Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition

Microbiol Spectr. 2022 Apr 27;10(2):e0029322. doi: 10.1128/spectrum.00293-22. Epub 2022 Mar 10.

Abstract

Outer membrane vesicles (OMVs) of Acinetobacter baumannii DS002 carry proteins which perform selective biological functions. The proteins involved in cell wall/membrane biogenesis and inorganic ion transport and metabolism occupied a significant portion of the 302 proteins associated with OMVs. Interestingly, the TonB-dependent transporters (TonRs), linked to the active transport of nutrients across the energy-deprived outer membrane, are predominant among proteins involved in inorganic ion transport and metabolism. The OMVs of DS002 contain TonRs capable of transporting iron complexed to catecholate, hydroximate, and mixed types of siderophores. Consistent with this observation, the OMVs were firmly bound to ferric-enterobactin (55Fe-Ent) and successfully transported iron into A. baumannii DS002 cells grown under iron-limiting conditions. In addition to the TonRs, OMVs also carry proteins known to promote pathogenesis, immune evasion, and biofilm formation. Our findings provide conclusive evidence for the role of OMVs in the transport of nutrients such as iron and show the presence of proteins with proven roles in pathogenicity and immune response. IMPORTANCE TonB-dependent transporters (TonRs) play a crucial role in transporting nutrients such as iron, nickel, copper, and complex carbohydrates across the energy-deprived outer membrane. Due to their unique structural features, TonRs capture nutrients in an energy-independent manner and transport them across the outer membrane by harvesting energy derived from the inner membrane-localized Ton-complex. In this study, we report the presence of TonRs capable of transporting various nutrients in OMVs and demonstrate their role in capturing and transporting ferric iron complexed with enterobactin into A. baumannii DS002 cells. The OMV-associated TonRs appear to play a critical role in the survival of A. baumannii, listed as a priority pathogen, under nutrient-deprived conditions.

Keywords: LC-ESI-MS/MS; OMVs; TonRs; iron uptake; proteomics; siderophores.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinetobacter baumannii* / metabolism
  • Bacterial Outer Membrane Proteins / metabolism
  • Bacterial Proteins / metabolism
  • Enterobactin / metabolism
  • Iron / metabolism
  • Membrane Transport Proteins / metabolism
  • Siderophores / metabolism

Substances

  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins
  • Membrane Transport Proteins
  • Siderophores
  • Enterobactin
  • Iron