Gossip in the gut: Quorum sensing, a new player in the host-microbiota interactions

Abstract

Bacteria are known to communicate with each other and regulate their activities in social networks by secreting and sensing signaling molecules called autoinducers, a process known as quorum sensing (QS). This is a growing area of research in which we are expanding our understanding of how bacteria collectively modify their behavior but are also involved in the crosstalk between the host and gut microbiome. This is particularly relevant in the case of pathologies associated with dysbiosis or disorders of the intestinal ecosystem. This review will examine the different QS systems and the evidence for their presence in the intestinal ecosystem. We will also provide clues on the role of QS molecules that may exert, directly or indirectly through their bacterial gossip, an influence on intestinal epithelial barrier function, intestinal inflammation, and intestinal carcinogenesis. This review aims to provide evidence on the role of QS molecules in gut physiology and the potential shared by this new player. Better understanding the impact of intestinal bacterial social networks and ultimately developing new therapeutic strategies to control intestinal disorders remains a challenge that needs to be addressed in the future.

How does Quorum Sensing of Intestinal Bacteria Affect Our Health and Mental Status?

“…Gram-positive bacteria communicate using small linear or cyclized oligopeptides (QS peptides, QSPs) consisting of 5 to 17 amino acids [ 2 , 28 , 33 , 34 ]. The most studied QS systems are those produced by Bacillus , e.g., the competence sporulation factor (CSF), a pentapeptide, and the heptapeptide SDLPFEH (PapRIV).…”

“…The 3-oxo-C12-HSL produced by P. aeruginosa ( Figure 5 ) is actively transported across epithelial and immune cells [ 2 , 82 ] and destroys the permeability of the gut wall by repressing the expression of genes encoding tight junction proteins (TJs). This leads to the re-arranging (misplacing) of occludin, tricellulin, ZO-1, ZO-3, JAM-A, E-cadherin and β-catenin and prevents mucin production [ 2 , 83 , 84 ]. This not only exposes epithelial cells to infection but also activates the mucosal immune system, leading to an increase in leucocytes and the accumulation of pro-inflammatory cytokines [ 85 ].…”

“…Furthermore, 3-oxo-C12-HSL also inhibits tumor necrosis factor (TNF)-α and IL-12 production, causes malfunctioning of the T helper cell-1 (Th1) response and stimulates Th2 to produce immunoglobulin G1 [ 86 ]. Inhibition of Th1 and Th2 T lymphocyte differentiation increases cytokine production [ 87 ], intensifies oxidative stress, stimulates apoptosis and inactivates mitochondria [ 2 ].…”

“…Once in the cell, CSF acts as a reporter monitoring changes in the behavior or composition of the gut microbiota [ 109 ]. HSP-27 acts as a protein chaperone and an antioxidant but also facilitates the refolding of damaged proteins, thus preventing apoptosis and actin cytoskeletal remodeling [ 2 , 110 ]. The autoinducers AI-2 and AI-3 promote the expression of the immune mediators TNSF9 and IL-8 ( Figure 5 ), and 3-oxo-C12:2-HSL reduces the production of IL-8 by epithelial cells.…”

“…In a highly competitive and ever-changing environment such as the gastrointestinal tract (GIT), microbiota have developed unique methods to communicate with each other. Quorum sensing (QS) molecules produced by the gut microbiota regulate a variety of cell functions such as expression of virulence genes, formation of biofilms, competence and sporulation and usually only initiate these processes when cell numbers reach a certain density [ 1 , 2 , 3 ]. These signals include autoinducers (AIs) such as AI-1, AI-2 and AI-3; 3-oxo-C12-homoserine lactone (3-oxo-C12-HSL); C4-homoserine lactone (C4-HSL); 2-heptyl-3-hydroxy-4(1H)-quinoline; 2-heptyl-4-hydroxyquinoline (HHQ); QS peptides (QSPs); peptide pheromone Agr; pore-forming toxins such as hemolysins, leucocidins and phenol-soluble modulins (psms) and proteases.…”