The limits to growth - energetic burden of the endogenous antibiotic tropodithietic acid in Phaeobacter inhibens DSM 17395

PLoS One. 2017 May 8;12(5):e0177295. doi: 10.1371/journal.pone.0177295. eCollection 2017.

Abstract

Phaeobacter inhibens DSM 17395, a model organism for marine Roseobacter group, was studied for its response to its own antimicrobial compound tropodithietic acid (TDA). TDA biosynthesis is encoded on the largest extrachromosomal element of P. inhibens, the 262 kb plasmid, whose curation leads to an increased growth and biomass yield. In this study, the plasmid-cured strain was compared to the wild-type strain and to transposon mutants lacking single genes of the TDA biosynthesis. The data show that the growth inhibition of the wild-type strain can be mainly attributed to the TDA produced by P. inhibens itself. Oxygen uptake rates remained constant in all strains but the growth rate dropped in the wild-type which supports the recently proposed mode of TDA action. Metabolome analysis showed no metabolic alterations that could be attributed directly to TDA. Taken together, the growth of P. inhibens is limited by its own antibacterial compound due to a partial destruction of the proton gradient which leads to a higher energetic demand. The universal presence of TDA biosynthesis in genome-sequenced isolates of the genus Phaeobacter shows that there must be a high benefit of TDA for P. inhibens in its ecological niche despite the drawback on its metabolism.

MeSH terms

  • Anti-Bacterial Agents / biosynthesis
  • Anti-Bacterial Agents / pharmacology*
  • Metabolome
  • Mutation
  • Oxygen / metabolism
  • Rhodobacteraceae / drug effects
  • Rhodobacteraceae / genetics
  • Rhodobacteraceae / growth & development*
  • Rhodobacteraceae / metabolism
  • Tropolone / analogs & derivatives*
  • Tropolone / pharmacology

Substances

  • Anti-Bacterial Agents
  • tropodithietic acid
  • Tropolone
  • Oxygen

Grants and funding

This study was supported by the Deutsche Forschungsgemeinschaft, SFB TRR 51 (www.dfg.de). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.