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Ciência e Tecnologia de Alimentos

ISSN: 

0101-2061



revista@sbcta.org.br

Sociedade Brasileira de Ciência e

Tecnologia de Alimentos

Brasil


Conceição RODRIGUES, Adeline; D’Ávila de OLIVEIRA, Brígida; da SILVA, Elis Regina;

Barbosa SACRAMENTO, Nayara Thais; Corrêa BERTOLDI, Michele; PINTO, Uelinton

Manoel

Anti-quorum sensing activity of phenolic extract from Eugenia brasiliensis (Brazilian



cherry)

Ciência e Tecnologia de Alimentos, vol. 36, núm. 2, abril-junio, 2016, pp. 337-343

Sociedade Brasileira de Ciência e Tecnologia de Alimentos

Campinas, Brasil

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Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016

337


Food Science and Technology

ISSN 0101-2061

DI:

D

http://dx.doi.org/10.1590/1678-457X.0089



1 Introduction

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 & 

Nychas, 2012).

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

1

, Brígida D’Ávila de DLIVEIRA



1

, Elis Regina da SILVA

1

,  


Nayara Thais Barbosa SACRAMENTD

1

, Michele Corrêa BERTDLDI



2

, Uelinton Manoel PINTD

3

*

a



Received 09 Dec., 2015 

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



*Corresponding author: uelintonpinto@usp.br

Abstract

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.



Keywords: quorum sensing; anti-quorum sensing; phenolic extract; Brazilian cherry; Eugenia brasiliensis.

Practical Application: The phenolic extract in this study presents potential applications in the food and pharmaceutical 

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.



Anti-quorum sensing activity of grumixama

Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016

338

antivirulence strategies (Adonizio et al., 2008). The combination 



of these inhibitors with other traditional antimicrobials could 

generate synergistic effects promoting more effective control 

against bacterial infections in plants, animals and humans 

(Givskov, 2012).

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

-1

 for 15 min. The seeds were manually 



removed and the pulp was homogenized and kept frozen at -20 °C  

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

3

 (Waters Corporation, 



Milford, MA) for concentration and purification of phenolic 

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

-1

).



2.2 Anti-quorum sensing assays

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

-1

, 599.7 mg GAE L



-1

, 299.85 mg GAE L

-1



199.9 mg GAE L



-1

 and 149.92 mg GAE L

-1

) were added. Plates 



were incubated at 28 °C for 24 h. Sterile distilled water and 

kanamycin (100 μg ml

-1

 - Sigma Aldrich) were used as controls. 



The quorum sensing inhibitory activity in C. violaceum was 

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

4

 colony forming units (CFU) of each 



microorganism was point inoculated in Mueller-Hinton agar 

(beef extract 30 g L

-1

, hydrolysate of casein 17.5 g L



-1

, starch 

1.5 g L

-1

, agar 15 g L



-1

) 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 

(CFU mL


-1

).

Quantification of violacein production in C. violaceum 



ATCC6357

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 

(approximately 10

8

 CFU mL



-1

) 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 



Rodrigues et al.

Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016

339

order to remove cellular debris. The absorbance was measured in 



a spectrophotomer EPDCH (Bio Pek®) set at 585 nm. The negative 

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 

furanone ((Z-)-4-Bromo-5(bromomethylene-2(5H)-furanone) 

at a concentration of 50 µM (Manefield et al., 1999). Colony 

forming units per mL (CFU mL

-1

) was also evaluated after the 



incubation period of C. violaceum in the treatments and control 

in order to evaluate any growth inhibition effects.

The percentage inhibition of violacein production was 

calculated by using the following Equation 1:

(

)



   

 

 



1 00

a b

inhibitionof violacein production

a



=

×





 (1)


Where “a” is the DD of control at 585 nm e “b” the DD of 

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).



3 Results

The total phenolic content of the extract, as determined by 

the Folin-Ciocalteu assay, was 2998.5 mg GAE L

-1

. The phenolic 



content of the extract was used as a parameter of comparison in 

our assays; therefore, all experiments are expressed as mg GAE L

-1

 

with the intent of making future comparisons with other food 



matrices, also rich in phenolic compounds, more feasible.

3.1 Agar diffusion assay with C. violaceum

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 

growth inhibition.



3.2 Minimum inhibitory concentration (MIC)

The MIC values of the phenolic extract from E. brasiliensis 

were 499.75 mg GAE L

-1

 for A. hydrophila IDC/FDA110-36, 



214.18 mg GAE L

-1

 for C. violaceum ATCC6357 and higher than 



149.93 GAE L

-1

 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 

ATCC6357

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

-1

 the extract was a better inhibitor than the 



positive control used in the assay (90% for the extract against 

79% for furanone). In other lower concentrations there was still 

significant inhibition of violacein production as compared to 

the negative control. The CFU ml

-1

 counts after 24 h incubation 



in the presence of phenolic extracts did not differ statistically 

from the control (Figure 2).



Figure 1. Agar diffusion assay with C. violaceum. (a) Negative control – sterile distilled water, (b) kanamycin (100 μg ml

-1

) – Control for bacterial 



growth inhibition, (c) phenolic extract at 2998.5 mg GAE L

-1

 and (d) at 599.70 mg GAE L



-1

.


Anti-quorum sensing activity of grumixama

Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016

340

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).



4 Discussion

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

-1

 and found that gallic acid reduced violacein 



production up to 59%, ferulic acid to 72%, caffeic acid to 75%, 

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 



Figure 3. Effect of E. brasiliensis phenolic extract against swarming motility of A. hydrophila and S. marcescens. (a) and (b) tests with A. hydrophila 

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

-1



(c) Control: S. marcescens; (d) phenolic extract at 119.94 mg GAE L



-1

. The experiment was performed twice.



Figure 2. Inhibition of violacein production by different sub-MIC 

concentrations of phenolic extracts from E. brasiliensis and evaluation 

of microbial growth (Log CFU ml

-1

) after 24 h incubation at 30 ºC. 



The controls consisted of LB broth added of 200 µl of sterile distilled 

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).



Rodrigues et al.

Food Sci. Technol, Campinas, 36(2): 337-343, Abr.-Jun. 2016

341

are related to the synergistic effect of the phenolic compounds 



or to the action of individual components.

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.



5 Conclusion

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.

Acknowledgements

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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