Abstract
Xanthomonas campestris pv. campestris causes black rot, a serious disease of crucifers. Xanthomonads encode a siderophore biosynthesis and uptake gene cluster xss (Xanthomonas siderophore synthesis) involved in the production of a vibrioferrin-type siderophore. However, little is known about the role of the siderophore in the iron uptake and virulence of X. campestris pv. campestris. In this study, we show that X. campestris pv. campestris produces an α-hydroxycarboxylate-type siderophore (named xanthoferrin), which is required for growth under low-iron conditions and for optimum virulence. A mutation in the siderophore synthesis xssA gene causes deficiency in siderophore production and growth under low-iron conditions. In contrast, the siderophore utilization ΔxsuA mutant is able to produce siderophore, but exhibits a defect in the utilization of the siderophore-iron complex. Our radiolabelled iron uptake studies confirm that the ΔxssA and ΔxsuA mutants exhibit defects in ferric iron (Fe3+ ) uptake. The ΔxssA mutant is able to utilize and transport the exogenous xanthoferrin-Fe3+ complex; in contrast, the siderophore utilization or uptake mutant ΔxsuA exhibits defects in siderophore uptake. Expression analysis of the xss operon using a chromosomal gusA fusion indicates that the xss operon is expressed during in planta growth and under low-iron conditions. Furthermore, exogenous iron supplementation in cabbage leaves rescues the in planta growth deficiency of ΔxssA and ΔxsuA mutants. Our study reveals that the siderophore xanthoferrin is an important virulence factor of X. campestris pv. campestris which promotes in planta growth by the sequestration of Fe3+ .
Highlights
Iron uptake and metabolism are crucial for the growth and survival of bacterial pathogens inside their hosts (Cassat and Skaar, 2013; Expert et al, 2012; Expert et al, 1996; Guerinot, 1994)
In order to understand the role of the siderophore in Xanthomonas campestris pv. campestris (Xcc) virulence and iron uptake, we characterized the siderophore biosynthesis and utilization mutants of Xcc 8004
We show that Xcc produces xanthoferrin, which is similar to the a-hydroxycarboxylate-type siderophore vibrioferrin
Summary
Iron uptake and metabolism are crucial for the growth and survival of bacterial pathogens inside their hosts (Cassat and Skaar, 2013; Expert et al, 2012; Expert et al, 1996; Guerinot, 1994). Iron acquisition by both animal- and plant-pathogenic bacteria inside their hosts acts as a crucial virulence-determining factor in many infection processes in which iron is sequestered by the host proteins (Expert et al, 1996; Schaible and Kaufmann, 2004; Weinberg, 2009). An ABC transporter, which is a cytoplasmic-ATPase-attached transmembrane permease, delivers periplasmic Fe31–siderophores to the cytoplasm and eventually Fe31 reduction occurs to release ferrous iron (Fe21) (Braun and Hantke, 2013; FaraldoGomez and Sansom, 2003; Krewulak and Vogel, 2008; Noinaj et al, 2010)
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