Ciência e Tecnologia de Alimentos
Sociedade Brasileira de Ciência e
Tecnologia de Alimentos
Barbosa SACRAMENTO, Nayara Thais; Corrêa BERTOLDI, Michele; PINTO, Uelinton
Anti-quorum sensing activity of phenolic extract from Eugenia brasiliensis (Brazilian
Ciência e Tecnologia de Alimentos, vol. 36, núm. 2, abril-junio, 2016, pp. 337-343
Sociedade Brasileira de Ciência e Tecnologia de Alimentos
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Bacteria coordinate gene expression as a function of cell
density in a communication mechanism named quorum sensing
(Fuqua et al., 1994). This process occurs through the production,
release and detection of signaling molecules by bacterial cells
(González & Keshava, 2006). The signaling molecules are usually
termed as autoinducers belonging to the acyl homoserine lactone
(AHL) group, commonly referred to as autoinducer 1 (AI-1),
which are used by Gram-negative bacteria; autoinducer peptides
(AIP) used by Gram-positive bacteria; and autoinducer 2 type
molecules (AI-2) used by both groups. Dther types of signaling
molecules such as p-coumaryl-homoserine lactone, unsaturated
fatty acids, quinolone, and a substituted alkane, among others
have also been described (Tsai & Winans, 2010).
Through the quorum sensing system bacteria are capable of
performing tasks as a group such as migration to more favorable
environments, biofilm formation, virulence gene expression,
bacteriocin and antibiotic production, bioluminescence, pigment
production, among others (Martins et al., 2014; Skandamis &
Nychas, 2012). The system has also been shown to regulate
bacterial behaviors in food ecosystems highlighting the importance
of understanding its control in order to improve food safety
and quality (Bai & Rai, 2011; Pinto et al., 2007; Skandamis &
A disruption in any of the steps required for the quorum
sensing communication could interfere with microbial pathogenesis
and aid in bacterial control (González & Keshava, 2006; Hentzer
& Givskov, 2003). This approach is part of a broader group of
antivirulence strategies (Rasko & Sperandio, 2010). Therefore,
quorum sensing inhibition can be accomplished by interfering
with the synthesis, secretion and degradation of the autoinducers,
as well as by hampering their recognition by receptor proteins
such as the LuxR type homologs, which recognize AHLs. The idea
of using quorum sensing inhibitors arises from the fact that they
target virulence factors with minimal to no effect on bacterial
growth which could potentially decrease the risk of selecting for
bacterial resistant strains (Dong et al., 2001; Hentzer et al., 2003).
Some natural compounds inhibit quorum sensing and it
has been argued that this effect could have great implications in
Anti-quorum sensing activity of phenolic extract
from Eugenia brasiliensis (Brazilian cherry)
Adeline Conceição RDDRIGUES
, Brígida D’Ávila de DLIVEIRA
, Elis Regina da SILVA
, Michele Corrêa BERTDLDI
, Uelinton Manoel PINTD
Accepted 22 Mar., 2016
Departamento de Alimentos, Universidade Federal de Ouro Preto – UFOP, Ouro Preto, MG, Brazil
Pharmaceutical Department, Faculty of Pharmacy and Biochemistry, Universidade Federal de Juiz de Fora – UFJF, Governador Valadares, MG, Brazil
Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, Universidade de São Paulo - USP, São Paulo, SP, Brazil
The aim of this study was to assess the anti-quorum sensing activity of phenolic extracts from grumixama (Eugenia brasiliensis),
also known as Brazilian cherry, in concentrations that did not interfere with bacterial growth. The pulp phenolic compounds
were extracted by using solid phage extraction in a mini-collumn C18 and quantified by spectrophotometry. The anti-quorum
sensing activity was evaluated by testing the inhibition of violacein production in Chromobacterium violaceum and by evaluating
the swarming motility in Aeromonas hydrophila and Serratia marcescens, both phenotypes regulated by quorum sensing.
The phenolic extract strongly inhibited the production of violacein in C. violaceum, reducing its production in comparison with
a control with no extract. No inhibition of growth was observed at the concentrations tested for quorum sensing inhibition.
Confirming the quorum sensing inhibition phenotype, the extract was also able to inhibit swarming motility in S. marcescens
and in A. hydrophila, although in the later the effect was marginal. Dverall, these results indicate that phenolic extract from
E. brasiliensis presents quorum sensing inhibitory activity most likely due to the presence of fruit phenolics which have been
implicated as quorum sensing inhibitors in Gram negative bacteria.
industries due to inhibition of phenotypes regulated by quorum sensing, which include production of virulence factors and
spoilage enzymes. By inhibiting phenotypes associated with quorum sensing, the extract presents potential application as a
natural preservative for food conservation and as an alternative or an adjuvant with antibiotics.
Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016
antivirulence strategies (Adonizio et al., 2008). The combination
generate synergistic effects promoting more effective control
against bacterial infections in plants, animals and humans
Some studies have shown that plant phenolic compounds
can interfere with bacterial quorum sensing (Borges et al., 2014;
Issac Abraham et al., 2011). Phenolic compounds are secondary
metabolites found in plants and plant derived foods such as fruits,
teas and red wine (Haminiuk et al., 2012). They are used by the
plants against phytopathogens, radiation and are involved in
antioxidant events (Tiveron et al., 2012). Phenolic compounds
are associated with stress response in plants and have recognized
antimicrobial properties (Martins et al., 2015).
Eugenia brasiliensis, popularly known as grumixama or
Brazilian cherry, is a fruit from the Myrtaceae family, and
it has been shown to be a source of phenolic compounds
(Moreno et al., 2007). The essential oil extracted from its leaves
presented anti-diarrhea, anti-fever, anti-infllamatory, and
antibacterial activities (Magina et al., 2009). Little is known
about the antimicrobial effects of the fruit and no study has been
found reporting its anti-quorum sensing activity. Therefore,
this work aimed at evaluating the quorum sensing inhibitory
potential of phenolic extracts obtained from E. brasiliensis fruit
against commonly phenotypes regulated by quorum sensing
in Chromobacterium violaceum, Aeromonas hydrophila and
Serratia marcescens (Morohoshi et al., 2007; Pinto et al., 2007;
Ponce-Rossi et al., 2016).
2 Materials and methods
2.1 Extract preparation
Fruits of E. brasiliensis were collected in the county of Duro
Preto – MG. The fruits were washed and sanitized with sodium
hypochloride at 50 mg L
for 15 min. The seeds were manually
until use. Phenolic compounds were extracted as previously
described (Bertoldi, 2009). Briefly, the fruit pulp was thawed and
mixed with ethanol:methanol:acetone 1:1:1 (v/v/v), followed by
filtration in Whatman paper n° 1. Then, the resulting extract was
evaporated in rotary evaporator at 40 °C (Büchi, Switzerland)
and the remaining aqueous extract applied to a mini-column
C18 Sep-Pak Vac 35cc 10 g 20 cm
compounds. The adsorbed phenolic compounds were eluted
from the column with methanol, while the aqueous fraction
was discarded. Then, methanol was completely evaporated in
rotary evaporator at 40 °C and distilled water was added with
the resulting product named phenolic extract. The term phenolic
extract used frequently within this report has no relation to the
solvent system used to obtain the extract. Phenol was not used
as an extraction solvent and instead the term phenolic extract
is used to describe an extract enriched in phenolic compounds.
The total phenolic content of the extracts was determined by the
Folin-Ciocalteu assay (Shahidi & Naczk, 1996) and expressed
as mg of galic acid equivalent per L (mg GAE L
Bacterial strains and culture conditions
C. violaceum ATCC6357 was cultured at 28 and 30 °C,
A. hydrophila IDC/FDA110-36 at 37 °C and S. marcescens at
30° C in Luria Bertani (LB) broth containing peptone 1%, yeast
extract 0.5% and NaCl 0.5% (instead of 1.0%) (Ravn et al., 2001).
Agar diffusion assay with C. violaceum ATCC6357
The assay was performed according to Tan et al. (2012),
with modifications. Aliquots of 1 mL were mixed to 20 mL of
fused LB agar (1.2%) in sterile Petri plates. The plates were kept
for 30 min after which wells of 5 mm were made with the use of
sterile tips. To each well, 20 µL of each concentration of extract
(2998.5 mg GAE L
, 599.7 mg GAE L
, 299.85 mg GAE L
199.9 mg GAE L
and 149.92 mg GAE L
) were added. Plates
kanamycin (100 μg ml
- Sigma Aldrich) were used as controls.
verified by the formation of a turbid halo, indicated by bacterial
growth, with no pigment production around the well, on a purple
background on the plate.
Minimum inhibitory concentration (MIC)
The assay was performed as previously described by Wiegand et al.
(2008). A population of 10
colony forming units (CFU) of each
(beef extract 30 g L
, hydrolysate of casein 17.5 g L
1.5 g L
, agar 15 g L
) added of different concentrations of the
phenolic extract of Brazilian cherry. The agar assay was chosen
due to the color of the extracts which would interfere in the
readings in a liquid assay. Plates were inoculated for 24 h, at
optimal temperature of growth of each microorganism and
MIC was determined as the lowest concentration in which no
bacterial growth was observed.
All quorum sensing assays were performed in sub-MIC
concentrations with no measurable interference on the bacterial
growth, as determined by plating appropriate dilutions on LB
agar plates and determining the population of each treatment,
compared to the control in colony forming units per mL
Quantification of violacein production in C. violaceum
The assay was performed as described by Tan et al. (2012),
with modifications. Briefly, C. violaceum was grown overnight at
28 °C and inoculated to a final optical density of 0.1 at 600 nm
) in tubes containing LB or LB
with phenolic extract at different concentrations. Tubes were
incubated at 28 °C for 24 h with agitation at 150 rotations per
min (RPM). The quantification of violacein was performed with
1 mL of culture from each treatment. The aliquot was centrifuged
at 13 RPM for 10 min in order to precipitate the insoluble
violacein piment. Then, the supernatant was discarded and the
pellet solubilized in 1 mL of dimethylsulfoxide (DMSD) with
vigorous agitation, followed by another centrifugation step in
order to remove cellular debris. The absorbance was measured in
control consisted of LB without the addition of the extracts (set to
100% of violacein production), while the positive control for
quorum sensing inhibition consisted of the quorum chenching
at a concentration of 50 µM (Manefield et al., 1999). Colony
forming units per mL (CFU mL
) was also evaluated after the
in order to evaluate any growth inhibition effects.
The percentage inhibition of violacein production was
calculated by using the following Equation 1:
treatment at 585 nm.
Swarming motility assay
The swarming motility assay was performed as described by
Huber et al. (2001) with A. hydrophila and S. marcescens. Briefly
LB agar was prepared to a final concentration of 0.4% of agar
with the addition of the tested extract and plates were kept half
open for 10 min in a laminar flow hood. Aliquots of 2 µL of each
bacterium previously grown overnight were inoculated as a spot
in the center of the medium. The plates were incubated in the
optimal temperature of each bacterium for 24 h after which the
swarming motility was visually observed. The negative control
consisted of LB agar without extract.
2.3 Statistical analysis
Data obtained for the variable (extract concentration) were
compared to the negative control (no extract) in each experiment.
Assays were performed in triplicate and the results expressed as
average of the values of each treatment with standard deviation.
The significance (p < 0.05) was obtained by the ANDVA test and
Tukey test by using the GraphPad Prism version 5.00 software
for Windows (San Diego, California, USA).
The total phenolic content of the extract, as determined by
the Folin-Ciocalteu assay, was 2998.5 mg GAE L
. The phenolic
our assays; therefore, all experiments are expressed as mg GAE L
with the intent of making future comparisons with other food
In this preliminary assay, the E. brasiliensis phenolic extract
presented a potential to inhibit quorum sensing in C. violaceum,
as observed on Figure 1. The result shows a clear, but turbid zone
(indicative of bacterial growth) around the wells (Figure 1c and d),
on a purple background, as opposed to a clear and transparent
halo with the kanamycin control (Figure 1b), indicative of
The MIC values of the phenolic extract from E. brasiliensis
were 499.75 mg GAE L
for A. hydrophila IDC/FDA110-36,
for C. violaceum ATCC6357 and higher than
for S. marcescens, since at this concentration there
was no growth inhibition for this bacterium (higher concentrations
were not tested for this microorganism). The determination of
the MIC was performed in order to provide information on the
concentrations used in the quorum sensing inhibition assays
which were all lower than the MIC values.
3.3 Quantification of violacein production in C. violaceum
The E. brasiliensis phenolic extract, in all the tested
concentrations, presented significant inhibition (p < 0.05)
of violacein production in C. violaceum, as compared to
the control (Figure 2). For instance, in the concentration of
119.94 mg GAE L
the extract was a better inhibitor than the
79% for furanone). In other lower concentrations there was still
significant inhibition of violacein production as compared to
the negative control. The CFU ml
counts after 24 h incubation
from the control (Figure 2).
) – Control for bacterial
and (d) at 599.70 mg GAE L
3.4 Swarming motility assay
The phenolic extract from E. brasiliensis had a considerable
inhibitory effect against swarming motility of S. marcescens while
presenting a marginal effect against A. hydrophila (Figure 3).
The phenolic extract from E. brasiliensis presented a potential
for inhibiting quorum sensing in C. violaceum (Figure 1). In the
plate diffusion assay, the inhibition in this bacterium can be
seen as a lack of purple pigmentation around the well, with
no detectable alteration on the bacterial growth, as previously
observed (Adonizio et al., 2008; Alvarez et al., 2014). However,
this assay can only be considered as a preliminary result, since
growth inhibition effects exemplified by the colorless transparent
halo formed with kanamycin (Figure 1b) are difficult to be
discerned from quorum sensing inhibition which form a turbid
colorless halo (Figure 1c and 1c).
Therefore, the extract was further tested in a quantitative
and confirmatory assay where it was able to inhibit violacein
production up to 90%, as compared with the control (Figure 2).
A similar effect was observed by Vattem et al. (2007) where
violacein production was inhibited from 20 to 60% by aqueous
extracts obtained from raspberry, wild blueberry and grape.
The inhibition found in our study was considerably higher
than that found by Vattem et al. (2007) probably because we
have used extracts enriched for phenolic compounds due to our
extraction method, which may contain more effective purified
phenolic compounds as opposed to aqueous extracts from
those authors. In fact, an extract from fruits of Rubus roaefolius,
prepared in similar conditions to the present study, inhibited
violacein production with values that approach those observed
in this work (Dliveira et al., 2016).
Some studies have shown anti quorum sensing activity of
phenolic compounds. For instance, an extract from Kigelia Africana
fruits, from the family Bignoniaceae, known for its therapeutic
activity due to the presence of phenolic compounds, presented a
great potential at inhibiting the production of violacein (Chenia,
2013). Borges et al. (2014) evaluated the quorum quenching
activity of isolated phenolic compounds in the concentration
of 1000 μg mL
and found that gallic acid reduced violacein
phloridzin to 48%, epicatechin to 33% and oleuropein glucoside
to 51%. Another study by Huber et al. (2003) showed anti
quorum sensing effects of isolated phenolic compounds such
as epigallocatechin gallate (EGCG), gallic acid and tannic acid
on the bioluminescence of the quorum sensing biosensor E. coli
MT102 pSB403 and the fluorescence of Pseudomonas putida
pKR-C12, as well as biofilm formation and swarming motility
in Burkholderia cepacia. In another study, the production of
violacein was completely abolished by leaves of Centella asiatica
L. and Adenanthera pavonina L, and the role of flavonoids on
this action was suggested (Vasavi et al., 2013).
The composition of phenolic compounds from in E. brasiliensis
fruits have been previously characterized as anthocyanins, cyanidin,
quercetins, sinapic acids, gallic acid, catechin, epicatechin,
flavonoids, ellagic acid, myricetin and rutin (Silva et al., 2014).
We hyphotesize that the anti-quorum sensing activity observed in
this work is related to the presence of these phenolic compounds
acting together against the phenotypes that have been evaluated.
Further studies are needed in order to show if the observed effects
IDC/FDA110-36; (c) and (d) tests with S. marcescens. (a) Control: A. hydrophila IDC/FDA110-36; (b) phenolic extract at 119.94 mg GAE L
(c) Control: S. marcescens; (d) phenolic extract at 119.94 mg GAE L
. The experiment was performed twice.
concentrations of phenolic extracts from E. brasiliensis and evaluation
of microbial growth (Log CFU ml
) after 24 h incubation at 30 ºC.
water (no inhibition control) and 39.4 µM of furanone (quorum sensing
inhibition control). Means followed by the same letter do not differ
statistically (p < 0.05).
are related to the synergistic effect of the phenolic compounds
In addition to the above mentioned studies, medicinal plants
have also been searched for quorum sensing inhibition against
violacein production for extracts of Syzygiumcumini L. and Pimenta
dioica L (Vasavi et al., 2013) and bioluminescence inhibition
in V. harveyi for extracts from Rhizophora annamalayanacasca
(Musthafa et al., 2013). Seeds from Cuminum cyminum, popularly
known as cumin, presented as potent inhibitors of quorum
sensing in C. violaceum, with inhibition reaching 86% with no
measurable interference on bacterial growth (Packiavathy et al.,
2011). Similar results have been observed for caffeine, with
mechanism of action probably related to the inhibition of AHL
production (Norizan et al., 2013).
Besides the anti-quorum sensing activity verified by vegetable
products, honey and propolis have also been shown to act as
inhibitors. As pointed out in the present study, the presence
of phenolic compounds in propolis has been attributed as the
cause of inhibition (Truchado et al., 2009).
The phenolic extract from E. brasiliensis also showed inhibition
against swarming motility in A. hydrophila and S. marcescens
(Figure 3). Castillo et al. (2015) have shown that epigallocatechin
gallate (EGCG), a compound extracted from green tea, inhibited
motility in Campylobacter jejuni. Packiavathy et al. (2011) found
that Cuminum cyminum extracts inhibited motility in Proteus
mirabilis, P. aeruginosa PAD1 and S. marcescens. Alterations
in cellular motility could have profound implications for the
microorganism’s pathogenicity as some virulence genes are
normally co-regulated with motility, according to Mccarter (2006).
Teplitski et al. (2000) suggested that plants could produce
substances that mimic AHL molecules, interfering with its
synthesis or transport and also interacting directly with the
receptor LuxR type proteins. Dther studies corroborate this
assertion (Nazzaro et al., 2013; Tan et al., 2012).
More studies need to be conducted in order to purify and
identify the compounds present in the phenolic extract of
E. brasiliensis that actually present quorum sensing inhibition
activity, as well as to elucidate their mode of action on modeled
studied bacteria. The results presented here have important
implications since quorum sensing is a global phenomenon
employed by bacteria in order to control distinct phenotypes.
This work presents important findings since there is a
scarcity of data showing anti-quorum sensing activity from
fruits, especially from native Brazilian species. There is also
an increase in the alternative potentials of natural products
towards controlling microbial activities. This study showed that
phenolic extract from E. brasiliensis presented anti-quorum
sensing activity which could have important implications for
the food and pharmaceutical industries, inhibiting spoilage and
virulence traits that are commonly regulated by quorum sensing
in foodborne bacteria.
UMP acknowledges a grant support for this project from
CNPq-Brazil (process 486240/2013-4). ACR would like to
thank CAPES-Brazil for providing scholarship. ERS and NTBS
acknowledge scholarships from Universidade Federal de Duro
Preto from the PIP´s program.
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