Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals

Abstract

Many bacteria use N-acyl homoserine lactone (AHL) signals to coordinate the behavior of individual cells in a local population. The successful infection of eukaryotic hosts by bacteria seems to depend particularly on such AHL-mediated ''quorum-sensing'' regulation. We have used proteome analysis to show that a eukaryotic host, the model legume Medicago truncatula, is able to detect nanomolar to micromolar concentrations of bacterial AHLs from both symbiotic (Sinorhizobium meliloti) and pathogenic (Pseudomonas aeruginosa) bacteria, and that it responds in a global manner by significant changes in the accumulation of over 150 proteins, 99 of which have been identified by peptide mass fingerprinting. The accumulation of specific proteins and isoforms depended on AHL structure, concentration, and time of exposure. AHLs were also found to induce tissue-specific activation of ␤-glucuronidase (GUS) reporter fusions to an auxin-responsive and three chalcone synthase promoters, consistent with AHL-induced changes in the accumulation of auxin-responsive and flavonoid synthesis proteins. In addition, exposure to AHLs was found to induce changes in the secretion of compounds by the plants that mimic quorum-sensing signals and thus have the potential to disrupt quorum sensing in associated bacteria. Our results indicate that eukaryotes have an extensive range of functional responses to AHLs that may play important roles in the beneficial or pathogenic outcomes of eukaryote-prokaryote interactions.

Exploiting Quorum Sensing To Confuse Bacterial Pathogens

“…Roots of the model host plant Medicago truncatula (legume), used to study symbiotic relationships with Sinorhizobium meliloti and pathogenic relationships with P. aeruginosa, were treated with nanomolar concentrations of AHLs, and subsequent changes in the plant proteome were measured (263). Cellular levels of at least 154 proteins were found to significantly change in the presence of AHLs, with concentrations of some increasing and those of others decreasing.…”

“…Cellular levels of at least 154 proteins were found to significantly change in the presence of AHLs, with concentrations of some increasing and those of others decreasing. Astonishingly, the response to AHL treatments included secretions by the root tissues that contained compounds having QS agonist properties that were able to induce a LasR reporter, as well as QS-inhibiting properties that were able to block an AI-2-based reporter (263). Though studies have yet to identify the compounds produced by the plant roots, the work offers a glimpse of the complex interplay between plants and microbes, whether their relationships are symbiotic or pathogenic.…”

N-3-Oxo-Decanoyl-l-Homoserine-Lactone Activates Auxin-Induced Adventitious Root Formation via Hydrogen Peroxide- and Nitric Oxide-Dependent Cyclic GMP Signaling in Mung Bean

“…Recently, more evidence demonstrate that AHLs are able to modulate plant growth and development (Mathesius et al, 2003;Ortíz-Castro et al, 2008;von Rad et al, 2008;Méndez-Bravo et al, 2010;MorquechoContreras et al, 2010). In Arabidopsis, treatment with AHLs alters primary growth, lateral root formation, and root hair development; specifically, AHLs with different lengths of unmodified branched chains differentially affect the root architecture.…”

“…For example, C10-HL treatment was unable to enhance GUS activity in Arabidopsis transgenic seedlings harboring the auxinresponse DR5:uidA gene construct (Ortíz-Castro et al, 2008). However, Mathesius et al (2003) reported that AHLs with an acyl-substituted branched chain, such as 3-O-C12-HL and 3-O-C16-HL, induce the tissue-specific activation of the auxin-response GH3 and the chalcone synthase genes in the model legume M. truncatula; these findings imply that there is some level of variability in auxin signaling in response to AHLs. To confirm this, we measured the abilities of various AHLs to activate polar auxin transport .We found that the AHLs with an acyl-modified branched chain at the C3 position, such as 3-O-C10-HL, 3-O-C8-HL, and 3-O-C12-HL, could efficiently promote polar auxin transport, with 3-O-C10-HL showing the greatest response (Fig.…”

“…Recent evidence indicates that plants are able to perceive AHLs; the application of AHLs to Arabidopsis or Medicago truncatula results in distinct transcriptional changes in the roots and shoots and affects primary root growth, lateral root formation, and root hair development (Mathesius et al, 2003;Ortíz-Castro et al, 2008;von Rad et al, 2008;Morquecho-Contreras et al, 2010). Similar to the structure of AHLs, the fatty acid amides, including N-acyl-ethanolamines (NAEs) and alkamides in plants, are also capable of regulating root and shoot architecture (Laxalt and Munnik, 2002;Campos-Cuevas et al, 2008;Morquecho-Contreras et al, 2010), and the Arabidopsis recessive mutant decanamide-resistant root1 (drr1) was isolated based on its continuous primary root and reduced lateral root formation in response to decanamide (an alkamide) or AHLs (Morquecho-Contreras et al, 2010).…”