Discovery of gas vesicles in Streptomyces sp. CB03234-S and potential effects of gas vesicle gene overexpression on morphological and metabolic changes in streptomycetes

Appl Microbiol Biotechnol. 2019 Jul;103(14):5751-5761. doi: 10.1007/s00253-019-09891-z. Epub 2019 May 21.

Abstract

Gas vesicles are usually found in aquatic microbes to help against adverse growth conditions and also present applied potentials in various biotechnological areas. Although gvp genes encoding gas vesicle proteins are occurred in many bacteria, the formation of gas vesicles in streptomycetes has not been reported yet. During the transcriptome analysis of Streptomyces sp. CB03234-S, a high producer of 10-membered enediynes tiancimycins (TNMs) generated in our previous studies, the notable activation of a gvp gene cluster (gvp3234) was detected, which may be related to the morphological change and yield increase in CB03234-S. Subsequent bioinformatic analysis revealed that gvp3234 possessed some unique features different from other gvp gene clusters, and its relative expression level was much higher than homologues in Streptomyces coelicolor. The overexpression of gvp3234 further improved the total titer of TNM-A and TNM-D from 12.3 ± 0.1 mg/L up to 21.4 ± 0.8 mg/L in CB03234-S, and TEM analysis clearly showed the emergence of gas vesicles, while the heterologous expression of gvp3234 in Streptomyces sp. CB09001 also resulted in the similar formation of fluffy mycelial pellets with long hyphae like in CB03234-S and enhanced the production of xanthone derivative. Our work reported a functionally expressed gvp gene cluster and the corresponding formation of gas vesicles in streptomycetes for the first time. The revealed potential effects of gas vesicles on morphological and metabolic changes shall provide an alternative strategy for strain improvement of industrial streptomycetes to obtain better performances in liquid cultivation and enhance production of secondary metabolites.

Keywords: Gas vesicles; Overexpression; Secondary metabolites; Streptomycetes; gvp genes.

MeSH terms

  • Bacterial Proteins / genetics
  • Computational Biology
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial*
  • Genes, Bacterial
  • Membrane Proteins / genetics
  • Multigene Family
  • Proteins / genetics*
  • Streptomyces / genetics*
  • Streptomyces / metabolism*
  • Streptomyces coelicolor / genetics
  • Vacuoles / physiology*

Substances

  • Bacterial Proteins
  • Membrane Proteins
  • Proteins
  • gas vesicle protein