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Environmental Sustainability

, Volume 2, Issue 4, pp 455–468 | Cite as

Endophytes as emphatic communication barriers of quorum sensing in Gram-positive and Gram-negative bacteria—a review

  • Ramappa Venkatesh KumarEmail author
  • Raghwendra Pratap Singh
  • Priyamvada Mishra
Review

Abstract

Endophytes are the microorganisms (bacteria or fungi) which live inside the plant without causing any kind of unhealthy symptoms to the host. They are endosymbiont in nature and assist the plant in promoting their growth and development. Similar to bacteria, endophytes also own the quorum sensing (QS) system for communication with each other and use it to organize their gene expression among local populations. Particularly, this paradox is a density-dependent where these microbes use the cascade to control the genes that endorse attack, resistance, and multiplication of their community. With the continuing manifestation of resistance mechanisms against antibiotics shown by pathogens, there is a contemporary requirement for the development of alternative therapeutic approach. An anti-virulence and antimicrobial mechanism by which QS is obstructed, has been providing a way for the modification of pathogenic processes. Recognition and classification of target autoinducers along with their signaling pathway can be helpful for the researchers to combat the harmful and lethal effect of the pathogenic microorganisms with the help of endophytes secreting bio-active substances like malabaricone and rosmarinic acid. Therefore, the current review focuses on QS, quorum quenching and their respective signaling molecules of endophytes which endorse as the medicinal substitute of synthetic pharmaceutical drugs and protection of plants from phytopathogems.

Keywords

Endophytes Quorum sensing Autoinducers Bio-active substances 

Introduction

The world of microorganisms requires communication within their community through gene-expression, which is determined by their population density, allowing the population to compel and co-ordinate with each other. The whole mechanism prone to cross-talk is known as quorum sensing (QS), and relies on the special kind of signaling molecules known as autoinducers. The signaling apparatus helps microbes to examine the differences in the amount of autoinducer to trail modification in their population density and to alter the global patterns of gene expression collectively. The pattern of gene expression comprises in the secretion of virulence factor, biofilm formation, synthesis of exopolysaccharide (EPS), endotoxins, exotoxins and involved in reproductive purposes like spore formation and mating behavior under the influence of high population density (Fig. 1) (Abisado et al. 2018; Bassler and Losick 2006). For this, the respective ligand molecule interacts with some cognate receptor to induce expression of the different target genes for the functioning of the processes as mentioned above. Moreover, the mechanism of QS is utilized by the microbial population, where in Gram-positive and Gram-negative bacteria employ different pathways and lead molecules in the signaling pathway. Here, Gram-positive bacteria preferentially exploit the two-component system using cytoplasmic factors and membrane-bound sensor kinase receptors by using secreted oligopeptide (peptide) as a lead molecule which modulates the gene expression (Hawver et al. 2016; Ng and Bassler 2009). On the other hand, Gram-negative bacteria employ different lead molecules. Here, the most frequently studied autoinducers belongs to three different categories, namely; acylated homoserine lactones (AHLs) or Autoinducer-1 (AI-1), peptide signal, and Autoinducer-2. AHL autoinducers are used by Gram-negative bacteria and peptide signal is used by Gram-positive bacteria population. Moreover, autoinducer-2 (AI-2) is used by both Gram-positive and Gram-negative bacterial population (Swem et al. 2009; Zhang and Li 2016). Further, autoinducers like acyl-homoserine lactones (AHLs) molecules are synthesized from S-adenosylmethionine (SAM), which can easily diffuse through the bacterial membrane for the activation of signaling cascade. Also, the processes of receptor-ligand binding followed by autoinducer are bound to their specific cognate receptors that exist either in inner membrane or cytosol. These circuits have the potential to characteristically modify diversity of genes that are essential for various biological responses by the host, and the expression of the gene has been achieved by the process called autoinduction which works in a feed-forward loop in density-dependent manner (Konai et al. 2018). The network of QS encourages self–nonself recognition, reliability, chronological control, and stretchy input–output dynamics. Most of the population of Gram-negative bacteria rely on AHL-mediated signaling systems for instances, species of α, β, and γ subclasses of Proteobacteria, including endophytic bacteria in the genera Agrobacterium, Aeromonas, Burkholderia, Chromobacterium, Citrobacter, Enterobacter, Erwinia, Hafnia, Nitrosomonas, Obesumbacterium, Pantoea, Pseudomonas, Rahnella, Ralstonia, Rhodobacter, Rhizobium, Serratia, Vibrio, Xenorhabdus and Yersinia (Lade et al. 2014; Papenfort and Vogel 2010). They also act in unison to make the behaviors successful by showing inter-kingdom communication. Besides these, the pathway helps to control the production of virulence factors and biofilms by involving intracellular second-messengers like cyclic adenosine monophosphate (cAMP). Furthermore, many more second-messengers have been identified which are involved in the cross-talk between Gram-negative bacteria; cyclic dimeric guanosine monophosphate (c-di-GMP), helps to switch from motile phase to stationary phase along with the expression of fimbriae in bacteria; cyclic guanosine monophosphate (cGMP) is involved in chemotaxis and UV stress-response (Fahmi et al. 2017; Pesavento and Hengge 2009). Burkholderia cenocepacia showed potential molecules having auto-inducers of diffusible signal factor (DSF)-family known as cis-2-dodecenoic acid (BDSF) performing antagonistic action against c-di-GMP molecule and negatively inhibits the second messenger. The mechanism behind this action is that the BDSF molecules bind to PAS domain (Per/Arnt/Sim)-GGDEF-EAL domain receptor of RpfR protein causes a detrimental decrease in the intracellular concentration of c-di-GMP resulting in improper swarming motility. Moreover, other microorganisms like Vibrio spp., pseudomonads and other Gram-negative pathogens show action against c-di-GMP and cAMP, respectively (Deng et al. 2012).
Fig. 1

Quorum sensing and its application

In the emerging era, antibiotic resistance and phenotypic heterogeneity among bacteria are helpful to strike the pathways that are necessary for the survival of their population in the respective niche. Endophytes operate and perform the network to counter the disease-causing bacteria by targeting on the secretion of virulence factor and biofilm formation. Endophytes secrete secondary metabolites which can target the QS pathways involved in disease causing symptoms of plant pathogens (Singh et al. 2017). Such as, the mechanism of QS regulates the virulence factors of pathogenic Gram-negative bacteria especially for Erwinia caratovora and Agrobacterium tumefaciens in plant-related genera, for Vibrio anguillarum, and Aeromonas salmonicida in aquaculture, and Pseudomonas aeruginosa, B. cepacia and Yersinia pseudotuberculosis in the category of disease-causing agents in humans (Hong et al. 2012). A diverse range of endophytic bacterial relationship including symbiotic, pathogenic or commensialistic with the host employed for the regulation of vast array of gene expression prominently depends on the physiological mechanism of QS, which helps them to produce biologically active metabolites. One of the best method to employ the endophytes performing QS is in using to regulate the lethal mechanism of pathogenesis of eukaryotic hosts (Galperin et al. 2001). The current review targets on endophytic and other bacterial population communication network where the chemistry of signaling molecules, i.e., autoinducers as ligand and their cognate receptors, design principles, the basic mechanisms of action, and species specificity to perform the desired function has been discussed (Table 1). We discuss newly discovered functions that emphasize their significance for symbiotic and cooperative bacterial behaviors, the possibility of heterogeneity in responses along with the highlight in host-bacterial interactions. Further, by knowing the pathway of development of the disease-causing character of particular bacteria by biofilm formation and the secretion of virulence factors the target to restrict their growth, reproduction, and spread by identifying novel antibiotics from endophytic bacterial population is discussed. Therefore, these bioactive compounds stuck the unhealthy QS mechanism of pathogens and function as antibacterial, antifungal, antiviral and anti-cancerous.
Table 1

Autoinducer and synthase of Gram-negative bacteria

Sl. no.

Organism

AHL

LuxI/R homologue (synthase)

Receptor

Function

References

1.

Pseudomonas aeruginosa

N-butanoyl-l-homoserine lactone(C4HSL), N-3 oxododecanoyl homoserine lactone, (3OC12HSL), Pseudomonas Quinolone Signal (PQS)

RhlR, LasR, QscR, PqsR

RhlR

Virulence, biofilm formation, motility, iron acquisition

Papenfort and Bassler (2016)

2.

Erwinia amylovora

N-3oxohexanoyl-l-homoserine lactone (3OC6HSL)

EamI, EamR

EamI, EamR

Virulence

Barnard et al. (2007)

3.

Erwinia carotovora ssp. Carotovora ATCC 39048

3OC6HSL

CarI, CarR (CarI also known as ExpI) (CarR is cryptic) CarI, VirR

CarI, CarR (CarI also known as ExpI) (CarR is cryptic) CarI, VirR

Carbapenem production, Exoenzyme and virulence factor production

Barnard et al. (2007)

4.

Erwinia carotovora ssp SCRI 193

3OC6HSL

ExpI, ExpR, VirR

ExpI, ExpR, VirR

Exoenzyme and virulence factor production

Barnard et al. (2007)

5.

Erwinia carotovora ssp SCC3193

3-oxo-C8-HSL(N-(3-oxooctanoyl)-l-homoserine lactone;), 3-oxo-C6-HSL(N-(3 oxohexanoyl)-l-homoserine lactone), C8-HSL

ExpI, ExpR

ExpI, ExpR

Exoenzyme and virulence factor production

Barnard et al. (2007)

6.

Erwinia carotovora ssp EC153

3-oxo-C8-HSL(N-(3-oxooctanoyl)-l-homoserine lactone;), 3-oxo-C6-HSL(N-(3-oxohexanoyl)-l-homoserine lactone)

AhlI, ExpR

AhlI, ExpR

Exoenzyme production

Barnard et al. (2007)

7.

Erwinia carotovora ssp Ecc 71

3-oxo-C6-HSL(N-(3-oxohexanoyl)-l-homoserine lactone)

ExpI (also known as AhlI, HslI), ExpR

ExpI, ExpR

Exoenzyme and virulence factor production

Barnard et al. (2007)

8.

Erwinia carotovora ssp. atroseptica SCRI1043

3-oxo-C6-HSL(N-(3-oxohexanoyl)-l-homoserine lactone)

ExpI, ExpR, VirR

ExpI, ExpR, VirR

Exoenzyme and virulence factor production

Barnard et al. (2007)

9.

Erwinia chrysanthemi EC 3937

3-Oxo-C6-HSL, C6-HSL, C10-HSL(N-decanoyl-l-homoserine lactone)

ExpI, ExpR

ExpI, ExpR

ExpI, ExpR

Barnard et al. (2007)

10.

Pantoea stewartii DC283

3-oxo-C6-HSL(N-(3-oxohexanoyl)-l-homoserine lactone)

EsaI, EsaR

EsaI, EsaR

Exopolysaccharide and virulence factor production

Barnard et al. (2007)

11.

Serratia sp.

ATCC 39006

C4-HSL ()N-butanoyl-l-homoserine lactone), C6-HSL (N-hexanoyl-l-homoserine lactone)

SmaI, SmaR, CarR, SmaI, SmaR

SmaI, SmaR, CarR, SmaI, SmaR

Carbapenem, prodigiosin and virulence factor production

Barnard et al. (2007)

12.

V. harveyi

C4-HSL ()N-butanoyl-l-homoserine lactone), 3OH-C4-HSL, Isovaleryl-HSL, 3OXO-C12-HSL, p-Coumaroyl-HSL, Cinnamoyl-HSL

Rh1R, LuxN, BjaR, LasR, QscR, RpaR, BraR

LuxI Or RpaI

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

13.

Ralstonia spp.

phcS

3-Hydroxypalmitic acid methylester (3-OH PAME) and (R) methyl 3-Hydroxymyristate ((R) 3-OH MAME)

PhcB

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

14.

Xanthomonas campestris

RpfC

Diffusible signal factor (DSF)

RpfF

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

15.

Vibrio harveyi and Vibrio cholerae

CqsA

Cholera autoinducer-1autoinducer synthase (CqsA)

CqsS receptor

Virulence factors and biofilm formation

Pereira et al. (2009)

16.

Vibrio spp.

LuxP or LuxQ

4,5dihydroxy2,3pentanedione (DPD)

LuxP, CqsS

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

E. coli

LsrB

1. S-THMF-borate

2. R-THMF

LuxS

17.

Pseudomonas aeruginosa

2(2hydroxyphenyl) thiazole4carbaldehyde (IQS) 2heptyl3hydroxy4quinolone (PQS)

AmbBCDE

PqsABCDH

PqsR

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

18.

Photorhabdus asymbiotica

Dialkylresorcinols (DARs)

DarABC

PauR

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

19.

Photorhabdus luminescens

PPYs

PluR transcriptional regulator

PpyS

Virulence factors and biofilm formation

Papenfort and Bassler (2016)

20.

Vibrio harveyi

3OH-C4-HSL (HAI-1), (Z)-3-aminoundec-2-ene-4-one, AI-2

LuxM synthase

LuxP, Lux N, CqsS

Virulence factors and biofilm formation

Pereira et al. (2009)

Signal transducing molecules and their specificity

Signal transduction in an endophytic microorganism and other bacterial population depends on the heterogeneous nature of their population density. They can come across in a multifaceted mixture of autoinducers produced by their clonal siblings, close relatives and non-kin neighbors, which could be ferocious in nature. The biochemical signaling of QS was first analyzed in marine bioluminescent bacterium ‘Vibrio harveyi’ and after the identification, several novel autoinducers has been recognized which expand the knowledge and understanding of QS. Moreover, three autoinducers have been acknowledged that regulate up to 600 different target genes which specifies intra-genera and intra-species level gene expression. Bacterial populations are omnipresent, and due to their diversity, they are facing challenges in the identification of themselves from the consortia of related and unrelated molecules. The communication in between Gram-negative bacteria is performed by one of the most standard class of autoinducer that are AHLs having a core N-acylated homoserine-lactone ring and a 4–18 carbon acyl chain with the modification that can affect the stability and gives an outcome of signaling dynamics (Schuster et al. 2013; Zhang and Li 2016). These autoinducers are synthesized by LuxI-type synthases and lactone derivatives of SAM, and acyl chain, and they are also synthesized from the intermediates of fatty acid biosynthesis. All the bacterial colonies do not obey the entire process. Rather some exceptions were also observed in the plant associated photosynthetic bacterium Rhodopseudomonas palustris, here acyl-group comes from the metabolite named p-coumarate, synthesized in the host itself, and the respective metabolite can synthesizes Lux I-type enzyme like 4-coumaroyl-homoserine lactone synthase (RpaI) which assist to synthesizes p-coumaroyl-homoserine lactone (HSL) (Schaefer et al. 2008). Moreover, several endophytic bacteria like Bradyrhizobium japanicum and Aeromonas spp. synthesize a quite unique type of homoserine lactone i.e., isovaleryl-HSL. On the other hand, cinnamoyl-HSL is produced by Bradyrhizobium BTAi by using bacterial substrates (Ahlgren et al. 2011). Additionally, some other endophytic bacteria, e.g., Xanthomonas campestris and Ralstonia solanacearum produce another class of autoinducers namely, 3-hydroxypalmitic-acid-methyl-ester (3-OH PAME) and (R)-methyl-3-hydroxymyristate ((R)-3-OH MAME), respectively. The respective autoinducers of R. solanacearum were synthesized by PhcB protein which controls the mechanism of biofilm formation and virulence (Flavier et al. 1997; Zapata et al. 2017). Further, bacterial population is using a diverse form of autoinducers for their respective need. Similarly, diffusible signal factor (DSF, cis-11-methyl-2-dodecenoic acid) is used by X. campestris for the transition between its planktonic and biofilm-formation associated lifestyles. A diffusible signal factor is kind of autoinducers which can be synthesized by their host endophytes, and their regulative protein is RpfF protein. Therefore, the large population of DSF can be seen in their particular niche (Deng et al. 2010, 2014). One of the research suggests that member of Gram-negative Proteobacterium namely endophytic RT1 Rhizobium etli, resident of root nodules of lentils and legumes such as Phaseolus vulgaris, produces another kind of AHLs namely, 3-oxo-C8-HSL which is essentially responsible for swarming motility and biofilm formation that enables the bacterial population to attach to solid substratum (Dixit et al. 2017). Moreover, mechanism of swarming can be seen in different genera namely, Azospiriillum, Aeromonas, Burkholderia, Bacillus, Chromobacterium, Clostridium, Escherichia, Proteus, Pseudomonas, Rhizobium, Salmonella, Serratia, Sinorhizobium, Vibrio, and Yersinia. Further, the diversity in the family of AHLs has been recognized with their important functions like motility, biofilm formation, bio-control, the productions of exo-enzymes and antibiotics, synthesis of the plant growth promoting auxin, indole-3-acetic acid (IAA), and the promotion of plant colonization in stress conditions (Butler et al. 2010; Dixit et al. 2017).

Neural network of quorum sensing

Integration of chemical information can be accurately executed for the study of QS behaviors. For this, the bacterial community analyzes the message from the surrounding environment, and the chemical messages can be utilized to regulate the gene expression for the specific response. All the signaling intermediates cumulatively perform these feats by using different types of autoinducers in community-wide level. Moreover, the information can be altered by various internal (such as fluctuations in transcript or protein numbers), and external factors (temperature, pH, osmolarity, and so on), or if the bacteria compete for the same autoinducers (Goryachev 2009). Similarly, it will be important to learn more about the molecular mechanisms that induce the bacteria to stimulate or inhibit QS signaling in neighboring bacteria. Such inter-species communication, and cross-talk is plausible to play pivotal roles in both inter-species competition and mutual symbiotic cooperation between bacterial species in their respective niche and is probably to provide us information with additional molecular tools for manipulating bacteria. In the forthcoming subsection, the molecules of QS in Gram-positive and Gram-negative microorganism along with their signaling mechanisms have been outlined.

Cross talk between Gram-negative bacteria

The species level communication in Gram-negative bacteria, V. harveyi, and Vibrio cholerae provides one of the best examples of a QS cascade which specifically relies on membrane-bound receptors. The importance of autoinducers and QS can be seen in different bacterial populations, like autoinducers are regulating the activation and inhibition of QS cascade, for instances; in the absence of autoinducers LuxR-type transcriptional activator proteins can be degraded and this can prevent premature activation of QS in the species of Pseudomonas whereas, in the Vibrio species, localization of membrane receptors decouples the cytosolic production of autoinducers from being detected in periplasm (Chu et al. 2013). Moreover, different receptors can be binding with different types of autoinducers like cholerae quorum sensing sensor i.e., CAI-1 autoinducer sensor kinase/phosphatase CqsS interacts with CAI-1, LuxN interact with HAI-1specifically in V. harveyi and LuxPQ interact with AI-2 in V. cholera, respectively. However, at the stage of low cell density, level of autoinducers gradually decreases and the LuxN, LuxPQ and CqsS receptors act as kinases by autophosphorylating itself and then transfer phosphate to the shared phosphotransfer protein, LuxU. LuxU transfers the phosphoryl group to the DNA-binding response regulator, LuxO, gathered with σ54 (sigma factor for nitrogen metabolism) to activate the transcription of genes that encode four (V. cholerae) or five (V. harveyi) homologous sRNAs, known as the quorum regulatory sRNAs (Qrr sRNAs), and Qrr1, Qrr2, Qrr3, Qrr4 and Qrr5 (Qrr1–5) are transcribed. The Qrr sRNAs are Hfq-dependent sRNA chaperone that regulates the gene expression by base-pairing with target mRNAs and as a result, altering translation by activation or repression. Here, Qrr sRNAs repress luxR and activate aphA. AphA controls genes that are involved in individual behaviors and activates genes that are required for virulence and the formation of biofilms (in V. cholerae) (Anetzberger et al. 2012; Lilley and Bassler 2000; Lenz et al. 2004). On the other hand, during high cell density condition, autoinducer levels are high and binding of autoinducer inhibits the autophosphorylation which enables the receptor namely, LuxN, LuxPQ and CqsS, function as phosphatases. LuxO is dephosphorylated (inactive) which terminates the expression of Qrr1–5 sRNAs. Therefore, AphA is not produced, whereas LuxR is produced. LuxR control the genes that are required for group behaviors, including genes that are responsible for bioluminescence (in V. harveyi), siderophore production, type III secretion, and metallo-protease production. Under this condition, LuxR or HapR is produced, and it activates the genes that underpins the collective behaviors (Rutherford and Bassler 2012; Swem et al. 2008) (Fig. 2). Additionally, the Qrr small RNAs repress lux MN by catalytic degradation of mRNA. This luxMN encode an autoinducer synthase and receptor pair, consequently represses translation of luxO by seizing luxO mRNA, which reveals the ribosome binding site to activates aphA. Even though catalytic degradation of the luxR or hapR mRNA by the Qrrs RNAs does not change the Qrr pool but coupled degradation and sequestration remove Qrrs RNAs from the system. Therefore, a regulatory mechanism is essential for the upholding of suitable Qrr pools and overall QS dynamics (Ball et al. 2017; Feng et al. 2015). The molecular structural designing is analogous to chemotaxis in Escherichia coli that proposes the universal significance of two states depending upon the free energy models of bacterial sensor kinases. Possibly due to the differences in the free energy state of two configurations, a meticulous receptor is in the kinase or phosphatase state. One of the most important things is, QS can never be fully turned off or on unless all the autoinducers are present or absent, respectively (Feng et al. 2015).
Fig. 2

Quorum sensing circuit in V. harveyi

Cross talk between Gram-positive bacteria

Gram-positive bacteria predominantly use modified oligo-peptide as autoinducers in QS system to regulate the desired gene expression. As they are impermeable to plasma membrane, they require specific transporters to mobilize the peptides. Here, the signaling pathway follows the two-component signaling system which consists of membrane-bound histidine kinase receptor and cytoplasmic response regulators for a series of phosphorylation activities. Membrane-bound histidine kinase receptors bind to peptide and stimulate ATP-driven auto-phosphorylation events on conserved histidine residue. Further, the phosphorylated histidine transfers its phosphate to a conserved aspartate residue of response regulator which convert inactive response regulator to an active state, thus, function as DNA binding transcription factor for manipulating target gene expression (Fig. 3). The whole process is regulated by the phenomenon of QS, which can be used to speed up the conversion from the low cell density to high cell density (Hawver et al. 2016). Some of the examples of QS pathway with their respective Gram-positive microbes include ComD/ComE system of Streptococcus pneumonia that controls competence development, the ComP/ComA system of Bacillus subtilis that controls competence and sporulation, the AgrC/AgrA system of Staphylococcus aureus that controls pathogenesis. Agr autoinducer is denoted as AIP (auto-inducing peptide) and encoded as a precursor peptide by AgrD gene, where the processing of peptide and secretion occurs via AgrB transporter. The autoinducing peptide is analyzed by histidine kinase AgrC receptors and follow the phosphorelay to AgrA response regulators (Banerjee and Ray 2017; Ng and Bassler 2009).
Fig. 3

Quorum sensing in Gram-positive bacteria

Quorum quenching molecules

Quorum quenching (QQ) is an important and critical phenomenon for bacterial pathogenesis. It is considered to be one of the coherent strategies to diminish the virulence of pathogens. Antibiotic resistance is emerging day by day in Gram-negative bacteria. Therefore, there is a need for alternative strategies to stop the bacterial infection and one of the methods is an anti-QS approach (Reen et al. 2018). The obstruction in the cross-talk of the bacterial population via QQ molecules from endophytes is used as natural means for the interruption of several bacterial diseases. In this approach, plant metabolites are playing a predominant role for regulating the development of microbial pathogens, which are used as a cure against several microbial diseases in plants and animals. The host plant and endophytes are competent of maintaining a mutualistic relationship which over and over again leads to co-evolution of some important functional traits like the production of the secondary metabolite, assist in plant defense response either by possessing quorum inhibiting enzymes or producing own quorum signal inhibiting chemicals (Fig. 4). Several reports are suggesting that the AHL-mediated QS inhibitors promote the breakdown of LuxR class of protein in the species of Delisea pulchra (Remy et al. 2018; Vasavi et al. 2013). In addition, AiiA is an AHL-lactonase enzyme considered as QQ molecule, biosynthesized by Bacillus sp., having the capacity to break the bonds of lactone ring of AHL molecules and acts as an inhibitor of AHL molecules. Additionally, the development of genetically engineered plants and animals like C. elegans using AiiA gene is extensively used against the virulence of Erwinia carotovora and P. aeruginosa. A group of researchers explained that many of the antimicrobial compounds which may be broad spectrum antibiotics, have the intrinsic action to inhibit LuxS-directed synthesis of 4,5-dihydroxy 2,3-pentanedione (DPD) or AI-2 in Gram-negative bacteria. Such antagonistic action gives the direction in the regulation of QS mechanism and hence role in a different aspect for controling the development of the bacterial community and pathogenesis and horizontal transfer of drug-resistance markers (Chen et al. 2013; Federle and Bassler 2003). Diverse variety of QQ compounds have now been identified and discussed below.
Fig. 4

Quorum sensing signal response

Wide application of quorum quenchers

Several medicinal plant products have been reported to significantly act like molecules that can assist to target the bacterial QS mechanism for destruction of infective agents of several lethal diseases. The basic mechanism in destruction is performed by three different methods, i.e., hindrance in the signaling molecules AHL synthase encoded by LuxI gene, deterioration of lead signaling molecules and also targeting the core signaling receptor of LuxR. Furthermore, S-adenosyl methionine (SAM) and acyl carrier protein (ACP) work efficiently in the production of AHL where SAM is amino acid donor utilized for formation of ring structure of AHL and ACP acts as a pioneer molecule for the synthesis of N-acyl side chains of respective AHL molecules (Shin et al. 2015). By knowing all the prerequisite information in the production of AHL molecules, a diverse analog of SAM has been produced pharmaceutically which possess anti-QS approach. Moreover, the fundamental mechanism in the hindrance of signaling cascade is the competitive interaction between the anti-QS molecules that can bind to AHL receptor and some molecules which can also impede the QS mechanism by showing non-competitive interaction in the binding site as they can bind to the allosteric site and interfere with the binding of AHL and its cognate receptor, LuxR. Some of the biological metabolites can structurally mimic the AHLs and all such metabolites effectively block the initiation of AHL pathway. In addition to this, QQ molecules assist the biosynthesis of conventional antibiotics which can cause destruction in biofilm formation and also assist the loss of probable resistance mechanism in the bacterial population (LaSarre and Federle 2013).

A wide variety of QQ molecules have been known in nature for instances, halogenated furanones were found to competitively bind to LuxR type proteins cause proteolytic degradation in the membrane of the bacterial population. On another hand, several furanones plays a pivotal role in decreasing of light emission among the Vibrio species, disruption of pigment production in Chromobacterium violaceum and interference in swarming motility in S. liquefaciens (Hong et al. 2012; Koh et al. 2013). Further, furanocoumarins were shown to have potential activity against autoinducer-1 and autoinducer-2 as well as an interruption in the biosynthesis of biofilm in P. aeruginosa, Salmonella typhimurium, and E.coli. Some of the bioactive compound like furocoumarins, carotenoids, limonoids, coumarins and pectate produced by medicinal plants such as extract of grapefruit show the potential antibacterial and anti-fungal properties (Koh et al. 2013).

In addition to this, few more QQ compounds were known with different potential activity, like obacunone acts as an antagonistic inhibitor of AHL and AI-2 and cause hindrance in the activity of biofilm formation and enterohemorrhagic E. coli (EHEC) virulence also (Vadakkan et al. 2018). Another known drug, aspirin is also showing the anti-QS approach. The aspirin aryl group is an aspirin derivative along with Tyr-88 amino acid present in the active center of Las receptor has been indulging in π–π interaction, shows a role in significant inhibition of production of virulence and toxin in P. aeruginosa. Some of the drugs such as metronidazole and tinidazole mimic AHL activities and give response against QS in a dose-dependent manner (Liu et al. 2011). Moreover, Staphylococcus species; S. delphini, S. intermedius, S. lutrae, S. pseudintermedius, and S. schleifer are Gram-positive and coagulase positive and are considered as an inter-medius group of zoonotic family. All these bacterial populations specifically S. delphini represent and synthesize a novel class of QQ compound, namely N-[2-(1H-indole]-urea and N-(2-phenethyl)-urea called as Yayurea A and B, respectively. Both of these compounds are able to quench the signaling pathway in a wide range of Gram-negative bacteria (Chu et al. 2013).

Quorum quenching compound from the plants

The mechanism of QQ is a radiant and booming research issue in the current era which elucidates the method to hinder the cross-talk between bacterial populations, and as a result, it helps in sustainable development of plant kingdom. There are diverse forms of QQ compounds which are adequately present inside the plant kingdom and help to restrain the QS mechanism (Remy et al. 2018). Moreover, some of the studies suggest that diverse class of plant metabolites like Malabaricone C have been reported from medicinal plant named Myristica cinnamomea (nutmeg), and possess anti-QS activity by impeding QS compound (Sivasothy et al. 2016). Other than this, compound Malabaricone C also inhibits the prominent system of P. aeruginosa PA01, namely RhlR and LasR systems and CviR in C. violaceum facilitate to hinder the pathway of QS. Moreover, propali (blue glue) herbal exudates of the medicinal plant is able to inhibit the production of violacein in C.violaceum and the same propalis extract has the potential activity to hinder the virulence factors like LasA and LasB proteases in P. aeruginosa. Some of the vegetables are also known for the rich concentration of metabolite having the possible activity of inhibiting the QS pathway; carrot (Daucus carota), chamomile (Matricaria chamomilla) and water lily (Nymphaeaceae) work antagonistically towards LuxI-GFP reporter strain. Some of the reports suggesting that both disulfide and trisulfide are the metabolite secreted from garlic plant (Allium sativum) show prominent activity to inhibit QS receptor such as, metabolite from A. sativum targets the receptors of LuxR gene and inhibits the pathway in P. aeruginosa. Another medicinal plant, namely, sweet basil (Ocimum basilicum) secrets a bioactive metabolite named rosmarinic acid showing a potential activity to reduce the expression of enzymes elastase and protease. It also renders the capacity to inhibit the formation of biofilm in P. aeruginosa. Root exudates from seedlings of pea plants (Pisum sativum) were found to be responsible for hindering the production of protease activity, exochitinase activity, and pigment of C.violaceum. Further, Glycine max, Oryza sativa, Lycopersicon esculentum, and Medicago truncatula also consist of several substances which can imitate the function of AHL (Koh et al. 2013).

Some of the research studies suggests that Phialocephala fortinii and Meliniomyces variabili were the symbiotic fungi associated with their respective plant, show the ability to mortify the activity of AHL which helps to diminish the microbial virulence (Koh et al. 2013). Some of the metabolic enzymes isolated from the plant namely, lactonase and acylases show potential activity to interfere with the QS via disrupting AHL signaling compounds, and assist in regulating the trait of virulence and used as bio-control agents.

Study shows multiple regulatory circuits of AHL in Gram-negative bacteria, including degradation of AiiA (autoinducer inactivator) dependent signal transduction pathway (Chu et al. 2013). Recent research on endophytes suggests that they are having a diverse range of QQ compounds which can target the pathogenicity and virulence factors of microorganisms. AHL autoinducers were extensively found in diverse forms of microbial pathogens with little modification in common homoserine lactone moiety i.e., alteration in the length of the acyl chain and they are involved in virulent gene expression. AHL lactonase has the potential activity to hydrolyze the lactone bond and modify itself against binding to target transcriptional regulators, which enhances the resistance mechanism against pathogenicity (Mookherjee et al. 2017).

One of the studies suggests that AHL lactonase used for the impedance of virulence in phytopathogens namely E. carotovora, by the induction expression of AiiA gene and the respective gene mediates the targeting of pathogenic signal reported in various microorganisms of rhizosphere, soil and also in Bacillus species especially B. thuringiensis (Chen et al. 2013). Similarly, AHL lactonase recently reported in endophytic Enterobacter species, is isolated from one of the woody climber, red creeper i.e., Ventilago madraspatana. Moreover, the presence of AHL lactonase in the different endophytic species namely Enterobacter asburiae VT65, Enterobacter aerogenes VT66, and Enterobacter ludwigii VT70 via amplification of AiiA homolog gene, exemplifies the putative tertiary structure of endophytic AHL lactonase (Dong et al. 2018). Additionally, some of the endophytic bacterial colonizers also carry homologs of AiiA gene in plants like red sandalwood (Pterocarpus santalinus L.) and contain a conserved zinc-finger binding motif that is effective against C4-HSL and 3-oxo-C12-HSL. Further, it is reported that utilization of cell-free lysates of endophytic bacterial isolates inhibits the biofilm formation in pseudomonads, especially P. aeruginosa PAO1 (known human pathogen) (Rajesh and Ravishankar 2014). All such reports suggest that the utilization of endophytes and genetically transformed endophytes can provide the emerging area for the impedance of virulence factors of specialized or generalized phytopathogens. This will aid the enhancement of the immune system via building up of host defense mechanism in particular niches. Other than the use of lactonase, endophytic actinomycetes Streptomyces LPC029 produces AHL acylase, which assists the suppression of disease of soft rot of potato by Pectobacterium carotovorum sp., carotovorum. Moreover, bacterial endophytes can be genetically engineered and used against phytopathogens rendering towards large scale application of endophytes as bio-control agents in agriculture (Ha et al. 2018). The present scenario focuses on the multidrug resistance which is a huge problem globally and the introduction of anti-virulence strategy against drug resistance mechanisms both clinically and ecologically. Additionally, application of QQ compounds in the pharmaceutical and clinical sector for the isolation and identification of drug molecules as a natural product from endophytes is being explored and utilized (Kusari et al. 2015).

One of the alternative mechanisms of enzymatic degradation is using AHL-lactonase and decarboxylase, also used to inhibit QS mechanism via hydrolyzing the lactone ring, and AHL-acylase and deaminases disrupt the acyl side chain, respectively (Chen et al. 2013). Further, acylases were extensively used to hydrolyze the amide moieties of AHL and they were specifically identified in several species like Streptomyces sp., P. aeruginosa, Comamonas, Pseudomonas syringae, Streptomyces sp., Bacillus cereus, and Kluyvera citrophila. Another enzyme namely, Metallo-β-lactamases were also reported in hydrolyzing the core lactone ring of AHL signaling molecules and reported information suggests that they were identified in Acinetobacter sp., Rhodococcus sp., A. tumefaciens and Chryseobacterium species (Zhang and Li 2016). Besides these, some of the biological compounds like Azithromycin, ceftazidime, and ciprofloxacin (CPR) were also reported to reduce the production of AHLs, which facilitates the change in the membrane permeability as a result, decreases in the concentration of AHL as well as expression of gene related to QS signaling cascade. Furthermore, down-regulation of abaI and A1S-0112 gene in Acinetobacter baumannii reduced by the action of streptomycin, which aids to decrease the concentration of 3-OH-C12-HSL at a sub-lethal concentration (Liu et al. 2011).

Application of quorum quenching in agriculture

Antibiotics have been used to kill the pathogenic micro-organisms and help to boost the health of the plants. However, antibiotic resistance is common in many bacterial phytopathogens like E. carotovora subsp. atroseptica, Xanthomonas sp., P. syringae, and Pectobacterium atrosepticum which leads to huge loss in the amount of crop production worldwide (Singh 2014). Further, the generation of resistance mechanism in bacterial population is due to QS and therefore, to inhibit the cascade, there is need of a mechanism which can restrict the pathway of QS. As a result, to combat the problem a novel approach involving QQ molecules have been used as bio-control method (i.e. in B. thuringiensis), also reducing the enzymatic action of QS ligand molecule. The entire phenomenon causes the impedance of the signal transduction mechanism of QS approach in the pathogen. Additionally, the application of QQ approach with respect to bacterial infection in a transgenic model of potato and tobacco plants have been reported and in this, the incorporation of quenching enzymes like lactonase has been used against the infection of E. carotovora (Gram-negative phytopathogen) (Hong et al. 2012). Moreover, genetic engineering assists to transfer some of the bacterial genes encoding QQ enzymes like Agrobacterium AttM lactonase and bacilli AiiA in different plants were achieved. Further, some of the plants expressing lactonase were observed to articulate reduction in QS signals in pathogens like Pectobacterium species causing soft-rot. In the emerging era, researchers are targeting QS mechanisms to increase the crop production by increasing the pre-harvest life. Further, diverse amount of QQ compounds have been identified against the QS autoinducers (Table 2). These impede the mechanisms important for the survival of the pathogens (through signaling between the microbial populations).
Table 2

List of QQ compounds present in some reported medicinal plants

Sl. no

Medicinal plant

Source

Quorum quenching compound

References

1.

Zingiber officinale

(ginger)

Essential oil

Monocyclic sesquiterpene α-zingiberene [2-methyl-5-(6 methylhept-5-en-2 yl)cyclohexa-1,3-diene]

Jaramillo-Colorado et al. (2012)

2.

Delisea pulchra (red algae)

Micoalga

Halogenated furanones

Teplitski et al. (2000)

3.

Curcuma longa (turmeric)

Extract

Curcumin [(1E,6E)-1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3,5-dione

Rudrappa and Bais (2008)

4.

Medicago sativa (alfalfa)

Seed exudates

An arginine analogue L-canavanine ((2S)-2-amino-4 {[(diaminomethylidene) amino]oxy}butanoic acid)

Keshavan et al. (2005)

5.

Myristica cinnamomea (nutmeg)

Nut extracts

Malabaricone C

Chong et al. (2011)

6.

Ocimum basilicum (sweet basil)

Root exudates

Rosmarinic acid (α-o-caffeoyl-3,4-dihydroxyphenyl lactic acid)

Walker et al. (2004)

7.

Psidium guajava (guava)

Extracts

Quercetin, quercetin-3-O-arabinoside

Vasavi et al. (2014)

8.

Fruits (e.g. apple, pear, peach, banana, pineapple, grape)

Extracts

Patulin (4-hydroxy-4H-furo[3,2-c]pyran-2(6H)-one)

Rasmussen et al. (2005)

9.

Brassica oleracea (broccoli)

Extracts

Synthetic preparations Isothiocyanates sulforaphane (4-methyl sulfinyl butyl isothiocyanate) and its precursor erucin (4-methyl thiobutyl isothiocyanate), analogues of iberin

Ganin et al. (Genin and Denny 2012)

10.

Allium sativum (garlic)

Bulb extracts

Ajoene (4,5,9-trithiadodeca-1,6,11-triene-9-oxide)

Kyung and Lee (2001), Chernin (2011) and Jakobsen et al. (2012)

11.

Elettaria cardamomun (green cardamom)

Essential oil

Cineol, syn/eucalyptol (1,3,3-trimethyl-2-oxabicyclo[2,2,2]octane)

Jaramillo-Colorado et al. (2012)

Conclusion

Endophytes primarily live in the niche by using the means of QS. Autoinducers of QS, help the endophytes to identify self non-self, kin non-kin and friend or foe. Also, QS assists to modify the pathogenic microbial population behavior. Further, identification of QS mechanisms may lead to the designing and synthesis of antimicrobial compounds which can result in enormous applications in the field of agriculture, pharmaceutical, and biotechnology industries. Moreover, by discerning the knowledge of QS signal, endophytes can be utilized to trouble-shoot the issues regarding our ecosystem e.g., combat soil pollution by the help of phytoremediation and rhizoremediation, augmentation of shelf-life and productivity of plants and biocontrol of phytopathogens. Additionally, studying and exploiting QS and QQ mechanisms of endophytes can assist in the up-gradation of rhizosphere, thus reducing the requirement of chemical fertilizers and pesticides. Hence, this can facilitate the need of sustainable agricultural practices, diminish the cost of production, and maintaining the socio-economic balance and environmental sustainability.

Notes

Funding

Funding has been received form Science and Engineering Research Board with Grand No. (No.SB/EMEQ-088/2014,Dt. 28/01/2016).

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Copyright information

© Society for Environmental Sustainability 2019

Authors and Affiliations

  • Ramappa Venkatesh Kumar
    • 1
    Email author
  • Raghwendra Pratap Singh
    • 2
  • Priyamvada Mishra
    • 1
  1. 1.Department of ZoologyBabasaheb Bhimrao Ambedkar UniversityLucknowIndia
  2. 2.Department of Nanotherapeutics and Nanomaterial ToxicologyIndustrial Toxicological Research CentreLucknowIndia

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