Ahl 4

Hindawi Publishing Corporation
BioMed Research International

Volume 2014, Article ID 162584, 25 pages
http://dx.doi.org/10.1155/2014/162584
Review Article
N-Acyl Homoserine Lactone-Mediated Quorum
Sensing with Special Reference to Use of Quorum Quenching
Bacteria in Membrane Biofouling Control
Harshad Lade, Diby Paul, and Ji Hyang Kweon

Department of Environmental Engineering, Konkuk University, Seoul 143-701, Republic of Korea
Correspondence should be addressed to Diby Paul; [email protected] and Ji Hyang Kweon; [email protected]
Received 2 June 2014; Revised 4 July 2014; Accepted 6 July 2014; Published 24 July 2014
Academic Editor: Bernd H. Rehm
Copyright © 2014 Harshad Lade et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Membrane biofouling remains a severe problem to be addressed in wastewater treatment systems affecting reactor performance and
economy. The finding that many wastewater bacteria rely on N-acyl homoserine lactone-mediated quorum sensing to synchronize
their activities essential for biofilm formations; the quenching bacterial quorum sensing suggests a promising approach for control
of membrane biofouling. A variety of quorum quenching compounds of both synthetic and natural origin have been identified
and found effective in inhibition of membrane biofouling with much less environmental impact than traditional antimicrobials.
Work over the past few years has demonstrated that enzymatic quorum quenching mechanisms are widely conserved in several
prokaryotic organisms and can be utilized as a potent tool for inhibition of membrane biofouling. Such naturally occurring
bacterial quorum quenching mechanisms also play important roles in microbe-microbe interactions and have been used to develop
sustainable nonantibiotic antifouling strategies. Advances in membrane fabrication and bacteria entrapment techniques have
allowed the implication of such quorum quenching bacteria for better design of membrane bioreactor with improved antibiofouling
efficacies. In view of this, the present paper is designed to review and discuss the recent developments in control of membrane
biofouling with special emphasis on quorum quenching bacteria that are applied in membrane bioreactors.
1. Introduction operational problems like decay in filtrate flux, pressure

drop increase, and, thus, alteration on membranes [4]. The
Advanced wastewater treatment technology membrane biofouling problem progresses throughout the treatment
bioreactor (MBR) combines the use of biological degradation process, so the membranes have to be cleaned and eventually
process by activated sludge with a direct solid-liquid replaced [5]. Thus, biofouling is considered as the most
separation by micro- or ultrafiltration membranes of pore severe problem in wastewater treatment systems resulting in
sizes ranging from 0.05 to 0.4 𝜇m [1]. These membranes greater loss in the economy.
allow the complete retention of bacteria and suspended solids Different physicochemical and biological practices have
within bioreactor and only water with reusable quality gets been tried to overcome the problem of membrane biofouling.
released. As a result, the MBRs are increasingly emerging as These include physical cleaning of membrane surfaces with
an advanced treatment processes in industrial and municipal hot water, fabrication of biofouling resistant membranes, and
wastewaters [2]. Even though MBRs have been implemented incorporation of antibiotics or antimicrobial compounds in
in commercial applications for more than two decades, MBR [1, 6]. Indiscriminate use of antibiotics puts selection
one of the major problems restricting their wide spread pressure on bacteria by interfering with their vital genomic
use is membrane biofouling [3]. Membrane biofouling is functions like protein synthesis, RNA synthesis, and DNA
the accumulation of microorganisms and their metabolites synthesis [7, 8]. These result in the emergence of multidrug
produced such as extracellular polymeric substances (EPS) resistance among pathogenic bacteria and thus are consid-
on membrane surfaces. This results in the unacceptable ered as a serious and growing phenomenon in contemporary
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2 BioMed Research International
medicines used in human healthcare. In this scenario, it is system has been divided into two paradigmatic classes:
necessary to use alternative approach to replace antibiotics for oligopeptide/two component-type quorum sensing circuits
combating membrane biofouling. in Gram-positive bacteria and Lux I/Lux R-type quorum
Studies to mitigate membrane biofouling have suggested sensing system in Gram-negative bacteria [28]. The difference
that biofilm formation is mostly associated with Gram- in regulatory process depends on the chemical structure
negative bacteria and their secreted metabolites [9]. Several of signal molecule and its detection mechanism [29]. In
species of Gram-negative bacteria communicate by synthe- general, Gram-positive bacteria use processed oligopeptides
sizing, secreting, and responding to small diffusible signal and Gram-negative bacteria use AHL as signal molecule to
molecules N-acyl homoserine lactones (AHLs) through a coordinate their behaviors. Furthermore, the molecular bases
mechanism called quorum sensing [10, 11]. The AHLs- of the synthesis and perception of different quorum sensing
mediated cell-to-cell signaling allows these bacteria to coor- signals and details of the signal transduction pathways have
dinate gene expression and regulate different phenotypes revealed their specific behaviors. As AHL-mediated quorum
such as biofilm formation, secretion of EPS, and virulence sensing system of Gram-negative bacteria is known to be
factor [12–14]. Moreover, the AHL-mediated quorum sensing
involved in biofilm formations, we will only briefly address
system is associated with almost all stages of biofilm for-
its mechanisms.
mation such as initial surface attachment, bacterial growth,
maturation, and detachment of aged cells [15, 16].
As quorum sensing plays significant roles in the estab- 2.1. AHL-Mediated Quorum Sensing. Predominant Gram-
lishment of biofilms by Gram-negative bacteria, disruption negative Proteobacteria belonging to 𝛼, 𝛽, and 𝛾 subdivisions
of AHL-based signaling has become the promising strategy utilize AHL-mediated quorum sensing pathways to regu-
to control membrane biofouling [17]. Three targets that late their behaviors [30]. However, Gram-positive bacteria
can intercept AHL-based quorum sensing and modulate its belonging to the Exiguobacterium genera have been recently
controlled behaviors like biofilm formation are known, which identified as AHL producer [31]. AHLs are amphipathic in
include (i) inhibition of AHL synthesis by blocking synthase nature and are soluble in water and freely diffusible through
proteins [18], (ii) interference with signal receptors [19], and cell membranes [32, 33].
(iii) enzymatic degradation or alteration of AHLs molecules The AHL-mediated quorum sensing system requires
[20, 21]. Recently, some natural compounds such as vanillin, three major components to function: (i) the AHL signal
furanones, and curcumin have been found to intercept AHL- molecule, (ii) AHL synthase protein to make the AHL signal,
mediated quorum sensing system and thus inhibit membrane and (iii) a regulatory protein which responds to the surround-
biofouling [22–24]. However, this approach is not feasible ing concentration of AHLs [34]. A schematic representation
to use at commercial levels due to higher cost of natural of the AHL-mediated quorum sensing is shown in Figure 1. In
compounds and the fact that more doses are required to AHL-mediated quorum sensing, a single synthase-regulator
achieve considerable biofouling inhibition. Another promis- complex is responsible for the expression of specific genes.
ing approach is that the enzymatic quorum quenching (in the The signal molecules are produced by an AHL synthase gene
form of a free enzyme or an immobilized form on a bead) has Lux I at low concentration and are distributed in and around
been successfully applied to mitigate biofouling in submerged the cell. At lower cell densities, the Lux I is constitutively
membrane bioreactor treating wastewaters [25, 26]. But the expressed at a low, basal level and thus AHLs get accumulated
higher cost of purified enzymes makes it difficult to use at in the surrounding [35]. At high concentration of AHLs, the
commercial levels. signal-receptor protein complex forms and gets activated.
In view of this, a novel biological paradigm with the The activated signal-receptor complex in turn forms dimers
application of quorum quenching bacteria in MBRs has been or multimers with other activated AHL-lux R complexes
investigated recently. This has proven more effective and and functions as transcriptional regulators controlling the
economically feasible with membrane encapsulated and bead expression of quorum sensing regulated target genes. At
entrapped quorum quenching bacterial studies and suggested a certain cell density, also known as “quorum size,” the
a new milestone towards widespread antibiofouling appli- transcription of quorum sensing genes gets triggered and
cations. Thus, in this review, we briefly overview the AHL- results in the expression of various phenotypes [36, 37]. Each
mediated biofilm formations by Gram-negative bacteria and individual quorum sensing regulated gene has its own specific
quorum size to activate and there is no single population
elucidate the roles of enzymatic interference of AHLs by quo-
density at which all the genes are activated [38, 39].
rum quenching bacteria in inhibiting membrane biofouling.
AHL-mediated quorum sensing is the most widely stud-
ied and best understood model of cell-to-cell communication
2. Quorum Sensing for Coordinated in Gram-negative bacteria regulating various phenotypes. In
Behaviors in Bacteria Pseudomonas aeruginosa PAO1, swarming motility, expres-
sion of virulence factors, and biofilm maturation are regu-
Many Gram-positive and Gram-negative bacteria use quo- lated by AHL-mediated quorum sensing system [40]. The
rum sensing signal circuits to coordinate a diverse array AHL-based quorum sensing in Serratia liquefaciens regulates
of physiological behaviors such as symbiosis, competence, swarming motility which results in the maturation of het-
virulence, conjugation, antibiotic production, sporulation, erogeneous biofilms [41]. Burkholderia cepacia, a common
motility, and biofilm formation [27]. The quorum sensing bacteria found in the membrane systems, has been shown
BioMed Research International 3
QS regulated genes
Lux R Lux I
R I
Target genes
AHL/Lux R complex AHL
Expression of phenotypes
Biofilm formation Surface motility

Virulence factor Antibiotic production
Threshold AHLs conc.
Figure 1: Schematic representation of the LuxR/AHL type quorum sensing system in Gram-negative bacteria. The “r” is a gene encoding Lux
R-type transcription factor R and “i” is gene encoding Lux I-type AHL synthase I. Transcription of QS-regulated target genes appears by Lux
R homologue proteins only when high AHL concentration is present, which required a threshold bacterial cell density.
to use cepI/R quorum sensing to control biofilm maturation production, swarming motility, antibiotic production, pig-
[42]. In a natural inhabitant of waters, Vibrio cholerae, mentation, and biofilm formation. The detailed structural
the transcriptional regulator hapRAHL, has been shown information of AHLs identified in Gram-negative bacteria
to be responsible for EPS synthesis and biofilm formation and various phenotypes controlled is given in Table 1.
[43]. Moreover, some other Gram-negative bacteria, v.z.
Aeromonas hydrophila, P. aeruginosa, and so forth, have been 2.3. AHLs-Mediated Biofilm Formations in Wastewaters. Bac-
shown to use AHL-based quorum sensing system to regulate terial biofilms are present in many water and wastewater
numerous phenotypes including biofilm formation [22, 44]. treatment systems, where they may play beneficial or detri-
mental roles [34]. Bacteria prefer to live in biofilms, as
2.2. AHLs Production and Phenotypes Controlled. The AHLs the mode of bacterial life in the form of biofilms confers
which have been characterized so far consist of homoserine many advantages over a planktonic mode of life, such as
lactone (HSL) ring unsubstituted in the 𝛽- and 𝛾-positions resistance to environmental stresses [156]. The formation of
which is N-acylated with a fatty acyl group at the 𝛼-position biofilms is a stepwise process involving the initial attachment
[154]. The naturally occurring AHLs produced by Gram- of bacteria to surfaces, microcolonies growth and matura-
negative bacteria exhibit varying lengths of acyl chain with tion into expanding structures, and further detachment of
4 to 18 carbon atoms and contain either N-acyl, N-(3- aged microorganisms [16]. In general, the transition from
oxoacyl), or N-(3-hydroxyacyl) classes [10, 73]. Some AHLs free-living individual cell to a sessile form initiated with
with unsaturation in the 5 and 7 positions in a chain of 12 the transportation and attachment of bacteria to specific
or 14 carbon atoms have been also reported. The screening substratum followed by adhesion, colonization, and setup
for putative AHL producers has revealed that Gram-negative of early biofilm structures [157]. It has been proposed that
bacteria belonging to different genera which occupy a wide AHL-mediated quorum sensing system of Gram-negative
variety of environmental sources produce AHLs. Some exam- bacteria is involved in almost all stages of biofilm formation
ples of AHLs producing bacteria include species of Acine- such as swarming motility and dispersal of aggregates in S.
tobacter, Aeromonas, Agrobacterium, Burkholderia, Erwinia, liquefaciens and biofilm maturation in P. aeruginosa [15, 158,
Enterobacter, Chromobacterium, Methylobacter, Paracoccus, 159]. The influence of quorum sensing signal molecule 3-oxo-
Pseudomonas, Ralstonia, Rhodobacter, Rhizobium, Serratia, C12-HSL synthesis on biofilm maturation in P. aeruginosa has
Sinorhizobium, Vibrio, and Yersinia [155]. Multiple AHLs been described by Davies et al. [9]. It is also reported that
have also been reported in these bacteria due to the presence quorum sensing regulated cell surface properties alteration
of more than one AHL synthase. In addition, AHL signal seems to translate to a biofilm phenotype variation [15, 160].
production is a consequence of sloppy active site selection The specific role of individual HSL in biofilm formation
for the acyl chain and hence a single synthase will often has been also reported, where C4-HSL was found to be
make multiple AHL types. Thus, the presence of single or involved in the initial surface attachment and maturation of
multiple AHL synthase in a single bacterium has resulted in A. hydrophila biofilms [161].
the regulation of various quorum sensing phenotypes in one Several biofilm forming bacterial species have been iden-
organism which includes virulence factor, exopolysaccharide tified in wastewater treatment systems and are known to
4
Table 1: Structures of common N-acyl homoserine lactones produced by different Gram-negative bacteria and the phenotype controlled.
Synonyms Chemical name Chemical structure, formula name, molecular formula, and formula weight Producing organisms Phenotypes controlled Reference
O H
Biofilm formation,
N
N-Butanoyl-L- O exoproteases, virulence
A. hydrophila, A. salmonicida, P. [41, 45, 46,
C4 -HSL homoserine factor, swimming
aeruginosa, S. liquefaciens MG1 46]
lactone O motility, and biofilm
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-butanamid) formation
MF: C8 H13 NO3 ; MW: 171.19
O H
Bioluminescence,
N-(3- N
3- O polyhydroxybutyrate
Hydroxybutyryl)-L- V. harveyi, Xenorhabdus
hydroxy- metabolism, virulence [47–49]
homoserine nematophilus
C4 -HSL O OH factor, and extracellular
lactone
3-Hydroxy-N-(2-oxo-tetrahydro-furan-3-yl)-butyramide lipase
MF: C8 H13 NO4 ; MW: 187.19
O H
N-(3-Hydroxy-7-cis- N
7Δ-3- O
tetradecenoyl)-L- Rhodobacter leguminosarum, Root nodulation,
hydroxy- [50–52]
homoserine Rhodococcus sphaeroides plasmid transfer
C4 -HSL O OH
lactone
3-Hydroxy-tetradec-7-enoic acid (2-oxo-tetrahydro-furan-3-yl)-amide
MF: C18 H13 NO4 ; MW: 325.44
O H Exoenzyme, cyanide,
pigment, virulence
N Chromobacterium violaceum, factor, biofilm
N-Hexanoyl-L- O Edwardsiella tarda, Bur. cepacia, formation, pigment
C6 -HSL homoserine [41, 53–59]
S. marcescens SS-1, S. liquefaciens prodigiosin, swimming
lactone O
MG1, and P. chlororaphis motility, biofilm
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-hexanamide) formation, and
MF: C10 H17 NO3 ; MW: 199.25 phenazine synthesis
Table 1: Continued.
O H
Bioluminescence,
N-(3-Oxo- N virulence factor,
O V. fischeri, Enterobacter
3-oxo-C6 - hexanoyl)-L- swarming motility,
agglomerans, Erwinia carotovora, [60–63]
HSL homoserine exoenzymes, antibiotic
O O and Pectobacterium chrysanthemi
lactone carbapenem, and

(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-hexanamide) pectinases
MF: C10 H15 NO4 ; MW: 213.20
O H
N-(3- N
3- O Regulate the
Hydroxyhexanoyl)-
hydroxy- V. anguillarum production of C10 -HSL [64]
L-homoserine
C6 -HSL O OH via vanRI
lactone
3-Hydroxy-hexanoic acid (2-oxo-tetrahydro-furan-3-yl)-amide
MF: C10 H17 NO4 ; MW: 215.25
O H
N
N-Heptanoyl-L- O Virulence factor,
C7 -HSL homoserine Ed. tarda, S. marcescens SS-1 [54, 57]
pigment prodigiosin
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-hexanamide)
MF: C11 H19 NO3 ; MW: 213.30
O H
Siderophore
N production, virulence
N-Octanoyl-L- O factor, biofilm
C8 -HSL homoserine Bur. cepacia, Rho. rubrum [55, 56, 65]
formation,
lactone O
photosynthetic
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-octanamide) membrane production
MF: C12 H21 NO3 ; MW: 227.30
O H
Photosynthetic
N-(3-Oxo- N Rho. rubrum, Agrobacterium
O membrane production,
3-oxo-C8 - octanoyl)-L- tumefaciens, Rhizobium sp.strain
conjugal transfer of [65–69]
HSL homoserine NGR234, Rhizobium
O O pTi, and root
lactone leguminosarum bv. viciae
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-octanamide) nodulation/symbiosis
MF: C12 H19 NO4 ; MW: 241.30
5
6
Table 1: Continued.
O H
N
N-Nonanoyl-L- O Virulence factor,
C9 -HSL homoserine Er. carotovora strain SCC 3193 [70]
O swarming motility
lactone
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-nonanamide)
MF: C13 H23 NO3 ; MW: 241.30
O H
N Photosynthetic
N-Decanoyl-L- O Rho. rubrum, Er. carotovora
membrane production,
C10 -HSL homoserine strain SCC 3193, and Bur. [65, 70, 71]
virulence factor, and
lactone O vietnamiensis
exoproteases
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-decanamid)
MF: C14 H25 NO3 ; MW: 255.35
O H
N-(3-Oxo- N
3-oxo-C10 - decanoyl)-L- O Virulence factor,
P. aeruginosa, P. putida [46, 72]
HSL homoserine biofilm formation
O O
lactone
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-decanamid)
MF: C14 H23 NO4 ; MW: 269.34
O H
N-Undecanoyl-L- N
O
C11 -HSL homoserine P. aeruginosa strain PAO1 Virulence factor [73]
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-undecanamide)
MF: C15 H27 NO3 ; MW: 269.40
O H
Virulence factor,
N-Dodecanoyl-L- N Klebsiella pneumonia, P. exopolysaccharide
O
C12 -HSL homoserine aeruginosa, and Sinorhizobium production, and [46, 74, 75]
lactone O meliloti Rm1021 symbiotic nodulation
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-dodecanamide) development
MF: C16 H29 NO3 ; MW: 283.41
Table 1: Continued.
O H
N-(3-Oxo- N Biofilm formation,
3-oxo-C12 - dodecanoyl)-L- O P. aeruginosa, P. putida, and virulence factor, and [65, 72, 76–
HSL homoserine Rho. rubrum photosynthetic 78]
O O
lactone membrane production
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-dodecanamide)
MF: C16 H27 NO4 ; MW: 297.39
O H
N-Tridecanoyl-L- N
O
C13 -HSL homoserine Yersinia pseudotuberculosis Virulence factor [79]
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-tridecanamide)
MF: C17 H31 NO3 ; MW: 297.4
O H
N-Tetradecanoyl-L- N
O Y. pseudotuberculosis, Proteus
C14 -HSL homoserine Virulence factor [79, 80]
mirabilis
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-tetradecanamide)
MF: C18 H33 NO3 ; MW: 311.46
O H
N-(3-Oxo- N Root nodulations,
3-oxo-C14 - tetradecanoyl)-L- O Rhi. leguminosarum, P. virulence factor, and
[75, 81]
HSL homoserine aeruginosa, and Si. meliloti symbiotic nodulation
lactone O O development
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-tetradecanamide)
MF: C18 H31 NO4 ; MW: 325.44
O H
N-(3-Oxo-tetradec)- N
3-oxo-C14 : O Root
7 7(Z)-enoyl-L-
1-Δ -cis- Rhi. leguminosarum nodulation/symbiosis, [69, 81–83]
homoserine
(L)-HSL O O growth inhibition
lactone
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-7-tetradecenamide)
MF: C18 H29 NO4 ; MW: 323.40
7
8
Table 1: Continued.
O H
C14 : N-cis-Tetradec-9Z- O N
1-Δ9 -cis- enoyl-L-homoserine Ag. vitis Virulence factor [84]
(L)-HSL lactone O O
(S,Z)-N-(2-Oxotetrahydrofuran-3-yl)tetradec-9-enamide)
MF: C18 H31 NO3 ; MW: 309.40
O H
N-Pentadecanoyl-L- N
C15 -HSL homoserine O Y. pseudotuberculosis Virulence factor [79]
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-pentadecanamide)
MF: C19 H35 NO3 ; MW: 325.50
O H
N-Hexadecanoyl-L- N
O Polyhydroxyalkanoates
C16 -HSL homoserine Rh. capsulatus [85]
synthesis
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-hexadecanamide)
MF: C20 H37 NO3 ; MW: 339.50
O H
3-oxo-C16 - N-(3-Oxo-hexadec)- N Virulence factor,
: 11(Z)-enoyl-L- O Ag. vitis, Si. meliloti symbiotic nodulation [75, 86]
1-Δ11 -cis- homoserine
O O development
(L)-HSL lactone
(3-Oxo-N-[(3S)-tetrahydro-2-oxo-3-furanyl]-(11Z)-hexadecanamide)
MF: C20 H33 NO4 ; MW: 351.50
O H
N-Octadecanoyl-L- N
O Symbiotic nodulation
C18 -HSL homoserine Si. meliloti [75]
development
lactone O
(N-[(3S)-Tetrahydro-2-oxo-3-furanyl]-octadecanamide)
MF: C22 H41 NO3 ; MW: 367.70
9
MF: C22 H39 NO3 ; MW: 365.60

(N-(Tetrahydro-2-oxo-3-furanyl)-9Z-octadecanamide)
O
lactone (L)-HSL
[87] — Dinoroseobacter shibae enoyl-L-homoserine O 1-Δ9 -cis-
N N-cis-Octadec-9Z- C18 :
H O
Reference Phenotypes controlled Chemical structure, formula name, molecular formula, and formula weight Producing organisms Synonyms Chemical name
Table 1: Continued.
Table 2: AHLs producing bacteria present in wastewater treatment systems and quorum sensing phenotypes regulated.
Phenotypes
Bacterial strains AHLs produced Reference
regulated
A. hydrophila subsp. hydrophila strain NA1, A. hydrophila subsp.
Short- to
dhakensis strain LBA2, A. media strain NA2, En. ludwigii strain Biofilm formation [88]
medium-chain
SWA1, K. variicola strain SWA2, and S. marcescens strain SWA6
Enterobacter sp. strain LBA3, En. cancerogenus strain LBA4,
Raoultella ornithinolytica strain TSA7, P. japonica strain TSA3, Long-chain Biofilm formation [88]
and Citrobacter freundii strain R2A5
A. hydrophila, A. media, A. punctate, A. sobria, A. veronii,
Short- to
A. jandaei, P. oryzihabitans, Ci. farmer, Ci. murliniae, and n.d. [89]
medium-chain
En. ludwigii
A. punctata GC3, Aeromonas sp. GC5, A. hydrophila GC10, A.
allosaccharophila GC15, A. media GC16, Citrobacter sp. GC20,
Acinetobacter johnsonii GC23, Klebsiella sp. GC30, Shigella sp. Short- to
n.d. [90]
GC37, Microbacterium paraoxydans GC42, Chitinimonas medium-chain
taiwanensis GC43, Pantoea agglomerans GC47, Ra. terrigena
GC49,and Microbacterium sp. GC50
A. punctata GC4, Aeromonas sp. GC8, Aeromonadaceae sp.
GC14, Citrobacter sp. GC19, Neisseria sp. GC34, Pseudomonas Long-chain n.d. [90]
sp. GC35, and Malikia spinosa GC45
Ac. junii Medium-chain Biofilm formation [91, 92]
A. hydrophila Short-chain n.d. [93]
P. putida Medium-chain n.d. [93]
Short- and
Ed. tarda Virulence factor [54]
medium-chain
n.d.: not determined; short-chain: C4 -HSL and C6 -HSL; medium-chain: C6 -HSL, 3-oxo-C8 -HSL, and C8 -HSL; long-chain: C8 -HSL, 3-oxo-C8 -HSL, C10 -HSL,
C12 -HSL, 3-oxo-C12 -HSL, and C14 -HSL.
possess AHL-mediated quorum sensing mechanism [162]. have not been specifically studied so far to understand their
Moreover, a number of AHLs producing bacterial strains genetic and physiological attributes. Advanced molecular
have been isolated from wastewaters and found to be involved biology techniques such as pyrosequencing will be used for
in quorum sensing-mediated biofilm formation [88, 163–165]. detailed characterization of unculturable bacteria present in
Different AHLs have also been detected from wastewaters as wastewater treatment systems and further study to under-
produced by Gram-negative Proteobacteria belonging to 𝛼, 𝛽, stand the quorum sensing mechanism involved.
and 𝛾 subdivisions [158]. Furthermore, a correlation between
AHL production and biofilm formation has been found
among wastewater bacterial isolates as accessed by biofilm 3. Quorum Quenching Disrupts Quorum
formation assay [88]. It is suggested that, in Gram-negative Sensing Phenotypes
bacterium S. liquefaciens, the AHL-mediated quorum sensing
regulates swarming motility resulting in formations of het- The mechanism that can interfere with any phenotype reg-
erogeneous biofilms [41]. The detection of C6-HSL and C8- ulated by quorum sensing is known as quorum quenching
HSL in the MBR biocake also indicates the involvement of [166]. There are three basic components and thus targets for
AHLs producing bacteria in biofilm formation [17]. All these external intervention in AHL-mediated quorum sensing sys-
evidences suggest that the AHL-mediated quorum sensing tem have been identified which include Lux I-type synthase
system present in several Gram-negative wastewater bacteria which generates AHL signals, the AHL ligand as signal itself,
is responsible for the formation of biofilms and thus by and the Lux R-type signal receptor [18, 167, 168]. Among
membrane biofouling. all these targets, the enzymatic degradation of AHL signal
The bacterial species identified in wastewater treatment molecules has been reported in a wide range of prokaryotes
systems possessing AHLs-mediated quorum sensing mech- and a few eukaryotes [169]. Thus, one of the most important
anisms are shown in Table 2. This list includes the only prerequisites for designing quorum quenching strategies is
culturable bacteria that were identified in wastewater treat- the screening of Gram-negative bacteria for putative AHLs
ment systems and are involved in AHL-based membrane production. In view of this, the simple AHL biosensors
biofouling. However, the number of biofouling bacteria will bacterial strains based on lux, lacZ, or gfp reporter gene
obviously increase with further investigation of quorum fusion or pigment induction have been developed which can
sensing regulation and interspecies interaction. In addition be used to detect the presence of broad range of AHLs among
to this, most of the wastewater bacteria are unculturable and Gram-negative bacteria [170].
O H
N
O n
O R
Exogenous AHL
H
O
O N
n
O R
(lacZ, violacein, luxCDABE and gfp)

Lux R Lux I
Reporter gene
Transcription
Expression of gene
Agar plate assay: TLC overly assay: Quantitative assay

T-streak (expression levels of):
cross feeding 𝛽-galactosidase activity
replica plating violacein pigmentation
well diffusion bioluminescence
gfp
Figure 2: Construction of bacterial biosensor for the detection of exogenous AHLs. The bacterial biosensor is deficient in AHL production
and when exogenous AHL interacts with LuxR protein, the transcription of reporter genes from LuxR-AHL regulated promoter initiated. This
results in the display of specific phenotypes such as 𝛽-galactosidase activity, violacein pigmentation, bioluminescence, and green fluorescent
protein production.
3.1. Bacterial Biosensors for Detection of AHLs. The detection biosensors were initially developed to detect the presence of
of AHLs producing bacteria can be achieved by several AHLs in environmental isolates, they have also been used to
methods. One common approach involving the use of biosen- investigate the activities of nonnative AHL analogues. The
sors strains is sensitive and convenient and allows real time AHL detection bioassays are most commonly performed by
detection of AHLs [171]. Biosensors strains contain quorum overlay method while quantitative assays are performed by
sensing regulatory promoters fused to lux operon or lacZ liquid cultures. A graphical representation for the construc-
and lack AHL synthase enzyme. Such developed strains tion of bacterial biosensor and its use to detect exogenous
cannot produce AHLs but promoter activity gets induced by AHLs by means of different assay is shown in Figure 2.
exogenous quorum sensing signals. Thus, the receptor gets The most commonly used biosensor strain Ag. tumefa-
activated and binds to its cognate LuxI promoter which ini- ciens NT1 (traR, tra::lacZ749) contains a lacZ fusion in the
tiates the expression of certain genes [45, 98]. The expression tra1 gene of pTiC58 which is induced to produce blue colour
of relevant genes results in the display of specific phenotypes from the hydrolysis of 5-bromo-4-chloro-3-indolyl-𝛽-D-
such as 𝛽-galactosidase production by Ag. tumefaciens NT1 galactopyranoside by the 𝛽-galactosidase activity, in response
[94], violacein pigmentation by C. violaceum CV026 [53], to broad range of AHLs such as 3-oxo-HSLs with side chains
green fluorescent protein production by V. fischeri [105], ranging from C4 to C12, 3-unsubstituted-HSLs with side
and bioluminescence by P. putida 117 [101]. These biosensors chains from C6 to C12, and 3-hydroxy-HSLs with side chains
strains can detect a narrow range of AHLs and thus more from C8 to C10 [94, 172]. Another equally sensitive biosensor
than one kind of such biosensors are required to test the wide strain for long chain AHLs detection is Ag. tumefaciens A136.
range of AHLs produced by a single bacterium. Although It contains the traI-lacZ fusion in the (pCF218) (pCF372)
plasmids and is capable of detecting the presence C8-HSL, 3- showed the inhibition of only short-chain C4-HSL and C6-
oxo-C8-HSL, C10-HSL, C12-HSL, 3-oxo-C12-HSL, and C14- HSL and medium-chain 3-oxo-C8-HSL and C8-HSL AHLs,
HSL exogenous AHLs by 𝛽-galactosidase activity [17, 37, 148]. while it failed to inhibit long-chain AHLs [22]. Moreover,
The second class of reporter strain required for identifying the quantity required to achieve considerable inhibition of
short-chain AHLs with acyl chains of C4 to C6 is represented AHLs is also high; that is, 0.25 mg/mL of vanillin showed
by C. violaceum CV026. It is mini-Tn5 mutant of ATCC31532 the highest QSI activity with C4-HSL (69%) followed by 3-
containing LuxR homologue CviR regulating the production Oxo-C8-HSL (59.8%), C6-HSL (32%), and C8-HSL (28%). In
of violacein, a purple pigment when induced by short-chain addition, only 46.3% of biofilm inhibition was observed at
exogenous AHLs [53, 96]. A more recent developed reporter the tested higher concentration of 0.25 mg/mL vanillin. The
strain for detecting long-chain AHLs ranging from 3-oxo- only major advantage of this novel strategy for antibiofouling
C6-HSL to C14-HSL is C. violaceum VIR24, an in-frame method is that it circumvents the problem of resistance which
deletion mutant of the cvil gene encoding AHL synthase in is linked to the use antibiotics, as it specifically interferes
C. violaceum ATCC12472 [97]. The use of P. putida 117 as with the expression of phenotypes rather than impede growth
bioluminescence sensor for detection of medium-chain C8- [137].
HSL is suggested by Steidle et al. [101]. The green fluorescent Another nonantibiotic approach studied to mitigate bac-
protein derivative GFPmut3∗ and its unstable variant have terial biofilms is the use of enzymes which can inter-
also proven effective biosensors for detecting the presence fere with AHL signals and thereby inhibit its phenotypes.
of AHLs [105]. The GFPmut3∗ emits fluorescent light in the This approach of enzymatic quorum quenching has been
presence of oxygen and does not require any additional sub- attempted by many researchers to control membrane biofoul-
strate. In addition to this, the plasmid sensor pSB1075 based ing in MBRs treating wastewaters. Paul et al. [177] demon-
on Escherichia coli bioluminescence has also been reported strated the potential of purified AHL-degrading enzyme
to detect the presence of C10-HSL, C12-HSL, and their 3- acylase I (porcine kidney) to reduce biofilm formations
oxo derivatives [98]. In addition to the above-mentioned by environmental strains A. hydrophila and P. putida on
biosensors, new biosensors have also been developed so far three different membrane surfaces. To avoid the loss of
and are summarized and listed in Table 3. free enzymes and maintain their stability, various methods
of enzyme carriers have been tried. Recently, Yeon et al.
3.2. Quorum Quenching and Biofilm Control. A large number [17] prepared a magnetic enzyme carrier by immobilizing
of molecules capable of disrupting AHL-mediated quorum quorum quenching enzyme acylase on magnetic particles to
sensing system have been identified and their mechanisms are overcome the limitation of free enzyme and demonstrated
revealed, which includes halogenated furanones produced its potential to control biofouling in MBR. In another study,
by seaweed Delisea pulchra and synthetic derivatives that the immobilization of acylase was carried out onto the
target R proteins [173], synthetic AHL analogues that may membrane surface and mitigation of membrane biofouling
compete with corresponding AHL signals [174], and quorum investigated [26]. These innovative approaches of enzymatic
quenching enzymes such as AHL-acylase, AHL-lactonase, quorum quenching have proven its potential for the control
and oxidoreductases which degrade or modify AHL signals of biofouling in MBR treating wastewaters. However, some
[20, 128, 153]. Such quorum quenching compounds and practical issues related to the high cost of purified enzymes
enzymes with different mechanisms have been widely used and its instability make it difficult to use at commercial
in quenching AHL-mediated quorum sensing and thus pre- level MBRs treating municipal and industrial wastewaters. As
venting bacterial biofilms. an alternative to enzymatic quenching, the use of bacteria
A detailed summary of the known natural quorum that produce quorum quenching enzymes and also help to
quenching molecules derived from plant, fungi, algae, and decompose wastewater pollutant has been suggested [17, 148,
bacteria is provided in our previous review [175]. These 178].
compounds have been widely investigated in disease to com-
bat AHL-mediated quorum sensing trait biofilm formations. 4. Quorum Quenching Bacteria
However, very little research has been done so far using
natural compounds on the inhibition of biofilm formations The discovery of quorum quenching mechanisms in several
in advanced wastewater treatment systems. Recently, vanillin bacterial species represents a new milestone in quorum
has shown to interfere with A. hydrophila quorum sensing sensing and quorum quenching research. Considering the
and inhibited biofilm formations on five different membrane essential roles of AHL-mediated quorum sensing in biofilm
surfaces in a CDC (Center for Disease Control) biofilm reac- formation by Gram-negative bacteria, degradation or dis-
tor study [22]. Two more natural quorum sensing inhibitory ruption of AHLs signals with quorum quenching enzymes
compounds, furanones and Piper betle, have also been found produced by other bacteria appears to be a promising alter-
to inhibit membrane biofouling in wastewater treatment ative for controlling membrane biofouling [179]. Therefore,
systems [23, 176]. However, such purified natural compounds strategies of disrupting the AHL-mediated quorum sensing
are not feasible to use at real MBRs due to the higher cost with special emphasis on the control of membrane biofouling
incurred for its extraction and purification, narrow efficacy by quorum quenching bacteria are discussed herein.
towards specific AHLs, and high quantity required to achieve Over the last few years, a range of quorum quenching
considerable biofouling inhibition. For example, vanillin enzymes have been identified in various Gram-negative
Table 3: The biosensors strains developed to detect AHLs produced by Gram-negative bacteria.
Biosensor strain/plasmid Responded AHLs Reporter system Reference

C6 -HSL, C8 -HSL, C10 -HSL, C12 -HSL,
Ag. tumefaciens NT1 (pDCI41E33 C14 -HSL, and AHLs with 3-oxo-, 𝛽-Galactosidase
[94]
containing traG::lacZ fusion) 3-hydroxy-, and activity
3-unsubstituted side chains
Ag. tumefaciens NT1 (pZLR4 C14 -HSL, 3-hydroxy-C6 -HSL, 𝛽-Galactosidase
[95]
containing Tral/R) 3-hydroxy-C8 -HSL, 3-hydroxy-C10 -HSL, activity
and all AHLs with 3-oxo-side chains
C6 -HSL, C8 -HSL, 3-oxo-C8 -HSL,
Ag. tumefaciens A136 (traI-lacZ 𝛽-Galactosidase
C10 -HSL, C12 -HSL, 3-oxo-C12 -HSL, and [37]
fusion (pCF218) (pCF372)) activity
C14 -HSL
C. violaceum CV026 (CviVR Violacein
C4 -HSL, C6 -HSL, and C8 -HSL [53, 96]
receptor) pigmentation
3-Oxo-C6 -HSL, C6 -HSL, C7 -HSL,
C. violaceum VIR24 (CviI Violacein
3-oxo-C8 -HSL, C8 -HSL, C10 -HSL, [97]
receptor) pigmentation
C12 -HSL, and C14 -HSL
E. coli (luxCDABE cassette
activated by Ahyl/R of A. C4 -HSL Bioluminescence [45]
hydrophila)
C6 -HSL
E. coli (pSB401 containing
3-Oxo-C8 -HSL luxCDABE [98]
LuxI/R of V. fischeri)
C8 -HSL
C6 -AHL
E. coli (pHV2001 containing luxCDABE
C8 -3-oxo-HSL [99]
luxI/R)
C8 -HSL
E. coli (pSB1075 containing
3-Oxo-C12 -HSL, C12 -HSL luxCDABE [98]
LusI/R of P. aeruginosa)
E. coli (pHV2001-containing C6 -HSL, 3-oxo-C6 -HSL, 3-oxo-C8 -HSL,
luxCDABE [100]
LuxI/R of V. fischeri) and C8 -HSL
E. coli (pKDT17 containing 3-Oxo-C10 -HSL, C10 -HSL, 𝛽-Galactosidase
[100]
LusI/R of P. aeruginosa) 3-oxo-C12 -HSL, and C12 -HSL activity
P. putida 117 (pAS-C8-CepR
C8 -HSL Bioluminescence [101]
receptor)
P. aeruginosa (M71LZ containing 𝛽-Galactosidase
3-Oxo-C10 -HSL, 3-oxo-C12 -HSL [102]
Lasl/R) activity
P. aeruginosa (pSB406 containing
C12 -HSL, and C14 -HSL with 3-oxo-side luxCDABE [98]
RhlI/R)
chains
P. fluorescens (pSF105 + pSF107 𝛽-Galactosidase
3-Hydroxy-C6 -HSL, 3-hydroxy-C8 -HSL [103]
containing Phzl/R) activity
Si. meliloti Rm41 (sinI::lacZ C14 -HSL, 3-oxo-C14 -HSL, C16 -HSL, and 𝛽-Galactosidase
[104]
pJNSinR) 1-3-oxo-C16 -HSL activity
V. fischeri (pJBA88 and pJBA89
C6 ∼C14 -3-oxo-HSL
encoding luxR and Pluxl fusion gfp [105]
C6 ∼C12 -HSL
of gfpmut3∗ )
and Gram-positive bacteria. These novel enzymes are key provided the valuable information to elucidate its catalytic
molecules for establishing the concept of quorum quench- mechanisms [166]. Additionally, the molecular biology tech-
ing in regulating quorum sensing phenotypes. The AHL- niques have identified the genes responsible for production
degrading or modifying enzymes are often classified into of quorum quenching enzymes and its phenotypes regulated.
three groups: (i) AHL-acylases, (ii) AHL-lactonases, and (iii) The general mechanisms of these enzymes involved in the
oxidoreductases [20, 128, 153]. It has been known so far that degradation or modification of AHL signals are shown in
four potential cleavage sites in the AHLs are likely cut off by Figure 3.
quorum quenching enzymes following a catabolic digestion AHL-acylases are known to irreversibly hydrolyze the
of carbon and nitrogen sources [124]. The crystal structural amide linkage between the acyl chain and homoserine moiety
characterization of quorum quenching enzymes has also of AHL signals resulting in the release of homoserine lactone
NH3 + HO
O n
AHL-acylase
O R
HSL Fatty acid
O H
O H
AHL degradation
HO N
N + H2 O
AHL-lactonase n
O n HO
O R
O R Acyl-HS
AHL
O H
N
O n
Oxidoreductase
O OH
Hydroxy-HS
Figure 3: AHL-degradation or modification mechanism of quorum quenching enzymes: AHL-acylase, AHL-lactonase, and oxidoreductase.
and corresponding fatty acid, which do not exhibit further activity is not affected by differences in the acyl chain length
residual quorum sensing activity [20, 119]. The AHL-acylase and substitutions in the AHLs [126, 181]. Another important
was first reported in V. paradoxus strain VAI-C, which class of AHL-lactonase is represented by the QsdA from Rh.
showed a wide range of degradation capacity against C4- erythropolis strain W2, which has been shown to degrade
HSL, 3-oxo-C6-HSL, C6-HSL, C8-HSL, C10-HSL, and C12- a wide range of AHLs including C6-HSL, C8-HSL, C10-
HSL [119]. Subsequently, several bacterial species have been HSL, C12-HSL, and C14-HSL with 3-oxo-substitutions [146].
reported to produce AHL-acylases such as AiiC in Anabaena The quorum quenching enzyme QsdA has been found to
sp. PCC7120 degrading C4-HSL to C14-HSL with 3-oxo and degrade the AHL-molecule and inhibits virulence factor in
3-hydroxy substitutions [106], QuiP in P. aeruginosa PAO1 Pec. carotovorum strain PCC797. It is also reported that the
degrading C8-HSL, C10-HSL, 3-oxo-C12-HSL, and C12-HSL QsdA lactonases belong to phosphotriesterase family which
[112], AiiD in Ralstonia sp. XJ12B degrading 3-oxo-C8-HSL, harbors lactonase, phosphotriesterase, or amidohydrolase
3-oxo-C10-HSL, and 3-oxo-C12-HSL [20], and AhlM in activities [146]. Several other bacterial species including
Streptomyces sp. M664 degrading C8-HSL, C10-HSL, and 3- Ochrobactrum sp. T63, Ag. tumefaciens c58, P. aeruginosa
oxo-C12-HSL [117]. PAO1, and Bacillus sp. 240B1 have been reported to encode
Another class of quorum quenching enzyme found in AHL-acylase for degradation of AHLs which results in the
bacteria which degrades AHL molecule is AHL-lactonases inhibition of biofilm formation as listed in Table 4.
[128]. This cleaves the homoserine lactone ring of AHLs in Oxidoreductase is the third important class of quorum
a hydrolytic and reversible manner to open the lactone ring, quenching enzymes found in limited number of bacterial
which makes the AHL incapable of binding to the target species. The oxidoreductases are known to target the acyl side
transcriptional regulator and attenuates its effectiveness [128]. chain by oxidative or reductive manner and thus catalyze the
The hydrolysis of lactone ring also appears at alkaline pH structural modification of AHL signal without degradation
and can be reversed by acidification. Several AHL-lactonases [182]. This structural change in AHL signal thus affects its
have been identified from a range of bacterial species and specificity and recognition which results in the disturbance
are mentioned in some previous reviews [175, 180]. The first of the activation of quorum sensing-mediated phenotypes
AHL-lactonase, encoded by aiiA gene of Bacillus sp. 240B1, by modified AHL [114]. The bacterial oxidoreductases are
was identified as AiiA240B1 by functional cloning of AHL suggested to oxidize a range of long-chain AHLs with or
signal as substrate in E. coli [128]. The AiiA240B1 has been without 3-oxo-substitutions [115, 153]. The first bacterial
shown to degrade C8-HSL and decreases the extracellular oxidoreductase P450BM3 has been isolated from Bacillus
pectolytic enzyme activities and inhibition of virulence in Er. megaterium which showed the oxidation of C12-HSL, 3-oxo-
carotovora. It is reported that AiiA like lactonases hydrolytic C12-HSL, C14-HSL, 3-oxo-C14-HSL, C16-HSL, C18-HSL,
Table 4: List of quorum quenching bacteria reported to degrade or modify AHLs.
Gene
Quenching bacteria AHLs degraded Phenotypes regulated Reference
involved
AHL-acylase mediated QQ
C4 -HSL, 3-oxo-C4 -HSL,
3-hydoxo-C4 -HSL, 3-oxo-C6 -HSL,
3-hydoxo-C6 -HSL, C6 -HSL,
3-oxo-C8 -HSL, 3-hydoxo-C8 -HSL,
Anabaena sp. PCC7120 aiiC C8 -HSL, 3-oxo-C10 -HSL, n.d. [106]
3-hydoxo-C10 -HSL, C10 -HSL,
3-oxo-C12 -HSL, 3-hydoxo-C12 -HSL,
C12 -HSL, 3-oxo-C14 -HSL,
3-hydoxo-C14 -HSL, and C14 -HSL
Acinetobacter sp. strain
Unknown C10 -HSL n.d. [89]
Ooi24
Inhibit biofilm formation in P.
B. pumilus S8-07 Unknown 3-Oxo-C12 -HSL [107]
aeruginosa PA01
C4 -HSL, 3-oxo-C6 -HSL, C6 -HSL,
Decreases virulence and
3-oxo-C8 -HSL, C8 -HSL, 3-oxo-C10 -HSL,
Comamonas strain D1 Unknown antibiotic production in Pec. [108]
carotovorum strain Pcc797
3-oxo-C14 -HSL, C14 -HSL, and C16 -HSL
Inhibits biofilm formation in
P. aeruginosa quiP C6 -HSL, C8 -HSL, C10 -HSL, and C12 -HSL [109]
Aeromonassp.
Reduce virulence factor elastase
P. aeruginosa PA01 PA2385 3-Oxo-C12 -HSL and pyocyanin in P. aeruginosa [73]
PA01
P. syringae strain B728a hacA C8 -HSL, C10 -HSL, and C12 -HSL Influence biofilm formation [110]
P. syringae strain B728a hacB Influence biofilm formation [110]
C10 -HSL, 3-oxo-C12 -HSL, and C12 -HSL
C11 -HSL, 3-oxo-C12 -HSL, C12 -HSL, Decreases elastolytic activity and
P. aeruginosa PAO1 PA2385 [73]
3-oxo-C14 -HSL, and C14 -HSL pyocyanin production
Pseudomonas sp. strain C10 -HSL, 3-oxo-C12 -HSL, C12 -HSL, and
pvdQ Inhibit virulence factor [111]
PAI-A C14 -HSL
C8 -HSL, C10 -HSL, 3-oxo-C12 -HSL, and
P. aeruginosa PAO1 quiP Inhibit virulence factor [112]
C12 -HSL
Inhibit biofilm formation in
Pseudomonas sp. 1A1 Unknown 3-oxo-C10 -HSL, C10 -HSL, 3-oxo-C12 -HSL, [113]
MBR
and C12 -HSL
C4 -HSL, 3-oxo-C6 -HSL, C6 -HSL, Reduces pathogenicity of Pec.
Rho. erythropolis strain W2 Unknown C7 -HSL, 3-oxo-C8 -HSL, C8 -HSL, and carotovorum subsp. carotovorum [114, 115]
C10 -HSL in plants
Decreases swarming ability and
3-Oxo-C8 -HSL, 3-oxo-C10 -HSL, and
Ralstonia sp. XJ12B aiiD production of elastase and [20]
3-oxo-C12 -HSL
pyocyanin in P. aeruginosa PA01
Ralstonia solanacearum C7 -HSL, C8 -HSL, 3-oxo-C8 -HSL, and Inhibits violacein and chitinase
aac [116]
GMI1000 C10 -HSL activity in C. violaceum CV026
Decreases virulence factor,
Streptomyces sp. strain
ahlM C8 -HSL, C10 -HSL, and 3-oxo-C12 -HSL elastase, protease, and LasA in P. [117]
M664
aeruginosa
Shewanella sp. strain Reduces biofilm formation in V.
aac C8 -HSL, C10 -HSL, and C12 -HSL [118]
MIB015 anguillarum
Variovorax paradoxus C4 -HSL, 3-oxo-C6 -HSL, C6 -HSL,
Unknown n.d. [119]
strain VAI-C C8 -HSL, C10 -HSL, and C12 -HSL
AHL-lactonase mediated QQ
Inhibit Ti plasmid conjugal
Ag. tumefaciens c58 attM 3-Oxo-C8 -HSL [120]
transfer
Ag. tumefaciens aiiB n.d. [121]
3-oxo-C8 -HSL, C8 -HSL, and C10 -HSL
Table 4: Continued.
Gene
involved
3-Oxo-C6 -HSL, C6 -HSL, C8 -HSL, Reduces virulence of Erwinia
Ag. tumefaciens C58 aiiB [122]
C7 -HSL, 3-oxo-C8 -HSL, and C8 -HSL strain 6276
3-Oxo-C6 -HSL, C6 -HSL,
3-oxo-C8 -HSL, C8 -HSL,
Ag. tumefaciens K84 aiiS n.d. [123, 124]
3-oxo-C10 -HSL, C10 -HSL, 3-oxo-C12 -HSL,
Inhibit production of phenazines
Acinetobacter sp. strain
Unknown C6 -HSL, C8 -HSL in P. chlororaphis O6 and [125]
C1010
virulence in Er. carotovora
3-Hydroxy-C4 -HSL, C5 -HSL,
3-hydroxy-C6 -HSL, C6 -HSL, C7 -HSL,
3-oxo-C8 -HSL, 3-hydroxy-C8 -HSL,
C8 -HSL, C9 -HSL, and 3-oxo-C10 -HSL,
3-hydroxy-C10 -HSL, C10 -HSL, C11 -HSL,
3-oxo-C12 -HSL, 3-hydroxy-C12 -HSL, Attenuates virulence of P.
Acinetobacter sp. GG2 Unknown [109]
C12 -HSL, 3-oxo-C14 -HSL, aeruginosa and Er. carotovora
3-hydroxy-C14 -HSL, C14 -HSL,
Δ9 -3-hydroxy-C14 -HSL,
Δ10 -3-hydroxy-C14 -HSL,
Δ11 -3-hydroxy-C14 -HSL, and
Δ13 -3-hydroxy-C14 -HSL
Decreases virulence of Pec.
Acidobacteria sp. qIcA 3-oxo-C8 -HSL, C8 -HSL, 3-oxo-C10 -HSL, [126]
carotovorum strain 6276
and C10 -HSL
C4 -HSL, 3-oxo-C6 -HSL, C6 -HSL, Decreases virulence of
Arthrobacter sp. IBN110 ahlD [127]
C8 -HSL, 3-oxo-C10 -HSL, and C10 -HSL Er. carotovora N98
Decreases extracellular pectolytic
Bacillus sp. 240B1 aiiA C8 -HSL enzyme activities and inhibits [128, 129]
virulence in Er. carotovora
B. cereus aiiA C6 -HSL, C8 -HSL, and C10 -HSL Decreases virulence factor [130]
B. mycoides aiiA C6 -HSL, C8 -HSL, and C10 -HSL Decreases virulence factor [130]
Bacillus strain COT1 aiiA 3-Oxo-C6 -HSL Decreases virulence factor [130]
Decreases swarming in Bur.
B. anthracis aiiA C6 -HSL, C8 -HSL, and C10 -HSL [131]
thailandensis
Inhibit biofouling on
microfiltration membranes by
Brevundimonas sp. SW1,
B. pumilus SW9 Unknown n.d. [132, 133]
Acidovorax sp. DB3,
Acinetobacter sp. GS1, and
Staphylococcus aureus SA1
B. thuringiensis subspecies Attenuates the pathogenicity of
aiiA 3-Oxo-C6 -HSL [134]
morrisoni Er. carotovora
Decreases virulence of
B. thuringiensis aiiA 3-Oxo-C6 -HSL [135]
Er. carotovora
Decreases production of elastase,
rhamnolipids, and pyocyanin
Bacillus sp. A24 aiiA C4 -HSL, C6 -HSL [136]
and inhibits swarming in
P. aeruginosa PA01
En. asburiae VT65 aiiA C4 -HSL, C6 -HSL n.d. [137]
Geobacillus C4 -HSL, 3-oxo-C6 -HSL, C6 -HSL,
Thermostable antivirulence
kaustophilus strain GKL 3-oxo-C8 -HSL, C8 -HSL, C10 -HSL, and [138]
therapeutic agent
HTA426 3-oxo-C12 -HSL
Decreases virulence of
K. pneumonia ahlK C6 -HSL, 3-oxo-C6 -HSL [127]
Er. carotovora N98
Table 4: Continued.
Gene
involved
C6 -HSL, 3-oxo-C6 -HSL, C10 -HSL, and Interrupts pathogenicity of Pec.
M. testaceum StLB018 Unknown [139]
3-oxo-C10 -HSL carotovorum subsp. carotovorum
Mycobacterium avium
subsp. paratuberculosis MCP n.d. [140]
K-10
My. tuberculosis AhlA, PPH C4 -HSL, 3-oxo-C8 -HSL, and C10 -HSL n.d. [141]
3-Oxo-C6 -HSL, C6 -HSL, Reduces pectinase activity and
M. testaceum StLB037 aiiM 3-oxo-C8 -HSL, C8 -HSL, virulence in Pec. carotovorum [142]
3-oxo-C10 -HSL, and C10 -HSL subsp. carotovorum
Reduce biofilm formation by P.
C4 -HSL, C6 -HSL, 3-oxo-C6 -HSL, fluorescens 2P24 and the
Ochrobactrum sp. T63 aidH [143]
3-oxo-C8 -HSL, and C10 -HSL pathogenicity of Pec.
carotovorum
3-Oxo-C6 -HSL, C6 -HSL, 3-oxo-C8 -HSL, Attenuates the A. hydrophila
Pichia pastoris aiiAB546 [144]
C8 -HSL, C10 -HSL, and C12 -HSL infection in aquaculture
Pseudoalteromonas Attenuates the plant
qsdH 3-oxo-C8 -HSL, C8 -HSL, C10 -HSL, [145]
byunsanensis strain 1A01261 pathogenicity of Er. carotovora
3-Oxo-C6 -HSL, C6 -HSL,
3-oxo-C8 -HSL, C8 -HSL, Decreases virulence of Pec.
Rho. erythropolis W2 qsdA [146]
3-oxo-C10 -HSL, C10 -HSL, 3-oxo-C12 -HSL, carotovorum strain PCC797
C6 -HSL, 3-oxo-C6 -HSL, C10 -HSL, and Reduces pectate lyase activity in
Rhodococcus strain LS31 Unknown [147]
3-oxo-C10 -HSL Er. carotovora
Reduces pectate lyase activity in
Rhodococcus strain PI33 Unknown C6 -HSL, C10 -HSL [147]
Er. carotovora
3-Oxo-C6 -HSL, C6 -HSL, 3-oxo-C8 -HSL,
Inhibit biofilm formation in
Rhodococcus sp. BH4 qsdA C8 -HSL, 3-oxo-C10 -HSL, C10 -HSL, [148, 149]
MBR
3-oxo-C12 -HSL, and C12 -HSL
Attenuates maceration ability of
Rhodococcus sp. A167 Unknown C6 -HSL, 3-oxo-C8 -HSL, and C8 -HSL Pec. carotovorum subsp. [150]
carotovorum
Attenuates maceration of plant
Solibacillus silvestris
ahlS C10 -HSL pathogen Pec. carotovorum [151]
StLB046
subsp. carotovorum
C4 -HSL, C6 -HSL, C8 -HSL, Decreases pathogenicity of V.
Thalassomonas sp. PP2-459 Unknown [152]
3-oxo-C10 -HSL, C10 -HSL, and C12 -HSL anguillarum ATCC 19264
Oxidoreductase mediated QQ
Oxidizes; C12 -HSL, 3-oxo-C12 -HSL,
B. megaterium CYP102A1 P450BM3 C14 -HSL, 3-oxo-C14 -HSL, C16 -HSL, n.d. [153]
C18 -HSL, and C20 -HSL.
Rho. erythropolis W2 Unknown Oxidizes; 3-oxo-C10 , 3-oxo-C12 -HSL n.d. [115]
n.d.: not determined.
and C20-HSL [153]. Another unknown quorum quenching tool in MBRs treating wastewaters. A detailed survey of
enzyme has been reported from Rho. erythropolis W2 which literature on quorum quenching bacteria has been carried
showed the oxidation of 3-oxo-C10 and 3-oxo-C12-HSL [115]. out and some strains with AHLs degradation or modification
Additionally, one more enzyme was found in Rho. erythro- activities are presented in Table 4.
polis W2 which can reduce the 3-oxo substituent of 3-oxo-
C14-HSL to yield the corresponding derivative 3-hydroxy- 4.1. Application of Quorum Quenching Bacteria in MBR.
C14-HSL and results in the inhibition of quorum sensing Enzymatic quorum quenching has proven its potential as
phenotypes. an effective approach for biofouling control in the MBRs
All these enzymatic quorum quenching mechanisms for advanced wastewater treatment [178]. Several groups
present in bacteria could be used as a potent antibiofouling of bacteria known to produce quorum quenching enzymes
have also been reported and could be further elaborated as alginate entrapped with Rhodococcus sp. BH4 have shown
economically feasible antibiofouling tool in MBR. This inter- the mitigation of membrane biofouling as attributed by
species quorum quenching mechanism present in bacterial both physical (friction) and biological (quorum quench-
cells will thus help to resolve the practical issues concerned ing) effects. The quorum quenching activity of CEBs has
with extraction and purification cost of free enzyme as also inhibited generation of EPS in biofilm cells and thus
well as its stability. In view of this, the practical applica- formed loosely bound biofilms. This approach of bacterial
bility of quorum quenching bacteria in the regulation of quorum quenching with CFBs has shown its potential over
biofilm formations in wastewater treatment systems has been microbial vessels and found more economically feasible than
investigated recently. This will provide valuable information pure enzymatic quorum quenching. This new process of
in addressing both the basic and connectional problems biofouling control with CFBs could open new horizons in
associated with membrane biofouling. the field of wastewater treatment technology. However, this
Oh et al. [178] investigated the inhibition of quorum approach needs further investigation using consortium of
sensing in MBR by two quorum quenching bacteria, a quorum quenching bacteria, as real MBR contains diversity of
recombinant E. coli which produces AHL-lactonase and a
microorganisms which may vary AHLs regulating biofouling
real MBR isolate Rhodococcus sp. A quorum quenching
phenotype.
microbial vessel prepared by encapsulating both the bacterial
strains into a microporous membrane (polyethylene hollow
fiber) has successfully inhibited the membrane biofouling 5. Future Perspectives
by interspecies interference in MBR treating wastewater.
The existence of AHL-mediated quorum sensing system in
Moreover, the continuous MBR operation in the presence
Gram-negative bacteria and its potential role in the formation
of inserted microbial vessel has also inhibited biofouling as
determined by substantial delay in the TMP rise-up with- of biofilms has suggested the application of quorum quench-
out any deterioration of wastewater treatment performance. ing as an alternative approach for combating membrane
In another study with Rhodococcus sp. BH4 encapsulated biofouling. Recently, some bacterial species having the ability
microbial vessel, the quorum quenching activity has been to produce AHL-degrading or modifying enzymes have been
found to coincide well with biofouling inhibition in the identified and successfully attempted in MBRs to reduce
continuous MBR [149]. Additionally, the internal submerged biofouling. These evidences strongly indicate that quorum
MBR equipped with quorum quenching microbial vessel quenching bacteria could be used to develop a potent tool
showed much lower biofouling than conventional MBR. The for the control of membrane biofouling. However, the direct
quorum quenching effect of the microbial vessel was found to application of quorum quenching bacteria has not yet been
be more pronounced when positioned nearer to the filtration tried in real MBRs treating municipal or industrial wastew-
membrane and also depends on recirculation rate of mixed aters. Since wastewaters are composed of diverse groups of
liquor between the bioreactor and membrane tank [2]. It is biofilm forming bacteria, there is need to design a consortium
also observed that the microbial vessel has mentioned its quorum quenching bacterial system which can destruct a
quorum quenching activity steadily over 100 days of MBR wide range of AHLs and will help to prevent multispecies
operation due to the continuous regeneration of quenching biofouling in MBR. Additionally, this economically feasible
bacteria inside the vessel. This indicates its future potential approach needs to be explored further in real MBRs under
in designing long-term cost effective antibiofouling strategies natural conditions.
in real MBRs treating wastewaters. Recently, a microbial
vessel encapsulated with indigenous sludge isolate Pseu- 6. Conclusions
domonas sp. 1A1 has been found effective in the inhibition
of AHL-mediated membrane biofouling in a lab-scale MBR As most of the wastewater bacteria responsible for biofilm
[113]. However, various factors such as vessel material, pore formations employ AHL-mediated quorum sensing mech-
structure, inner volume of vessel, and amount of quorum anism to regulate their behaviours, the application of quo-
quenching bacteria have been found to affect the microbial rum quenching strategy suggests an alternative nontoxic
vessel performance and should be taken into account while approach for control of biofouling in MBR. The AHLs-
designing further microbial vessel containing antibiofouling mediated quorum quenching mechanisms exist in several
strategies. The microbial vessels have some limitations which Proteobacteria and could be explored further as a new
need to be resolved before elaborating further for batch version of antagonism for combating biofilms. Recently,
scale MBRs, which include the following: (i) as the quorum the use of microbial vessel and bead entrapped quorum
quenching microbial vessel has been submerged in a fixed quenching bacteria has been found as an effective tool
place in the MBR, it could degrade only soluble AHLs that in controlling AHL-mediated biofouling in MBRs. These
were able to diffuse into the vessel, and (ii) the mass transfer observations will help researchers to design the futuristic
of AHLs from the mixed liquor to the inside of the microbial AHL-mediated biofouling control strategies in real MBRs
vessel is also limited [148]. treating industrial and municipal wastewaters. Since quorum
To overcome the limitations of quorum quenching micro- quenching bacteria showed direct involvement in interfering
bial vessel, Kim et al. [148] demonstrated cell entrapping with quorum sensing behaviours, their further therapeutic
beads (CEBs) as an alternative method of bacterial quorum and bioindustrial applications should be evaluated in the near
quenching. The CEBs prepared by free-moving beads of future.
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Hindawi Publishing Corporation

BioMed Research International

Harshad Lade, Diby Paul, and Ji Hyang Kweon

Academic Editor: Bernd H. Rehm

1. Introduction operational problems like decay in filtrate flux, pressure

Biofilm formation Surface motility

lactone carbapenem, and

MF: C22 H39 NO3 ; MW: 365.60

(lacZ, violacein, luxCDABE and gfp)

Agar plate assay: TLC overly assay: Quantitative assay

Biosensor strain/plasmid Responded AHLs Reporter system Reference

Table 4: List of quorum quenching bacteria reported to degrade or modify AHLs.

Abbreviations [6] A. Ramesh, D. J. Lee, M. L. Wang et al., “Biofouling in mem-

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