The role of iron uptake in pathogenicity and symbiosis in Photorhabdus luminescens TT01

Robert J Watson,Stuart Reynolds,Susan A Joyce,David J Clarke,Peter Millichap

doi:10.1186/1471-2180-10-177

Robert J Watson, Stuart Reynolds + Show 3 more

Open Access

https://doi.org/10.1186/1471-2180-10-177

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Journal: BMC microbiology	Publication Date: Jun 22, 2010
Citations: 83	License type: cc-by

Affiliation: University of Bath, University College Cork

Abstract

BackgroundPhotorhabdus are Gram negative bacteria that are pathogenic to insect larvae whilst also having a mutualistic interaction with nematodes from the family Heterorhabditis. Iron is an essential nutrient and bacteria have different mechanisms for obtaining both the ferrous (Fe2+) and ferric (Fe3+) forms of this metal from their environments. In this study we were interested in analyzing the role of Fe3+ and Fe2+ iron uptake systems in the ability of Photorhabdus to interact with its invertebrate hosts.ResultsWe constructed targeted deletion mutants of exbD, feoABC and yfeABCD in P. luminescens TT01. The exbD mutant was predicted to be crippled in its ability to obtain Fe3+ and we show that this mutant does not grow well in iron-limited media. We also show that this mutant was avirulent to the insect but was unaffected in its symbiotic interaction with Heterorhabditis. Furthermore we show that a mutation in feoABC (encoding a predicted Fe2+ permease) was unaffected in both virulence and symbiosis whilst the divalent cation transporter encoded by yfeABCD is required for virulence in the Tobacco Hornworm, Manduca sexta (Lepidoptera) but not in the Greater Wax Moth, Galleria mellonella (Lepidoptera). Moreover the Yfe transporter also appears to have a role during colonization of the IJ stage of the nematode.ConclusionIn this study we show that iron uptake (via the TonB complex and the Yfe transporter) is important for the virulence of P. luminescens to insect larvae. Moreover this study also reveals that the Yfe transporter appears to be involved in Mn2+-uptake during growth in the gut lumen of the IJ nematode. Therefore, the Yfe transporter in P. luminescens TT01 is important during colonization of both the insect and nematode and, moreover, the metal ion transported by this pathway is host-dependent.

Highlights

Photorhabdus are Gram negative bacteria that are pathogenic to insect larvae whilst having a mutualistic interaction with nematodes from the family Heterorhabditis
Genetic analysis of iron uptake systems in P. luminescens TT01 We have previously shown that the exbD gene is important for both virulence and symbiosis in P. temperata (Pt) K122 [11]
The P. luminescens (Pl) TT01 genome is predicted to encode a variety of siderophores, it is interesting that the phb genes, encoding the proteins required for photobactin biosynthesis, are not present [19]

Summary

Introduction

Photorhabdus are Gram negative bacteria that are pathogenic to insect larvae whilst having a mutualistic interaction with nematodes from the family Heterorhabditis. Mutations in the cipA and cipB genes of Photorhabdus luminescens NC1 resulted in a strain that was unable to support nematode growth and development [7]. It has been shown that overproduction of CipA and CipB in E. coli can improve the growth and development of Steinernema nematodes implying some role for these proteins in nematode nutrition [8]. We have recently shown that a mutation in the exbD gene of Photorhabdus temperata K122 was unable to support the growth and development of its nematode partner, H. downesi [11]. The defect in symbiosis of the K122 exbD mutant was rescued by the addition of FeCl3 to the media suggesting that siderophore-mediated iron uptake was important for nematode growth and development [11]

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