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. 2025 Apr 4;15(7):1047.
doi: 10.3390/ani15071047.

Swine Gut Lactic Acid Bacteria and Their Exopolysaccharides Differentially Modulate Toll-like Receptor Signaling Depending on the Agave Fructans Used as a Carbon Source

Enrique A Sanhueza-Carrera  1   2 , Cynthia Fernández-Lainez  3 , César Castro-De la Mora  4 , Daniel Ortega-Álvarez  4 , Claudia Mendoza-Camacho  4 , Jesús Manuel Cortéz-Sánchez  5 , Beatriz Pérez-Guillé  6 , Paul de Vos  7 , Gabriel López-Velázquez  1
Affiliations

Swine Gut Lactic Acid Bacteria and Their Exopolysaccharides Differentially Modulate Toll-like Receptor Signaling Depending on the Agave Fructans Used as a Carbon Source

Enrique A Sanhueza-Carrera et al. Animals (Basel). .

Abstract

Exopolysaccharides (EPSs) produced by probiotic bacteria have garnered attention due to their effects on the gut health of humans and animals. The nutrients that probiotics access during their growth are essential for producing beneficial effects on host health. Direct immunomodulatory effects of graminan-type fructans (GTFs) from Agave tequilana through toll-like receptors (TLRs) have been demonstrated. However, the immunomodulatory effects of these fructans, mediated through the EPSs produced by the probiotics cultivated with them, remain unexplored. We explored the immunomodulatory effects of lactic acid bacteria (LAB) strains isolated from swine and their EPSs, based on the GTFs used as carbon sources during their growth. While the LAB strains activated the NF-κB pathway independently of the GTF source, their EPSs activated it in a GTF source-dependent manner. LAB activation through TLR2 showed a GTF source dependency, whereas their EPSs activated TLR2 independently of the GTF source. The LAB and their EPSs activated TLR4 in a GTF source-dependent manner. Both the LAB and their EPSs inhibited the activation of TLR2 and TLR4 agonists, which exhibited a strong dependence on the GTF source. The strength of GTF C's immunomodulatory effects on LAB illustrates its specificity, its impact on the EPS structure, and its biological effects. Our results support the promising health benefits of this synbiotic model for swine health and lowering inflammation.

Keywords: TLRs; agave; exopolysaccharides; fructans; lactobacilli; probiotics; swine.

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Conflict of interest statement

The authors declare that there are no conflicts of interest.

Figures

Figure 1
Figure 1
Exopolysaccharide production by LAB strains isolated from swine feces. Data are expressed as EPS micrograms isolated from each milliliter of LAB culture.
Figure 2
Figure 2
Growth curves of the INP_MX_001 LAB strain incubated with three different graminan-type fructans as carbon sources.
Figure 3
Figure 3
Comparison between the EPSs produced by the LAB strain isolated from swine feces and the EPSs produced by other well-characterized lactobacilli incubated with three different graminan-type fructans as carbon sources. The data are expressed as EPS micrograms isolated from each milliliter of bacterium culture. * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001.
Figure 4
Figure 4
Activation of the NF-κB pathway in THP1 reporter cells by LAB grown with different GTFs as carbon sources and by EPSs obtained from the abovementioned LAB. (A) Effects of the LAB strain when incubated using the different GTFs as carbon sources; (B) effects of the EPSs extracted from the abovementioned LAB strain under the same conditions. Activation is shown as the fold change of the untreated control. The results are plotted as the mean ± Std. deviation; **** p-value < 0.0001.
Figure 5
Figure 5
The activation of the NF-κB pathway via TLR2 by LAB grown with different GTFs as a carbon source and by EPSs was obtained from the LAB mentioned above. (A) Effects of the LAB strain when incubated using the different GTFs as carbon sources; (B) effects of the EPSs extracted from the abovementioned LAB strain under the same conditions. Activation is shown as the fold change of the untreated control. The results are plotted as the mean ± Std. deviation; * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001.
Figure 6
Figure 6
Inhibitory effect of a LAB strain isolated from swine and grown with three structurally different graminan-type fructans (GTF A, B, and C) and inhibitory effect of EPSs obtained from this LAB strain on the TLR2 reporter cell line. (A) Effects of the LAB strain when incubated using the different GTFs as carbon sources; (B) effects of the EPSs extracted from the abovementioned LAB strain under the same conditions. Inhibition is shown as the fold change of the TLR2 agonist, Pam3CSK4. The results are plotted as the mean ± Std. deviation; **** p < 0.0001.
Figure 7
Figure 7
Activation of NF-κB pathway via TLR4 by LAB grown with different GTFs as carbon sources and by EPSs obtained from the LAB mentioned above. (A) Effects of the LAB strain when incubated using the different GTFs as carbon sources; (B) effects of the EPSs extracted from the abovementioned LAB strain under the same conditions. Activation is shown as the fold change of the untreated control. The results are plotted as the mean ± Std. deviation; * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001.
Figure 8
Figure 8
Inhibitory effects of a LAB strain isolated from a pig, grown with three different graminan-type fructans (GTF A, B, and C) obtained from three GTFs, and inhibitory effects of EPSs obtained from this LAB strain on the TLR4 reporter cell line. (A) Effects of the LAB strain when incubated using the different GTFs as carbon sources; (B) effects of the EPSs extracted from the abovementioned LAB strain under the same conditions. Inhibition is shown as the fold change of the TLR4 agonist, LPS, 10 ng/mL. The results are plotted as the mean ± Std. deviation; **** p < 0.0001.
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