Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice

ABSTRACT Candida albicans is an opportunistic pathogen that causes gastrointestinal (GI) candidiasis closely associated with intestinal inflammation and dysbiosis. Drug resistance, side effects of available antifungal agents, and the high recurrence of candidiasis highlight the need for new treatmen...

Full description

Bibliographic Details
Main Authors: Hélène Authier, Valérie Bardot, Lucile Berthomier, Bénédicte Bertrand, Claude Blondeau, Sophie Holowacz, Agnès Coste
Format: Article
Language:English
Published: American Society for Microbiology 2022-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02355-21
_version_ 1818141822870880256
author Hélène Authier
Valérie Bardot
Lucile Berthomier
Bénédicte Bertrand
Claude Blondeau
Sophie Holowacz
Agnès Coste
author_facet Hélène Authier
Valérie Bardot
Lucile Berthomier
Bénédicte Bertrand
Claude Blondeau
Sophie Holowacz
Agnès Coste
author_sort Hélène Authier
collection DOAJ
description ABSTRACT Candida albicans is an opportunistic pathogen that causes gastrointestinal (GI) candidiasis closely associated with intestinal inflammation and dysbiosis. Drug resistance, side effects of available antifungal agents, and the high recurrence of candidiasis highlight the need for new treatments. We investigated the effects of hydroethanolic extracts of licorice root (LRE) and walnut leaf (WLE) on GI colonization by C. albicans, colon inflammation, and gut microbiota composition in C57BL/6 female mice. Oral administration of LRE and WLE alone or in combination once daily for 12 days before C. albicans infection and then for 5 days after infection significantly reduced the level of C. albicans in the feces of gastrointestinal infected mice as well as colonization of the GI tract, both extracts showing robust antifungal activity. Although total bacterial content was unaffected by the extracts (individually or combined), the abundance of protective bacteria, such as Bifidobacterium spp. and Faecalibacterium prausnitzii, increased with the combination, in contrast to that of certain pathobiont bacteria, which decreased. Interestingly, the combination induced a more robust decrease in the expression of proinflammatory genes than either extract alone. The anti-inflammatory activity of the combination was further supported by the reciprocal increase in the expression of anti-inflammatory cytokines and the significant decrease in enzymes involved in the synthesis of proinflammatory eicosanoids and oxidative stress. These findings suggest that LRE and WLE have synergistic effects and that the LRE/WLE combination could be a good candidate for limiting GI candidiasis and associated inflammation, likely by modulating the composition of the gut microbiota. IMPORTANCE The adverse effects and emergence of resistance of currently available antifungals and the high recurrence of candidiasis prompt the need for alternative and complementary strategies. We demonstrated that oral administration of hydroethanolic extracts of licorice root (LRE) and walnut leaf (WLE) separately or in combination significantly reduced the colonization of the gastrointestinal (GI) tract by C. albicans, highlighting a robust antifungal activity of these plant extracts. Interestingly, our data indicate a correlation between LRE and WLE consumption, in particular the combination, and a shift within the gut microbiome toward a protective profile, a decrease in colonic inflammation and prooxidant enzymes, suggesting a synergistic effect. This study highlights the significant prebiotic potential of the LRE/WLE combination and suggests that the health benefits are due, at least in part, to their ability to modulate the gut microbiota, reduce inflammation and oxidative stress, and protect against opportunistic infection.
first_indexed 2024-12-11T11:06:00Z
format Article
id doaj.art-976c92298bd84824838084f4ef0531aa
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-12-11T11:06:00Z
publishDate 2022-04-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-976c92298bd84824838084f4ef0531aa2022-12-22T01:09:41ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-04-0110210.1128/spectrum.02355-21Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in MiceHélène Authier0Valérie Bardot1Lucile Berthomier2Bénédicte Bertrand3Claude Blondeau4Sophie Holowacz5Agnès Coste6Geroscience and Rejuvenation Research Center (RESTORE), UMR 1301-Inserm 5070-CNRS EFS, Université P. Sabatier, Toulouse, FrancePiLeJe Industrie, Saint-Bonnet-de-Rochefort, FrancePiLeJe Industrie, Saint-Bonnet-de-Rochefort, FranceGeroscience and Rejuvenation Research Center (RESTORE), UMR 1301-Inserm 5070-CNRS EFS, Université P. Sabatier, Toulouse, FrancePiLeJe Laboratoire, Paris, FrancePiLeJe Laboratoire, Paris, FranceGeroscience and Rejuvenation Research Center (RESTORE), UMR 1301-Inserm 5070-CNRS EFS, Université P. Sabatier, Toulouse, FranceABSTRACT Candida albicans is an opportunistic pathogen that causes gastrointestinal (GI) candidiasis closely associated with intestinal inflammation and dysbiosis. Drug resistance, side effects of available antifungal agents, and the high recurrence of candidiasis highlight the need for new treatments. We investigated the effects of hydroethanolic extracts of licorice root (LRE) and walnut leaf (WLE) on GI colonization by C. albicans, colon inflammation, and gut microbiota composition in C57BL/6 female mice. Oral administration of LRE and WLE alone or in combination once daily for 12 days before C. albicans infection and then for 5 days after infection significantly reduced the level of C. albicans in the feces of gastrointestinal infected mice as well as colonization of the GI tract, both extracts showing robust antifungal activity. Although total bacterial content was unaffected by the extracts (individually or combined), the abundance of protective bacteria, such as Bifidobacterium spp. and Faecalibacterium prausnitzii, increased with the combination, in contrast to that of certain pathobiont bacteria, which decreased. Interestingly, the combination induced a more robust decrease in the expression of proinflammatory genes than either extract alone. The anti-inflammatory activity of the combination was further supported by the reciprocal increase in the expression of anti-inflammatory cytokines and the significant decrease in enzymes involved in the synthesis of proinflammatory eicosanoids and oxidative stress. These findings suggest that LRE and WLE have synergistic effects and that the LRE/WLE combination could be a good candidate for limiting GI candidiasis and associated inflammation, likely by modulating the composition of the gut microbiota. IMPORTANCE The adverse effects and emergence of resistance of currently available antifungals and the high recurrence of candidiasis prompt the need for alternative and complementary strategies. We demonstrated that oral administration of hydroethanolic extracts of licorice root (LRE) and walnut leaf (WLE) separately or in combination significantly reduced the colonization of the gastrointestinal (GI) tract by C. albicans, highlighting a robust antifungal activity of these plant extracts. Interestingly, our data indicate a correlation between LRE and WLE consumption, in particular the combination, and a shift within the gut microbiome toward a protective profile, a decrease in colonic inflammation and prooxidant enzymes, suggesting a synergistic effect. This study highlights the significant prebiotic potential of the LRE/WLE combination and suggests that the health benefits are due, at least in part, to their ability to modulate the gut microbiota, reduce inflammation and oxidative stress, and protect against opportunistic infection.https://journals.asm.org/doi/10.1128/spectrum.02355-21candidiasisgut inflammationlicoriceplant extractprebioticwalnut
spellingShingle Hélène Authier
Valérie Bardot
Lucile Berthomier
Bénédicte Bertrand
Claude Blondeau
Sophie Holowacz
Agnès Coste
Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
Microbiology Spectrum
candidiasis
gut inflammation
licorice
plant extract
prebiotic
walnut
title Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
title_full Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
title_fullStr Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
title_full_unstemmed Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
title_short Synergistic Effects of Licorice Root and Walnut Leaf Extracts on Gastrointestinal Candidiasis, Inflammation and Gut Microbiota Composition in Mice
title_sort synergistic effects of licorice root and walnut leaf extracts on gastrointestinal candidiasis inflammation and gut microbiota composition in mice
topic candidiasis
gut inflammation
licorice
plant extract
prebiotic
walnut
url https://journals.asm.org/doi/10.1128/spectrum.02355-21
work_keys_str_mv AT heleneauthier synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT valeriebardot synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT lucileberthomier synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT benedictebertrand synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT claudeblondeau synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT sophieholowacz synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice
AT agnescoste synergisticeffectsoflicoricerootandwalnutleafextractsongastrointestinalcandidiasisinflammationandgutmicrobiotacompositioninmice