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Involvement of type VI secretion system in secretion of iron chelator pyoverdine in Pseudomonas taiwanensis

View Article: PubMed Central - PubMed

ABSTRACT

Rice bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) is one of the most destructive rice diseases worldwide. Therefore, in addition to breeding disease-resistant rice cultivars, it is desirable to develop effective biocontrol agents against Xoo. Here, we report that a soil bacterium Pseudomonas taiwanensis displayed strong antagonistic activity against Xoo. Using matrix-assisted laser desorption/ionization imaging mass spectrometry, we identified an iron chelator, pyoverdine, secreted by P. taiwanensis that could inhibit the growth of Xoo. Through Tn5 mutagenesis of P. taiwanensis, we showed that mutations in genes that encode components of the type VI secretion system (T6SS) as well as biosynthesis and maturation of pyoverdine resulted in reduced toxicity against Xoo. Our results indicated that T6SS is involved in the secretion of endogenous pyoverdine. Mutations in T6SS component genes affected the secretion of mature pyoverdine from the periplasmic space into the extracellular medium after pyoverdine precursor is transferred to the periplasm by the inner membrane transporter PvdE. In addition, we also showed that other export systems, i.e., the PvdRT-OpmQ and MexAB-OprM efflux systems (for which there have been previous suggestions of involvement) and the type II secretion system (T2SS), are not involved in pyoverdine secretion.

No MeSH data available.


Schematic of the pyoverdine secretion pathways in P. taiwanensis.Pyoverdine precursors are synthesized in the cytoplasm and secreted into the periplasm by the inner membrane transporter PvdE, and then form mature fluorescent pyoverdine in the periplasmic space74445. There are three possibilities that can explain the secretory pathways of pyoverdine: (1) pyoverdine adheres to T6SS tube structure and secretes into the culture medium after pushing the Hcp tube with the VgrG spike; (2) pyoverdine secretes into medium through passive diffusion after T6SS punches a hole in the outer-membrane; (3) pyoverdine is secreted via an unknown export system.
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f8: Schematic of the pyoverdine secretion pathways in P. taiwanensis.Pyoverdine precursors are synthesized in the cytoplasm and secreted into the periplasm by the inner membrane transporter PvdE, and then form mature fluorescent pyoverdine in the periplasmic space74445. There are three possibilities that can explain the secretory pathways of pyoverdine: (1) pyoverdine adheres to T6SS tube structure and secretes into the culture medium after pushing the Hcp tube with the VgrG spike; (2) pyoverdine secretes into medium through passive diffusion after T6SS punches a hole in the outer-membrane; (3) pyoverdine is secreted via an unknown export system.

Mentions: A schematic summary of pyoverdine transportation in P. taiwanensis is shown in Fig. 8. Our studies on the involvement of T6SS in the secretion of pyoverdine produced several interesting findings. Our results showed that T6SS is necessary for the secretion of wild-type levels of pyoverdine. However, the mechanism for the involvement of T6SS in the secretion of a small molecule remains to be elucidated. Based on the current results, there are three possible explanations of the secretory routes of pyoverdine: (1) pyoverdine adheres to the T6SS tube and secretes into culture medium after pushing the Hcp tube with the VgrG spike or via T6SS in a specific manner; (2) pyoverdine can be secreted into medium via passive diffusion during ejection of a T6SS Hcp-VgrG puncturing device; (3) secretion via an unknown export system. In addition to the above possibilities, we cannot exclude the possibility that T6SS is a signal in the regulation of pyoverdine secretion.


Involvement of type VI secretion system in secretion of iron chelator pyoverdine in Pseudomonas taiwanensis
Schematic of the pyoverdine secretion pathways in P. taiwanensis.Pyoverdine precursors are synthesized in the cytoplasm and secreted into the periplasm by the inner membrane transporter PvdE, and then form mature fluorescent pyoverdine in the periplasmic space74445. There are three possibilities that can explain the secretory pathways of pyoverdine: (1) pyoverdine adheres to T6SS tube structure and secretes into the culture medium after pushing the Hcp tube with the VgrG spike; (2) pyoverdine secretes into medium through passive diffusion after T6SS punches a hole in the outer-membrane; (3) pyoverdine is secreted via an unknown export system.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5015096&req=5

f8: Schematic of the pyoverdine secretion pathways in P. taiwanensis.Pyoverdine precursors are synthesized in the cytoplasm and secreted into the periplasm by the inner membrane transporter PvdE, and then form mature fluorescent pyoverdine in the periplasmic space74445. There are three possibilities that can explain the secretory pathways of pyoverdine: (1) pyoverdine adheres to T6SS tube structure and secretes into the culture medium after pushing the Hcp tube with the VgrG spike; (2) pyoverdine secretes into medium through passive diffusion after T6SS punches a hole in the outer-membrane; (3) pyoverdine is secreted via an unknown export system.
Mentions: A schematic summary of pyoverdine transportation in P. taiwanensis is shown in Fig. 8. Our studies on the involvement of T6SS in the secretion of pyoverdine produced several interesting findings. Our results showed that T6SS is necessary for the secretion of wild-type levels of pyoverdine. However, the mechanism for the involvement of T6SS in the secretion of a small molecule remains to be elucidated. Based on the current results, there are three possible explanations of the secretory routes of pyoverdine: (1) pyoverdine adheres to the T6SS tube and secretes into culture medium after pushing the Hcp tube with the VgrG spike or via T6SS in a specific manner; (2) pyoverdine can be secreted into medium via passive diffusion during ejection of a T6SS Hcp-VgrG puncturing device; (3) secretion via an unknown export system. In addition to the above possibilities, we cannot exclude the possibility that T6SS is a signal in the regulation of pyoverdine secretion.

View Article: PubMed Central - PubMed

ABSTRACT

Rice bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) is one of the most destructive rice diseases worldwide. Therefore, in addition to breeding disease-resistant rice cultivars, it is desirable to develop effective biocontrol agents against Xoo. Here, we report that a soil bacterium Pseudomonas taiwanensis displayed strong antagonistic activity against Xoo. Using matrix-assisted laser desorption/ionization imaging mass spectrometry, we identified an iron chelator, pyoverdine, secreted by P. taiwanensis that could inhibit the growth of Xoo. Through Tn5 mutagenesis of P. taiwanensis, we showed that mutations in genes that encode components of the type VI secretion system (T6SS) as well as biosynthesis and maturation of pyoverdine resulted in reduced toxicity against Xoo. Our results indicated that T6SS is involved in the secretion of endogenous pyoverdine. Mutations in T6SS component genes affected the secretion of mature pyoverdine from the periplasmic space into the extracellular medium after pyoverdine precursor is transferred to the periplasm by the inner membrane transporter PvdE. In addition, we also showed that other export systems, i.e., the PvdRT-OpmQ and MexAB-OprM efflux systems (for which there have been previous suggestions of involvement) and the type II secretion system (T2SS), are not involved in pyoverdine secretion.

No MeSH data available.