Yersiniabactin is a quorum sensing autoinducer and siderophore in uropathogenicEscherichia coli

Author:

Heffernan James R.,Katumba George L.,McCoy William H.,Henderson Jeffrey P.ORCID

Abstract

ABSTRACTSiderophores are secreted ferric ion chelators used to obtain iron in nutrient-limited environmental niches, including human hosts. While allE. coliencode the enterobactin (Ent) siderophore system, isolates from patients with urinary tract infections additionally encode the genetically distinct yersiniabactin (Ybt) siderophore system. To determine whether the Ent and Ybt systems are functionally redundant for iron uptake, we compared growth of different isogenic siderophore biosynthesis mutants in the presence of transferrin, a human iron-binding protein. We observed that the Ybt system does not compensate for loss of the Ent system during siderophore-dependent, low density growth. Using transcriptional and product analysis, we found that this non-redundancy is attributable to a density-dependent transcriptional stimulation cycle in which Ybt assume an additional autoinducer function. These results distinguish the Ybt system as a combined quorum-sensing and siderophore system. These functions may reflect Ybt as a public good within bacterial communities or as an adaptation to confined, subcellular compartments in infected hosts. The efficiency of this arrangement may contribute to the extraintestinal pathogenic potential ofE. coliand relatedEnterobacterales.IMPORTANCEUrinary tract infections (UTIs) are one of the most common human bacterial infections encountered by physicians. Adaptations that increase the pathogenic potential of commensal microbes such asE.coliare of great interest. One potential adaptation observed in clinical isolates is accumulation of multiple siderophore systems, which scavenge iron for nutritional use. While iron uptake is important for bacterial growth, the increased metabolic costs of siderophore production could diminish bacterial fitness during infections. In a siderophore-dependent growth conditions, we show that the virulence-associated yersiniabactin siderophore system in uropathogenicE. coliis not redundant with the ubiquitousE. colienterobactin system. This arises not from differences in iron scavenging activity but because yersiniabactin is preferentially expressed during bacterial crowding, leaving bacteria dependent upon enterobactin for growth at low cell density. Notably, this regulatory mode arises because yersiniabactin stimulates its own expression, acting as an autoinducer in a previously unappreciated quorum-sensing system. This unexpected result connects quorum-sensing with pathogenic potential inE. coliand relatedEnterobacterales.

Publisher

Cold Spring Harbor Laboratory

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