A Disturbed Siderophore Transport Inhibits Myxobacterial Predation

Abstract

Background: Understanding the intrinsic mechanisms of bacterial competition is a fundamental question. Iron is an essential trace nutrient that bacteria compete for. The most prevalent manner for iron scavenging is through the secretion of siderophores. Although tremendous efforts have focused on elucidating the molecular mechanisms of siderophores biosynthesis, export, uptake, and regulation of siderophores, the ecological aspects of siderophore-mediated competition are not well understood. Methods: We performed predation and bacterial competition assays to investigate the function of siderophore transport on myxobacterial predation. Results: Deletion of msuB, which encodes an iron chelate uptake ABC transporter family permease subunit, led to a reduction in myxobacterial predation and intracellular iron, but iron deficiency was not the predominant reason for the decrease in the predation ability of the ∆msuB mutant. We further confirmed that obstruction of siderophore transport decreased myxobacterial predation by investigating the function of a non-ribosomal peptide synthetase for siderophore biosynthesis, a TonB-dependent receptor, and a siderophore binding protein in M. xanthus. Our results showed that the obstruction of siderophores transport decreased myxobacterial predation ability through the downregulation of lytic enzyme genes, especially outer membrane vesicle (OMV)-specific proteins. Conclusions: This work provides insight into the mechanism of siderophore-mediated competition in myxobacteria.

Myxococcus xanthus predation: an updated overview

“…Experimentally, it has been demonstrated that depletion of iron triggers the biosynthesis of the antibiotic actinorhodin in S. coelicolor to prevent predation from M. xanthus ( Lee et al, 2020 ). Moreover, a mutant of M. xanthus that produces less siderophores (myxochelins) is defective in predation against P. aeruginosa ( Dong et al, 2022b ). Similarly, mutants in a putative TonB-dependent transporter for ferrimyxochelins and in components of the ABC transporter that introduces ferrimyxochelins into the cytoplasm also exhibit less efficient predation on this prey ( Dong et al, 2022b ).…”

“…Moreover, a mutant of M. xanthus that produces less siderophores (myxochelins) is defective in predation against P. aeruginosa ( Dong et al, 2022b ). Similarly, mutants in a putative TonB-dependent transporter for ferrimyxochelins and in components of the ABC transporter that introduces ferrimyxochelins into the cytoplasm also exhibit less efficient predation on this prey ( Dong et al, 2022b ). All these data seem to indicate that competition for iron plays a decisive role in the myxobacterial predatory interaction with the prey.…”

“…While short-range killing mainly involves the production of a battery of secondary metabolites (SMs) such as antibiotics, and of hydrolytic enzymes to degrade and feed on the cellular components of the prey ( Muñoz-Dorado et al, 2016 ), contact-dependent lysis is mediated by secretion systems ( Seef et al, 2021 ; Thiery et al, 2022 ). Moreover, recent studies have shown that metals are also involved in M. xanthus predation either by using metals to provoke oxidative stress or by outcompeting prey for possession of essential metals ( Contreras-Moreno et al, 2020 ; Lee et al, 2020 ; Dong et al, 2022b ; Pérez et al, 2022 ).…”

Exploring the Biological Pathways of Siderophores and Their Multidisciplinary Applications: A Comprehensive Review

“…This complex formation is facilitated by specific transport proteins that transfer siderophores from inside the cell to the outside, creating soluble complexes with iron ions. These complexes are then recognized and absorbed by the microbial uptake system [52]. Once inside the cell, iron ions are dissociated from the siderophores through two primary methods [53].…”