scholarly journals The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity

2020 ◽  
Vol 3 (10) ◽  
pp. e202000720
Author(s):  
Tuan Minh Tran ◽  
Zhiming Ma ◽  
Alexander Triebl ◽  
Sangeeta Nath ◽  
Yingying Cheng ◽  
...  

Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern–triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern–triggered host immunity.

2020 ◽  
Author(s):  
Tuan Minh Tran ◽  
Zhiming Ma ◽  
Alexander Triebl ◽  
Sangeeta Nath ◽  
Yingying Cheng ◽  
...  

AbstractQuorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely under-studied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of oligomerization states and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase of the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate PAMP-triggered host immunity.SIGNIFICANCE STATEMENTBacteria rely on small signalling molecules called quorum sensing (QS) signals to communicate and coordinate their behaviors. QS is known to regulate gene expression, production of virulence factors, and biofilm formation for pathogenic bacteria to effectively colonize their hosts and cause diseases. In this work, we found a class of QS molecule called diffusible-signal factor (DSF), produced by devastating phytopathogenic bacteria such as Xanthomonas spp. and Xylella fastidiosa, could communicate directly with plant host and subvert plant innate immunity by inducing plant sterol production and thereby, attenuating receptor signalling through hindering the receptor clustering and plant endocytosis. The results significantly enrich our understanding of the mechanisms in the tug-of-war between bacterial pathogenesis and host immunity.


Author(s):  
Salvador Barrera-Ortiz ◽  
Claudia Marina López-García ◽  
Randy Ortiz-Castro ◽  
Ángel Arturo Guevara-García ◽  
José López-Bucio

2020 ◽  
Vol 74 (1) ◽  
pp. 201-219 ◽  
Author(s):  
Sheyda Azimi ◽  
Alexander D. Klementiev ◽  
Marvin Whiteley ◽  
Stephen P. Diggle

Bacteria are highly interactive and possess an extraordinary repertoire of intercellular communication and social behaviors, including quorum sensing (QS). QS has been studied in detail at the molecular level, so mechanistic details are well understood in many species and are often involved in virulence. The use of different animal host models has demonstrated QS-dependent control of virulence determinants and virulence in several human pathogenic bacteria. QS also controls virulence in several plant pathogenic species. Despite the role QS plays in virulence during animal and plant laboratory-engineered infections, QS mutants are frequently isolated from natural infections, demonstrating that the function of QS during infection and its role in pathogenesis remain poorly understood and are fruitful areas for future research. We discuss the role of QS during infection in various organisms and highlight approaches to better understand QS during human infection. This is an important consideration in an era of growing antimicrobial resistance, when we are looking for new ways to target bacterial infections.


Planta ◽  
2008 ◽  
Vol 229 (1) ◽  
pp. 73-85 ◽  
Author(s):  
Uta von Rad ◽  
Ilona Klein ◽  
Petre I. Dobrev ◽  
Jana Kottova ◽  
Eva Zazimalova ◽  
...  

PLoS ONE ◽  
2014 ◽  
Vol 9 (12) ◽  
pp. e115232 ◽  
Author(s):  
Yu-Yuan Chen ◽  
Jiann-Chu Chen ◽  
Yong-Chin Lin ◽  
Suwaree Kitikiew ◽  
Hui-Fang Li ◽  
...  

2010 ◽  
Vol 285 (50) ◽  
pp. 39140-39149 ◽  
Author(s):  
Nana F. Keinath ◽  
Sylwia Kierszniowska ◽  
Justine Lorek ◽  
Gildas Bourdais ◽  
Sharon A. Kessler ◽  
...  

2019 ◽  
Author(s):  
Justin E. Silpe ◽  
Bonnie L. Bassler

AbstractQuorum sensing (QS) is a process of cell-to-cell communication that bacteria use to orchestrate collective behaviors. QS relies on the cell-density-dependent production, accumulation, and receptor-mediated detection of extracellular signaling molecules called autoinducers (AIs). Gram-negative bacteria commonly use N-acyl homoserine lactones (AHLs) as their AIs and they are detected by LuxR-type receptors. Often, LuxR-type receptors are insoluble when not bound to a cognate AI. In this report, we show that LuxR-type receptors are encoded on phage genomes and, in the cases we tested, the phage LuxR-type receptors bind to and are solubilized specifically by the AHL AI produced by the host bacterium. We do not yet know the viral activities that are controlled by these phage QS receptors, however, our observations, coupled with recent reports, suggest that their occurrence is more widespread than previously appreciated. Using receptor-mediated detection of QS AIs could enable phages to garner information concerning the population density status of their bacterial hosts. We speculate that such information can be exploited by phages to optimize the timing of execution of particular steps in viral infection.ImportanceBacteria communicate with chemical signal molecules to regulate group behaviors in a process called quorum sensing (QS). In this report, we find that genes encoding receptors for Gram-negative bacterial QS communication molecules are present on genomes of viruses that infect these bacteria. These viruses are called phages. We show that two phage-encoded receptors, like their bacterial counterparts, bind to the communication molecule produced by the host bacterium, suggesting that phages can “listen in” on their bacterial hosts. Interfering with bacterial QS and using phages to kill pathogenic bacteria represent attractive possibilities for development of new antimicrobials to combat pathogens that are resistant to traditional antibiotics. Our findings of interactions between phages and QS bacteria need consideration as new antimicrobial therapies are developed.


Pathogens ◽  
2020 ◽  
Vol 9 (10) ◽  
pp. 787
Author(s):  
Raeesa H. Hussan ◽  
Ian A. Dubery ◽  
Lizelle A. Piater

Lipopolysaccharides (LPS) are recognized as microbe-associated molecular patterns (MAMPs) responsible for eliciting defense-related responses and while the effects have been well-documented in mammals, there is a lack of knowledge regarding the mechanism of perception in plant systems and recognized structural moieties within the macromolecular lipoglycan structure. Thus, identification of the LPS plasma membrane (PM) receptor(s)/receptor complex in Arabidopsis thaliana through proteomics will contribute to a deeper understanding of induced defense responses. As such, structurally characterized LPS chemotypes from Xanthomonas campestris pv. campestris (Xcc) wild-type 8004 (prototypical smooth-type LPS) and mutant 8530 (truncated core with no O–chain) strains were utilized to pre-treat A. thaliana plants. The associated proteomic response/changes within the PM were compared over a 24 h period using mass spectrometry-based methodologies following three variants of LPS-immobilized affinity chromatography. This resulted in the identification of proteins from several functional categories, but importantly, those involved in perception and defense. The distinct structural features between wild-type and mutant LPS are likely responsible for the differential changes to the proteome profiles, and many of the significant proteins were identified in response to the wild-type Xcc LPS where it is suggested that the core oligosaccharide and O-chain participate in recognition by receptor-like kinases (RLKs) in a multiprotein complex and, notably, varied from that of the mutant chemotype.


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