Cargando…

Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus

In this study, we show that Bacteroides species utilize Fe(III)‐xenosiderophores as the only source of exogenous iron to support growth under iron‐limiting conditions in vitro anaerobically. Bacteroides fragilis was the only species able to utilize Fe(III)‐ferrichrome while Bacteroides vulgatus ATCC...

Descripción completa

Detalles Bibliográficos
Autores principales: Rocha, Edson R., Krykunivsky, Anna S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5552952/
https://www.ncbi.nlm.nih.gov/pubmed/28397401
http://dx.doi.org/10.1002/mbo3.479
_version_ 1783256554534862848
author Rocha, Edson R.
Krykunivsky, Anna S.
author_facet Rocha, Edson R.
Krykunivsky, Anna S.
author_sort Rocha, Edson R.
collection PubMed
description In this study, we show that Bacteroides species utilize Fe(III)‐xenosiderophores as the only source of exogenous iron to support growth under iron‐limiting conditions in vitro anaerobically. Bacteroides fragilis was the only species able to utilize Fe(III)‐ferrichrome while Bacteroides vulgatus ATCC 8482 and Bacteroides thetaiotaomicron VPI 5482 were able to utilize both Fe(III)‐enterobactin and Fe(III)‐salmochelin S4 as the only source of iron in a dose‐dependent manner. We have investigated the way B. fragilis assimilates Fe(III)‐ferrichrome as initial model to understand the utilization of xenosiderophores in anaerobes. B. fragilis contains two outer membrane TonB‐dependent transporters (TBDTs), FchA1 and FchA2, which are homologues to Escherichia coli ferrichrome transporter FhuA. The disruption of fchA1 gene had only partial growth defect on Fe(III)‐ferrichrome while the fchA2 mutant had no growth defect compared to the parent strain. The genetic complementation of fchA1 gene restored growth to parent strain levels indicating that it plays a role in Fe(III)‐ferrichrome assimilation though we cannot rule out some functional overlap in transport systems as B. fragilis contains abundant TBDTs whose functions are yet not understood. However, the growth of B. fragilis on Fe(III)‐ferrichrome was abolished in a feoAB mutant indicating that Fe(III)‐ferrichrome transported into the periplasmic space was reduced in the periplasm releasing ferrous iron prior to transport through the FeoAB transport system. Moreover, the release of iron from the ferrichrome may be linked to the thiol redox system as the trxB deletion mutant was also unable to grow in the presence of Fe(III)‐ferrichrome. The genetic complementation of feoAB and trxB mutants completely restored growth on Fe(III)‐ferrichrome. Taken together, these findings show that Bacteroides species have developed mechanisms to utilize ferric iron bound to xenosiderophores under anaerobic growth conditions though the regulation and role in the biology of Bacteroides in the anaerobic intestinal environment remain to be understood.
format Online
Article
Text
id pubmed-5552952
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-55529522017-08-15 Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus Rocha, Edson R. Krykunivsky, Anna S. Microbiologyopen Original Research In this study, we show that Bacteroides species utilize Fe(III)‐xenosiderophores as the only source of exogenous iron to support growth under iron‐limiting conditions in vitro anaerobically. Bacteroides fragilis was the only species able to utilize Fe(III)‐ferrichrome while Bacteroides vulgatus ATCC 8482 and Bacteroides thetaiotaomicron VPI 5482 were able to utilize both Fe(III)‐enterobactin and Fe(III)‐salmochelin S4 as the only source of iron in a dose‐dependent manner. We have investigated the way B. fragilis assimilates Fe(III)‐ferrichrome as initial model to understand the utilization of xenosiderophores in anaerobes. B. fragilis contains two outer membrane TonB‐dependent transporters (TBDTs), FchA1 and FchA2, which are homologues to Escherichia coli ferrichrome transporter FhuA. The disruption of fchA1 gene had only partial growth defect on Fe(III)‐ferrichrome while the fchA2 mutant had no growth defect compared to the parent strain. The genetic complementation of fchA1 gene restored growth to parent strain levels indicating that it plays a role in Fe(III)‐ferrichrome assimilation though we cannot rule out some functional overlap in transport systems as B. fragilis contains abundant TBDTs whose functions are yet not understood. However, the growth of B. fragilis on Fe(III)‐ferrichrome was abolished in a feoAB mutant indicating that Fe(III)‐ferrichrome transported into the periplasmic space was reduced in the periplasm releasing ferrous iron prior to transport through the FeoAB transport system. Moreover, the release of iron from the ferrichrome may be linked to the thiol redox system as the trxB deletion mutant was also unable to grow in the presence of Fe(III)‐ferrichrome. The genetic complementation of feoAB and trxB mutants completely restored growth on Fe(III)‐ferrichrome. Taken together, these findings show that Bacteroides species have developed mechanisms to utilize ferric iron bound to xenosiderophores under anaerobic growth conditions though the regulation and role in the biology of Bacteroides in the anaerobic intestinal environment remain to be understood. John Wiley and Sons Inc. 2017-04-11 /pmc/articles/PMC5552952/ /pubmed/28397401 http://dx.doi.org/10.1002/mbo3.479 Text en © 2017 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Rocha, Edson R.
Krykunivsky, Anna S.
Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title_full Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title_fullStr Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title_full_unstemmed Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title_short Anaerobic utilization of Fe(III)‐xenosiderophores among Bacteroides species and the distinct assimilation of Fe(III)‐ferrichrome by Bacteroides fragilis within the genus
title_sort anaerobic utilization of fe(iii)‐xenosiderophores among bacteroides species and the distinct assimilation of fe(iii)‐ferrichrome by bacteroides fragilis within the genus
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5552952/
https://www.ncbi.nlm.nih.gov/pubmed/28397401
http://dx.doi.org/10.1002/mbo3.479
work_keys_str_mv AT rochaedsonr anaerobicutilizationoffeiiixenosiderophoresamongbacteroidesspeciesandthedistinctassimilationoffeiiiferrichromebybacteroidesfragiliswithinthegenus
AT krykunivskyannas anaerobicutilizationoffeiiixenosiderophoresamongbacteroidesspeciesandthedistinctassimilationoffeiiiferrichromebybacteroidesfragiliswithinthegenus