Stenotrophomonas maltophilia produces an EntC-dependent catecholate siderophore that is distinct from enterobactin

Megan Y. Nas, Nicholas P. Cianciotto*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

30 Scopus citations

Abstract

Stenotrophomonas maltophilia, a Gram-negative, multi-drug-resistant bacterium, is increasingly recognized as a key opportunistic pathogen. Thus, we embarked upon an investigation of S. maltophilia iron acquisition. To begin, we determined that the genome of strain K279a is predicted to encode a complete siderophore system, including a biosynthesis pathway, an outer-membrane receptor for ferrisiderophore, and other import and export machinery. Compatible with these data, K279a and other clinical isolates of S. maltophilia secreted a siderophore-like activity when grown at 25-37 °C in low-iron media, as demonstrated by a chrome azurol S assay, which detects iron chelation, and Arnow and Rioux assays, which detect catecholate structures. Importantly, these supernatants rescued the growth of iron-starved S. maltophilia, documenting the presence of a biologically active siderophore. A mutation in one of the predicted biosynthesis genes (entC) abolished production of the siderophore and impaired bacterial growth in low-iron conditions. Inactivation of the putative receptor gene (fepA) prevented the utilization of siderophore-containing supernatants for growth in low-iron conditions. Although the biosynthesis and import loci showed some similarity to those of enterobactin, a well-known catecholate made by enteric bacteria, the siderophore of K279a was unable to rescue the growth of an enterobactin-utilizing indicator strain, and conversely iron-starved S. maltophilia could not use purified enterobactin. Furthermore, the S. maltophilia siderophore displayed patterns of solubility in organic compounds and mobility upon thin-layer chromatography that were distinct from those of enterobactin and its derivative, salmochelin. Together, these data demonstrate that S. maltophilia secretes a novel catecholate siderophore.

Original languageEnglish (US)
Article number000545
Pages (from-to)1590-1603
Number of pages14
JournalMicrobiology (United Kingdom)
Volume163
Issue number11
DOIs
StatePublished - Nov 2017

Funding

M. Y. N. was supported in part by NIAID grant T32 AI007476. Overall support for this work came from NIAID grants AI117082 and AI125968 awarded to N. P. C. M. Y. N. was supported in part by National Institute of Allergy and Infectious DiseasesNIAID grant T32 AI007476. Overall support for this work came from NIAID grants AI117082 and AI125968 awarded to N. P. C. We thank members of the Cianciotto lab, especially Ashley Du Mont and Chris White, for their helpful advice. We also acknowledge Wolfgang Rabsch at the Robert Koch Institute (Wernigerode) for sending us the S. typhimurium indicator strain TA2700. Finally, we thank Michele Swanson at the University of Michigan for providing strain DY330.

Keywords

  • EntC
  • Enterobactin
  • FepA
  • Salmochelin
  • Siderophore
  • Stenotrophomonas maltophilia

ASJC Scopus subject areas

  • Microbiology

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