Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis.

Tietao Wang,Qinqin Pu,Yarong Wang,Min Wu,Linxuan Ji,Haihua Liang,Jing Wen,Yuying Han,Jing Dang,Xiao Du

doi:10.1016/j.celrep.2021.108957

Abstract

Type VI secretion system (T6SS) is widely distributed in Gram-negative bacteria and functions as a versatile protein export machinery that translocates effectors into eukaryotic or prokaryotic target cells. Growing evidence indicates that T6SS can deliver several effectors to promote bacterial survival in harmful environments through metal ion acquisition. Here, we report that the Pseudomonas aeruginosa H2-T6SS mediates molybdate (MoO42-) acquisition by secretion of a molybdate-binding protein, ModA. The expression of H2-T6SS genes is activated by the master regulator Anr and anaerobiosis. We also identified a ModA-binding protein, IcmP, an insulin-cleaving metalloproteinase outer membrane protein. The T6SS-ModA-IcmP system provides P.aeruginosa with a growth advantage in bacterial competition under anaerobic conditions and plays an important role in bacterial virulence. Overall, this study clarifies the role of T6SS in secretion of an anion-binding protein, emphasizing the fundamental importance of this bacterium using T6SS-mediated molybdate uptake to adapt to complex environmental conditions.

Highlights

Bacteria use diverse specialized secretion systems to deliver proteins to the extracellular environment or host cell cytosol (Abdallah et al, 2007; Hood et al, 2010)
T6SS4 in Yersinia pseudotuberculosis, H3-T6SS in P. aeruginosa, and T6SS-4 in Burkholderia thailandensis deliver YezP (Wang et al, 2015), TseF (Lin et al, 2017), and TseZ (Si et al, 2017a)/TseM (Si et al, 2017b), respectively, to the extracellular milieu for metal ion acquisition to deal with environmental niches and improve interbacterial competition
The secretion of ModA is regulated by H2-T6SS In our previous secretome analysis, we found that the abundance of ModA was much lower in the DretSDclpV2 mutant than in the DretS strain, indicating that ModA is a potent substrate for H2-T6SS

Summary

Introduction

Bacteria use diverse specialized secretion systems to deliver proteins to the extracellular environment or host cell cytosol (Abdallah et al, 2007; Hood et al, 2010). The best-studied function of T6SSs is their antibacterial activity, whereby effectors capable of killing competitive bacterial species are delivered into target cells in a contact-dependent manner (Jiang et al, 2014; Russell et al, 2013). P. aeruginosa H1-T6SS delivers two effector proteins, namely, Tse and Tse, to the periplasm of recipient cells; both of these proteins hydrolyze peptidoglycan and provide a competitive fitness advantage (Russell et al, 2011). The expression of T6SS is regulated by multiple elements at the transcriptional and posttranslational level Both H1- and H2-T6SS are repressed by the hybrid sensor RetS, which regulates the two-component GacS/GacA and Rsm signaling pathway (Burkinshaw et al, 2018; Mougous et al, 2006). H2-T6SS and H3-T6SS are co-regulated by the Las and Rhl quorum-sensing systems and repressed by RsmA and AmrZ (Allsopp et al, 2017; Lesic et al, 2009)

Results

Discussion

Conclusion