Xenosiderophore Utilization Promotes Bacteroides thetaiotaomicron Resilience during Colitis

Wenhan Zhu, Maria G. Winter, Luisella Spiga, Elizabeth R. Hughes, Rachael Chanin, Aditi Mulgaonkar, Jenelle Pennington, Michelle Maas, Cassie L. Behrendt, Jiwoong Kim, Xiankai Sun, Daniel P. Beiting, Lora V. Hooper, Sebastian E. Winter

Research output: Contribution to journalArticle

Abstract

During short-lived perturbations, such as inflammation, the gut microbiota exhibits resilience and reverts to its original configuration. Although microbial access to the micronutrient iron is decreased during colitis, pathogens can scavenge iron by using siderophores. How commensal bacteria acquire iron during gut inflammation is incompletely understood. Curiously, the human commensal Bacteroides thetaiotaomicron does not produce siderophores but grows under iron-limiting conditions using enterobacterial siderophores. Using RNA-seq, we identify B. thetaiotaomicron genes that were upregulated during Salmonella-induced gut inflammation and were predicted to be involved in iron uptake. Mutants in the xusABC locus (BT2063-2065) were defective for xenosiderophore-mediated iron uptake in vitro. In the normal mouse gut, the XusABC system was dispensable, while a xusA mutant colonized poorly during colitis. This work identifies xenosiderophore utilization as a critical mechanism for B. thetaiotaomicron to sustain colonization during inflammation and suggests a mechanism of how interphylum iron metabolism contributes to gut microbiota resilience.

Original languageEnglish (US)
Pages (from-to)376-388.e8
JournalCell Host and Microbe
Volume27
Issue number3
DOIs
StatePublished - Mar 11 2020

Keywords

  • bacteroidetes
  • gut inflammation
  • gut microbiota resilience
  • iron metabolism
  • siderophore

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Virology

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  • Cite this

    Zhu, W., Winter, M. G., Spiga, L., Hughes, E. R., Chanin, R., Mulgaonkar, A., Pennington, J., Maas, M., Behrendt, C. L., Kim, J., Sun, X., Beiting, D. P., Hooper, L. V., & Winter, S. E. (2020). Xenosiderophore Utilization Promotes Bacteroides thetaiotaomicron Resilience during Colitis. Cell Host and Microbe, 27(3), 376-388.e8. https://doi.org/10.1016/j.chom.2020.01.010