by binding to the LuxR-type receptor and inducing its
proteolysis (Manefield et al. 2002). Production of furanones
is thought to limit bacterial colonization and prevent
expression of virulence phenotypes controlled by AHLs.
The unicellular alga Chlamydomonas reinhardtii produces
a dozen compounds that stimulate functions regulated by
QS (Teplitski et al. 2004). Plants, especially legumes like
peas, soybean, and Medicago, exude different compounds
mimicking AHLs that stimulate or inhibit phenotypes
regulated by QS (Keshavan et al. 2005). Although most
of these compounds have not been characterized, their
discovery suggests that interactions established between
plants and pathogenic symbiotic or saprophytic bacteria
can be “manipulated” by plants.
9.3.4 Acyl Homoserines Lactones (AHLs),
Signals Only for Bacteria?
Several studies have revealed that eukaryotic organisms
might respond to AHLs. The first demonstration of a eukaryotic detection of AHLs comes from the stimulation of the
production of interleukin-8 by epithelial cells exposed to the
3-oxo-C12-HSL produced by P. aeruginosa (DiMango et al.
1995). Subsequently, immunomodulatory effects of AHLs
have been shown to play a direct role in pathogenicity
(Smith et al. 2002; Khajanchi et al. 2011).
In the marine environment, AHLs released by bacterial
biofilms can attract zoospores of the marine Viridiplantae
Ulva (Joint et al. 2002). When zoospores detect the AHL,
their rate of swimming is reduced and they aggregate near
the AHL source; AHLs would act as indicators for the
attachment of zoospores and would influence the biogeography of the seaweed.
In the rhizosphere, the model legume Medicago
truncatula responds to nanomolar or micromolar concentrations of two different long acyl chain AHLs and shows
significant changes in the accumulation of more than 150
proteins (Mathesius 2003); these proteins are involved in
functions related to defense, stress, transcriptional regulation, and hormone response. In addition, AHLs induce
changes in the exudation of compounds that mimic AHLs
(Mathesius et al. 2003). Plants may use the information
encoded by AHLs as a reliable means of detection, in order
to activate defense responses before the bacterial infection
occurs.
Inoculation of Serratia liquefaciens onto tomato plants
infected by the leaf pathogen Alternaria alternata increases
systemic resistance, a phenotype that is not observed when a
strain of Serratia defective in the synthesis of AHLs is used
(Schuhegger et al. 2006); in addition, C6-HSL induces a
systemic accumulation of salicylic acid and expression of
defense genes of the ethylene pathway in tomato. The
contact of Arabidopsis thaliana roots with C6-HSL induces
changes in gene expression in roots and also in aerial parts,
modifies the auxin/cytokinin ratio, and increases root elongation, whereas long-chain AHLs reinforce plant resistance
(von Rad et al. 2008; Schenk et al. 2012); such modifications
could be an integral part of the phytobeneficial effect of
some rhizosphere AHL-producing bacteria.
9.3.5 Other Bacterial Signal Molecules
N-acyl homoserine lactones are not the only class of signaling molecules used by prokaryotes. In Gram-negative bacteria, fatty acids (Xanthomonas campestris, Stenotrophomonas
maltophilia), esters of fatty acids (Ralstonia solanacearum),
and quinolones (P. aeruginosa, Burkholderia spp.) also
have a role as signal molecules (Fig. 9.16) (Vial et al.
2008). In P. aeruginosa, PQS signals are involved in the
hierarchical regulatory cascade leading to the synthesis of
AHLs. During nutritional deficiency, Myxococcus xanthus
secretes an unknown compound, which causes cells to clump
together and form a fruiting body; within this globular
aggregate which can consist of more than 100,000 bacteria,
some cells then turn into myxospores.
With the exception of Streptomyces that produce
γ-butyrolactones such as A-factor (Fig. 9.16, a compound
that controls sporulation and antibiotic production),
Firmicutes generally use autoinducer peptides (AIPs)
(Fig. 9.16). These peptides (from 5 to 34 amino acids) are
produced in the cytoplasm and are then modified (some are
cyclized) after translation and exported via a specific transporter. Above a threshold concentration, AIPs specifically
interact with a membrane histidine kinase; this interaction
stimulates the kinase activity, leading to phosphorylation
of a response regulator which can then bind to DNA and
control the transcription of target genes. The most studied
phenotypes regulated by AIPs are competence and sporulation in Bacillus subtilis, competence in Streptococcus
pneumoniae, expression of virulence factors and biofilm
formation in Staphylococcus aureus, and virulence in
Enterococcus faecalis (Lyon and Novick 2004). Differences
in the primary structure of AIPs result in a high degree of
specificity. In the human pathogen S. aureus, each of the four
AIPs is specifically recognized by a receptor (Lyon and
Novick 2004).
The use of peptides does not seem to be restricted to
Firmicutes since a linear pentapeptide involved in cell
death has recently been identified in E. coli (Kolodkin-Gal
et al. 2007).
Although no universal bacterial QS system has been
discovered, many Gram negative and Gram positive produce
autoinducer-2 (AI-2) (Fig. 9.16, a collective term for a group
of interconvertible furanones). The luxS gene required for
316
P. Normand et al.
proteolysis (Manefield et al. 2002). Production of furanones
is thought to limit bacterial colonization and prevent
expression of virulence phenotypes controlled by AHLs.
The unicellular alga Chlamydomonas reinhardtii produces
a dozen compounds that stimulate functions regulated by
QS (Teplitski et al. 2004). Plants, especially legumes like
peas, soybean, and Medicago, exude different compounds
mimicking AHLs that stimulate or inhibit phenotypes
regulated by QS (Keshavan et al. 2005). Although most
of these compounds have not been characterized, their
discovery suggests that interactions established between
plants and pathogenic symbiotic or saprophytic bacteria
can be “manipulated” by plants.
9.3.4 Acyl Homoserines Lactones (AHLs),
Signals Only for Bacteria?
Several studies have revealed that eukaryotic organisms
might respond to AHLs. The first demonstration of a eukaryotic detection of AHLs comes from the stimulation of the
production of interleukin-8 by epithelial cells exposed to the
3-oxo-C12-HSL produced by P. aeruginosa (DiMango et al.
1995). Subsequently, immunomodulatory effects of AHLs
have been shown to play a direct role in pathogenicity
(Smith et al. 2002; Khajanchi et al. 2011).
In the marine environment, AHLs released by bacterial
biofilms can attract zoospores of the marine Viridiplantae
Ulva (Joint et al. 2002). When zoospores detect the AHL,
their rate of swimming is reduced and they aggregate near
the AHL source; AHLs would act as indicators for the
attachment of zoospores and would influence the biogeography of the seaweed.
In the rhizosphere, the model legume Medicago
truncatula responds to nanomolar or micromolar concentrations of two different long acyl chain AHLs and shows
significant changes in the accumulation of more than 150
proteins (Mathesius 2003); these proteins are involved in
functions related to defense, stress, transcriptional regulation, and hormone response. In addition, AHLs induce
changes in the exudation of compounds that mimic AHLs
(Mathesius et al. 2003). Plants may use the information
encoded by AHLs as a reliable means of detection, in order
to activate defense responses before the bacterial infection
occurs.
Inoculation of Serratia liquefaciens onto tomato plants
infected by the leaf pathogen Alternaria alternata increases
systemic resistance, a phenotype that is not observed when a
strain of Serratia defective in the synthesis of AHLs is used
(Schuhegger et al. 2006); in addition, C6-HSL induces a
systemic accumulation of salicylic acid and expression of
defense genes of the ethylene pathway in tomato. The
contact of Arabidopsis thaliana roots with C6-HSL induces
changes in gene expression in roots and also in aerial parts,
modifies the auxin/cytokinin ratio, and increases root elongation, whereas long-chain AHLs reinforce plant resistance
(von Rad et al. 2008; Schenk et al. 2012); such modifications
could be an integral part of the phytobeneficial effect of
some rhizosphere AHL-producing bacteria.
9.3.5 Other Bacterial Signal Molecules
N-acyl homoserine lactones are not the only class of signaling molecules used by prokaryotes. In Gram-negative bacteria, fatty acids (Xanthomonas campestris, Stenotrophomonas
maltophilia), esters of fatty acids (Ralstonia solanacearum),
and quinolones (P. aeruginosa, Burkholderia spp.) also
have a role as signal molecules (Fig. 9.16) (Vial et al.
2008). In P. aeruginosa, PQS signals are involved in the
hierarchical regulatory cascade leading to the synthesis of
AHLs. During nutritional deficiency, Myxococcus xanthus
secretes an unknown compound, which causes cells to clump
together and form a fruiting body; within this globular
aggregate which can consist of more than 100,000 bacteria,
some cells then turn into myxospores.
With the exception of Streptomyces that produce
γ-butyrolactones such as A-factor (Fig. 9.16, a compound
that controls sporulation and antibiotic production),
Firmicutes generally use autoinducer peptides (AIPs)
(Fig. 9.16). These peptides (from 5 to 34 amino acids) are
produced in the cytoplasm and are then modified (some are
cyclized) after translation and exported via a specific transporter. Above a threshold concentration, AIPs specifically
interact with a membrane histidine kinase; this interaction
stimulates the kinase activity, leading to phosphorylation
of a response regulator which can then bind to DNA and
control the transcription of target genes. The most studied
phenotypes regulated by AIPs are competence and sporulation in Bacillus subtilis, competence in Streptococcus
pneumoniae, expression of virulence factors and biofilm
formation in Staphylococcus aureus, and virulence in
Enterococcus faecalis (Lyon and Novick 2004). Differences
in the primary structure of AIPs result in a high degree of
specificity. In the human pathogen S. aureus, each of the four
AIPs is specifically recognized by a receptor (Lyon and
Novick 2004).
The use of peptides does not seem to be restricted to
Firmicutes since a linear pentapeptide involved in cell
death has recently been identified in E. coli (Kolodkin-Gal
et al. 2007).
Although no universal bacterial QS system has been
discovered, many Gram negative and Gram positive produce
autoinducer-2 (AI-2) (Fig. 9.16, a collective term for a group
of interconvertible furanones). The luxS gene required for
316
P. Normand et al.