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

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.

A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition

“…Regulation of T6SS by Fur or iron has also been reported in E. coli , Edwardsiella tarda , Burkholderia mallei and Burkholderia pseudomallei s535455. Finally, a T6SS in Pseudomonas taiwanensis was recently shown to be involved in the secretion of the iron chelator pyoverdine by a yet unidentified mechanism56. Together, these observations suggest that iron uptake may be a common function of T6SSs.…”

Iron Uptake Analysis in a Set of Clinical Isolates of Pseudomonas putida

“…PvdRT and OpmQ mediate the transport of the newly synthesized pyoverdine across the outer membrane and the recycling of pyoverdines. The FvpA receptor is a TonB-transporter family protein involved in pyoverdine-Fe sensing and internalization (Imperi et al, 2009; Cornelis, 2010; Schalk and Guillon, 2013; Gasser et al, 2015; Chen et al, 2016). fpvI that encodes for a RNA polymerase ECF-type sigma factor is also present in all the strains at the same locus.…”

Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis

“…Together with the report that T6SS is involved in Zn 2+ uptake in Y. pseudotuberculosis (32), our finding of the involvement of T6SS in Mn 2+ uptake significantly expands the range of known functions of this specialized protein secretion system. Recently, Chen et al (53) reported that the T6SS in Pseudomonas taiwanensis is involved in the secretion of iron chelator pyoverdine. Although the secretion mechanism of pyoverdine remains unidentified, this study implies the role of T6SS in iron uptake.…”