Natural compounds inhibiting
Abstract
The biofilm lifestyle mode certainly represents one of the most successful behaviors to facilitate bacterial survival in diverse inhospitable environments. Conversely, the ability of bacteria to develop effective biofilms represents one of the major obstacles in the fight against bacterial infections. In Pseudomonas aeruginosa, the biofilm formation is intimately connected to the quorum sensing (QS) mechanisms, a mode of cell-to-cell communication that allows many bacteria to detect their population density in order to coordinate common actions. In this chapter, we propose an overview (i) on P. aeruginosa QS mechanisms and their implication in biofilm formation, and (ii) on natural products that are known to interfere with these QS mechanisms, subsequently disrupting biofilm formation. The concluding remarks focus on perspectives of these compounds as possible antibiotherapy adjuvants.
Keywords
- biofilm
- las
- natural products
- PQS
- pseudomonas
- quorum sensing
- rhl
1. Introduction
Bacterial infections are mainly related to the ability of bacteria to invade and disseminate through their hosts by using different types of motility, by releasing a myriad of virulence factors, by building structured biofilm which lead to host cell and tissue damage but also allow bacteria to evade the immune system and conventional antimicrobial agents [1]. For decades, antibiotics, although less effective in biofilm-growing bacteria [2], have represented our best weapon against bacterial diseases. However, the on-going emergence and worldwide spreading of resistant bacteria is considerably reducing the antibiotic pallet available for the treatment of bacterial infections [3]. This alarming situation forces researchers to consider other strategies to combat bacterial infections, notably the use of phages [4] or the use of alternative agents, such as essential oils [5], silver nanoparticles [6], bacteriocins [7], and antimicrobial peptides [8]. Some interesting strategies propose original compounds that disrupt biofilm formation without affecting the viability of invading bacteria; this strategy is expected (i) to reduce the bacterial aptitude to build protective barriers, but without exerting a selective pressure
In most bacteria, the expressions of virulence factors are coordinated by quorum sensing (QS) mechanisms, a cell-to-cell communication which allows bacteria to detect their population density by producing and perceiving diffusible signal molecules to synchronize common actions [9]. This cell-to-cell communication has been largely investigated in
2. P. aeruginosa biofilm lifestyle
Like most bacteria,
The biofilm formation can be delimited in five main stages (Figure 1, image A). A first reversible phase corresponds to the initial adhesion of bacteria to surfaces; this adhesion becomes irreversible in the second stage (image B). Then, thanks to a proliferation period corresponding to the third stage, microcolonies are built concomitantly with the production of extracellular matrix (image C), leading to the fourth stage of biofilm structuration and organization in which the growth of three dimensional communities is observed with amplified extracellular matrix production (image D). This biofilm cycle is completed by a dispersion step (image E) [12].
The secreted extracellular matrix mainly consists of proteins, nucleic acids, lipids, and exopolysaccharides (EPS). These account for 50–90% of total organic matter [16].
Extracellular DNA (eDNA) is an important component of
3. QS mechanisms and their implication in biofilm formation
The complex regulation of biofilm formation involves multiple bacterial machineries including the QS systems. In
Evidence that the
Furthermore, Gilbert et al. [33] observed the binding of the QS regulator LasR to the promoter region of the
Notably, the production of rhamnolipids and lectins is under QS control, indicating a further indirect link between biofilm formation/degradation and QS.
Indeed, the
4. Other mechanisms implied in biofilm formation
The QS systems are not the sole key actors intervening in biofilm formation by
5. Natural products that affect QS and biofilm formation by Pseudomonas aeruginosa
5.1 From prokaryotes
5.1.1 Enzymes
Microorganisms known to have the ability to produce anti-QS enzymes are still limited to a few bacteria from the families of (i)
Four types of enzymes are known to degrade AHLs [57, 58], a phenomenon sometimes described as “quorum quenching” (QQ) [59]; these include AHL-lactonases and decarboxylases that attack the lactone ring (
5.1.2 Organic acids
The acetic and phenyl lactic acids, found in the supernatant of probiotic strains
5.2 From fungi
5.2.1 Antibiotics and mycotoxins
Penicillin produced by
Erythromycin, a macrolide antibiotic isolated from
5.2.2 Alkylcyclopentanone
Recently, Kim et al. [77] indicated that the alkylcyclopentanone terrein, isolated from
5.3 From Plants
5.3.1 Derivatives of shikimic acid, phenols, and polyphenols
Many phenolic compounds and derivatives with anti-QS and antibiofilm activities have been isolated from plants [79]. Cinnamaldehyde [the dominant compound of certain essential oils, in particular
Ellagic acid derivatives from
Flavonoids have been investigated for their roles as QS modulating compounds. From these, naringenin and taxifolin reduced the expression of several QS-controlled genes (i.e.,
Furocoumarins from grapefruit can inhibit the QS signaling (AHLs and AI-2) of
Malabaricone C, a diarylnonanoid isolated from the bark of
A screening of various herbs revealed that a clove extract [
5.3.2 Alkaloids
Recently, caffeine (a purine alkaloid) has been shown to inhibit AHLs production and swarming mobility in
5.3.3 Terpenoids and Triterpenoids
The pentacyclic triterpenoid ursolic acid was identified as an inhibitor of biofilm formation from
5.3.4 Isothiocyanates and organosulfur compounds
Isothiocyanates produced by many plants are also QS inhibitors in
A further compound known to affect the QS-regulated genes in
5.4 From marine organisms
5.4.1 Furanones
A series of studies have indicated that marine organisms are a potential source of anti-QS [102–104]. The halogenated furanones produced by the red alga
5.4.2 Terpenoids
Following a screening of 284 extracts from the marine sponge
5.5 From animals and human
5.5.1 Enzymes
Type I porcine kidney acylase inactivates QS signals such as C6-HSL and 3-oxo-C12-HSL but not C4-HSL [50]. This type I acylase moderately reduces biofilm formation in
Mammalian cells release enzymes called paraoxonases 1 (extracted from human and murine sera) that have lactonase activity; degrading
5.5.2 Alkaloids
The
6. Concluding remarks
This review presents natural compounds reported to exhibit anti-QS and antibiofilm properties against
Origin | Compounds (class) | Target (QS) | Synergy with antibiotics | |
---|---|---|---|---|
Prokaryotes |
|
AHL-acylase (Enzyme) | AHL degradation | NC |
AHL-lactonase (Enzyme) | NC | |||
|
Acetic acid, lactic acid, phenyl lactic acid | AHL antagonist | NC | |
Fungi |
|
Penicillic acid (Furanone) | LasR and RhlR | NC |
Patulin (Furopyranone) | LasR and RhlR ǂ | + 1 | ||
|
Erythromycin (Macrolide) |
|
NC | |
|
Terrein (alkylcyclopentanone) | LasR and RhlR antagonist; c-di-GMP |
NC | |
marine organisms |
|
halogenated furanones and derivative | AHL antagonist | + 1 |
|
Manoalide (Sesterterpenoid) |
|
NC | |
Plants |
|
Cassipourol (terpenoid), β-sitosterol (terpenoid) |
|
+ 1 |
|
Catechin (Flavonoid) |
|
NC | |
|
Oleanolic aldehyde Coumarate (Phenolic compound) |
|
+ 1 | |
|
Ajoene (Organosulfur) |
|
+ 1 | |
|
Iberin (Isothiocyanate) |
|
NC | |
|
Ellagic acid derivatives (Phenolic compound) |
|
+ 1 | |
|
Eugenol (Phenylpropanoid) |
|
NC | |
|
Curcumin (Phenolic compound) | AHLs inhibition | NC | |
|
Bergamottin and dihydroxybergamottin (Furocoumarins) | AHLs inhibition | NC | |
|
Emodin (Anthraquinone) | docking traR * | + 2 | |
|
Baicalin (Flavonoid) |
|
+ 1 | |
|
6-gingerol (Phenolic compound) | docking lasR | NC | |
Animals and Human | Porcine kidney [50, 107] | Type I acylase | AHL degradation | NC |
Human and murine sera [109, 110] | Paraoxonases 1 Enzyme (lactonase) | AHL degradation | NC | |
|
Solenopsin A (Alkaloid) |
|
NC |
The increasing presence of antibiotic-resistant bacteria certainly pushes scientists to reorient the strategy of fight against bacterial infections to defer entry into a post-antibiotic era where major antibiotics would not be effective even for banal infections. Antivirulence approaches and antivirulence drugs are being increasingly considered as potential therapeutic alternatives and/or adjuvants to currently failing antibiotics. For example, oleanolic aldehyde coumarate and cassipourol, anti-QS compounds, exert interesting antibiofilm properties, restoring the effectiveness of the antibiotic tobramycin in the clearance of biofilm-encapsulated
Despite these important prospects, however, the big breakthrough in antibacterial strategies is still out of reach. This is probably due to a very complex entanglement between different QS systems, to the ability of
Acknowledgments
The authors would like to thank ARES (Académie de Recherche et d’Enseignement Supérieur, Belgium) for financial support throughout PRD projects.
Conflict of interest
The authors declare that there is no conflict of interests regarding the publication of this paper.
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