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

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. Inte...

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Autores principales: Dhurve, Ganeshwari, Madikonda, Ashok Kumar, Jagannadham, Medicharla Venkata, Siddavattam, Dayananda
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045253/
https://www.ncbi.nlm.nih.gov/pubmed/35266817
http://dx.doi.org/10.1128/spectrum.00293-22
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author Dhurve, Ganeshwari
Madikonda, Ashok Kumar
Jagannadham, Medicharla Venkata
Siddavattam, Dayananda
author_facet Dhurve, Ganeshwari
Madikonda, Ashok Kumar
Jagannadham, Medicharla Venkata
Siddavattam, Dayananda
author_sort Dhurve, Ganeshwari
collection PubMed
description 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 ((55)Fe-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.
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spelling pubmed-90452532022-04-28 Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition Dhurve, Ganeshwari Madikonda, Ashok Kumar Jagannadham, Medicharla Venkata Siddavattam, Dayananda Microbiol Spectr Research Article 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 ((55)Fe-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. American Society for Microbiology 2022-03-10 /pmc/articles/PMC9045253/ /pubmed/35266817 http://dx.doi.org/10.1128/spectrum.00293-22 Text en Copyright © 2022 Dhurve et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Dhurve, Ganeshwari
Madikonda, Ashok Kumar
Jagannadham, Medicharla Venkata
Siddavattam, Dayananda
Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title_full Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title_fullStr Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title_full_unstemmed Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title_short Outer Membrane Vesicles of Acinetobacter baumannii DS002 Are Selectively Enriched with TonB-Dependent Transporters and Play a Key Role in Iron Acquisition
title_sort outer membrane vesicles of acinetobacter baumannii ds002 are selectively enriched with tonb-dependent transporters and play a key role in iron acquisition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045253/
https://www.ncbi.nlm.nih.gov/pubmed/35266817
http://dx.doi.org/10.1128/spectrum.00293-22
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