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Review
. 2022 Nov 25:13:1002185.
doi: 10.3389/fmicb.2022.1002185. eCollection 2022.

Quorum sensing in human gut and food microbiomes: Significance and potential for therapeutic targeting

A Kate Falà  1   2   3 , Avelino Álvarez-Ordóñez  4 , Alain Filloux  5 , Cormac G M Gahan  1   2   6 , Paul D Cotter  1   3
Affiliations
Review

Quorum sensing in human gut and food microbiomes: Significance and potential for therapeutic targeting

A Kate Falà et al. Front Microbiol. .

Abstract

Human gut and food microbiomes interact during digestion. The outcome of these interactions influences the taxonomical composition and functional capacity of the resident human gut microbiome, with potential consequential impacts on health and disease. Microbe-microbe interactions between the resident and introduced microbiomes, which likely influence host colonisation, are orchestrated by environmental conditions, elements of the food matrix, host-associated factors as well as social cues from other microorganisms. Quorum sensing is one example of a social cue that allows bacterial communities to regulate genetic expression based on their respective population density and has emerged as an attractive target for therapeutic intervention. By interfering with bacterial quorum sensing, for instance, enzymatic degradation of signalling molecules (quorum quenching) or the application of quorum sensing inhibitory compounds, it may be possible to modulate the microbial composition of communities of interest without incurring negative effects associated with traditional antimicrobial approaches. In this review, we summarise and critically discuss the literature relating to quorum sensing from the perspective of the interactions between the food and human gut microbiome, providing a general overview of the current understanding of the prevalence and influence of quorum sensing in this context, and assessing the potential for therapeutic targeting of quorum sensing mechanisms.

Keywords: food matrix; food microbiome; gut microbiome; quorum quenching; quorum sensing; quorum sensing inhibition.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Overview of representative bacterial quorum sensing systems: Escherichia coli cell illustrates an Autoinducer 3 (AI-3) Quorum Sensing (QS) system which regulates the locus of enterocyte effacement (LEE) pathogenicity island (Walters and Sperandio, 2006; Machado Ribeiro et al., 2021); an Autoinducing Peptide (AIP) system in Lactococcus lactis is presented, in which nisin has a dual role as a Quorum Sensing Molecule (QSM) and antimicrobial peptide (Kleerebezem, 2004); Vibrio fischeri cell illustrates the control of bioluminescence through an Acylated Homoserine Lactone (AHL) system also referred to as Autoinducer 1 (AI-1; Nealson, Platt and Woodland Hastings, 1970); Autoinducer 2 (AI-2) signalling is presented at the intersection due to its role in species- and genera-agnostic communications. The AI-2 biosynthetic pathway is highlighted in yellow alongside the Lsr/Lux pathways which provide for its internalisation/detection in various genera (Pereira, Thompson and Xavier, 2013). Created with BioRender.com.
Figure 2
Figure 2
Overview of Quorum Sensing Processes as involved in food production, adapted from (Blana, Doulgeraki and Nychas, 2011; Plummer, 2012; Nahar et al., 2018; Quintieri et al., 2020; Wang and Xie, 2020). The left hand side of the figure in yellow maps food-associated bacteria reported in the literature to utilise QS for spoilage or pathogenesis, organised into columns based on the class of QSM (AHL, AI-2 and others) and by the type of food in which they are reported. This scheme is repeated on the right hand side in blue for those food-borne bacteria with positive attributes in food with respect to biopreservation and biotransformation. Created with BioRender.com.
Figure 3
Figure 3
Quorum Sensing Molecules (QSM) which have been detected in samples from the human gastrointestinal tract (white boxes). Mammalian receptors present in the human gut capable of binding QSM as ligands are shown in light green boxes towards the bottom of the figure. Created with BioRender.com.
Figure 4
Figure 4
Overview of the source and structures of some prominent examples of QQ enzymes and QSI compounds. Many QQ enzymes have been described for AHLs, such as the AHL acylase GqqA reported in Komagataeibacter europaeus isolated from grape vinegar [Werner et al., 2021; Image from the RCSB PDB (rcsb.org) of PDB ID 7ALZ], AHL lactonases such as AiiA from E. faecium isolated from the gut of Oreochromis niloticus [Vadassery and Pillai, 2020; Image from the RCSB PDB (rcsb.org) of PDB ID 7L5F] and paraoxonase enzymes which are expressed widely in mammalian tissues (Peyrottes et al., 2020). Oxidoreductase enzymes have been isolated from environments such as soil and activity has been reported against AHLs (Bijtenhoorn et al., 2011; Image from the RCSB PDB (rcsb.org) of PDB ID 3RKR) as well as AI-2 (Weiland-Bräuer et al., 2016). Examples of non-enzymatic QSI include tryptophol acetate, active against CAI-1 and AHLs (Malka et al., 2021), coumarin and derivatives, which can interfere with AHL-QS (Gutiérrez-Barranquero et al., 2015) and AIP analogues produced by closely related staphylococcal species (Peng et al., 2019). Created with BioRender.com.
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