Molecular strategies of microbial iron assimilation: from high-affinity complexes to cofactor assembly systems

Abstract

Microorganisms have to cope with restricted iron bioavailability in most environmental habitats as well as during host colonization. The continuous struggle for iron has brought forth a plethora of acquisition and assimilation strategies that share several functional and mechanistic principles. One common theme is the utilization of high-affinity chelators for extracellular iron mobilization, generally known as siderophore-dependent iron acquisition. This basic strategy is related with another central aspect of microbial iron acquisition, which is the release of the mobilized iron from extracellular sources to allow its transfer and incorporation into metabolically active proteins. A variety of mechanisms which are often coupled with high-affinity uptake have evolved to facilitate the removal of iron from siderophore ligands; however, they differ in many key aspects including substrate specificities and release efficiencies. The most sophisticated iron release pathways comprise processes of specific hydrolysis and reduction of ferric siderophores, especially in the case of high-affinity iron complexes with greatly negative redox potentials that often represent crucial factors for virulence development in bacterial and fungal pathogens. During the following steps of iron utilization, the acquired metal is transferred through intracellular trafficking pathways which may include diverse storage compartments in order to be directed to cofactor assembly systems and to final protein targeting. Several of these iron channeling routes have been described recently and provide first insights into the later steps of iron assimilation that characterize an essential part of the cellular iron homeostasis network.

Chemical Characterization and Cycling of Dissolved Organic Matter

“…In many remote areas of the equatorial Pacific, northwest Pacific, and Southern Oceans iron concentrations fall to <100 pM, creating enormous selective pressures for microbes to develop efficient Fe uptake and utilization strategies (Barton et al, 2010;Boyd and Ellwood, 2010;Bragg et al, 2010;De Baar et al, 2005;Dutkiewicz et al, 2009Dutkiewicz et al, , 2012Follows et al, 2007;Jickells et al, 2005;Martin and Fitzwater, 1988;Martin et al, 1991;Miethke, 2013). Microbes that can access iron-organic ligand complexes have a distinct competitive advantage in iron-depleted regions of the ocean.…”

Bacteria in an intense competition for iron: Key component of the Campylobacter jejuni iron uptake system scavenges enterobactin hydrolysis product

“…In addition, increasing numbers of lower-denticity siderophores are being isolated from bacterial cultures and found to coordinate Fe(III) and mediate its uptake (14)(15)(16)(17)(18). For example, the trilactone backbone of enterobactin makes it prone to hydrolysis, and although this lability is necessary to allow the intracellular release of Fe(III) from the siderophore, it in addition leads to its slow degradation in aqueous media (7,(19)(20)(21).…”

Catechol Siderophore Transport by Vibrio cholerae

“…Siderophores fall into several chemical classes, including catechols, hydroxamates, carboxylates, and mixed siderophores containing more than one of the above structures (9). The archetype catecholate siderophore enterobactin is produced by Escherichia coli, Salmonella enterica, and related bacteria.…”