Role of iron homeostasis in the virulence of phytopathogenic bacteria: an 'à la carte' menu

Abstract

The interaction between pathogenic microbes and their hosts is determined by survival strategies on both sides. As a result of its redox properties, iron is vital for the growth and proliferation of nearly all organisms, including pathogenic bacteria. In bacteria-vertebrate interactions, competition for this essential metal is critical for the outcome of the infection. The role of iron in the virulence of plant pathogenic bacteria has only been explored in a few pathosystems in the past. However, in the last 5 years, intensive research has provided new insights into the mechanisms of iron homeostasis in phytopathogenic bacteria that are involved in virulence. This review, which includes important plant pathosystems, discusses the recent advances in the understanding of iron transport and homeostasis during plant pathogenesis. By summarizing the recent progress, we wish to provide an updated view clarifying the various roles played by this metal in the virulence of bacterial phytopathogens as a nutritional and regulatory element. The complex intertwining of iron metabolism and oxidative stress during infection is emphasized.

Figure 1

Schematic representation of the various iron uptake systems in phytopathogenic Gram‐negative bacteria. Bacterial cells can synthesize and excrete siderophores that form a siderophore–ferric complex with Fe(iii), designated as ‘ferric‐siderophore’. A ferric‐siderophore is specifically recognized by an outer membrane TonB‐dependent transporter (rectangles), which is a gated‐channel energized by the cytoplasmic membrane‐generated proton motive force transduced by the TonB protein and its auxiliary proteins ExbB and ExbD. Transport of a ferric‐siderophore across the inner membrane involves a less specific ABC permease (triangle and circles). Ferric complexes of citrate or of exogenous siderophores, i.e. produced by other microbes, are imported in a similar way. Haem can be transported in two ways: either directly or bound to a secreted haemophore protein which delivers it to the cytoplasm via specific TonB‐dependent transporters and specific ABC permeases. Ferrous iron can be transported through the FeoAB and/or EfeUOB systems. FeoB, the main component of the Feo system, is an integral membrane protein with an N‐terminal domain having guanosine triphosphatase (GTPase) activity essential for the transport function. The function of the FeoA peptide is unknown. EfeU is a potential integral inner protein acting as a permease for ferrous or ferric forms of iron. The functions of EfeO and EfeB proteins are unknown. The Yfe ABC permease can import an uncharacterized form of iron. The nature of the Fe‐nicotianamine uptake system is unknown. The diversity of these iron acquisition systems allows bacteria to obtain this metal from the plant iron sources. IM, inner membrane; OM, outer membrane.