • Molecular Sequence Data
  • Plasmids
  • Sequence Alignment
  • Streptomyces coelicolor / genetics
  • Streptomyces coelicolor / ultrastructure*

Substances

  • Bacterial Proteins
  • DNA, Bacterial
  • Intermediate Filament Proteins