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Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during malnutrition

Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during malnutrition
Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during malnutrition

Undernutrition in children commonly disrupts the structure and function of the small intestinal microbial community, leading to enteropathies, compromised metabolic health, and impaired growth and development. The mechanisms by which diet and microbes mediate the balance between commensal and pathogenic intestinal flora remain elusive. In a murine model of undernutrition, we investigated the direct interactions Giardia lamblia, a prevalent small intestinal pathogen, on indigenous microbiota and specifically on Lactobacillus strains known for their mucosal and growth homeostatic properties. Our research reveals that Giardia colonization shifts the balance of lactic acid bacteria, causing a relative decrease in Lactobacillus spp . and an increase in Bifidobacterium spp . This alteration corresponds with a decrease in multiple indicators of mucosal and nutritional homeostasis. Additionally, protein-deficient conditions coupled with Giardia infection exacerbate the rise of primary bile acids and susceptibility to bile acid-induced intestinal barrier damage. In epithelial cell monolayers, Lactobacillus spp . mitigated bile acid-induced permeability, showing strain-dependent protective effects. In vivo, L. plantarum, either alone or within a Lactobacillus spp consortium, facilitated growth in protein-deficient mice, an effect attenuated by Giardia , despite not inhibiting Lactobacillus colonization. These results highlight Giardia's potential role as a disruptor of probiotic functional activity, underscoring the imperative for further research into the complex interactions between parasites and bacteria under conditions of nutritional deficiency.

bioRxiv
Bhatt, Aadra P.
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Arnold, Jason W.
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Awoniyi, Muyiwa
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Sun, Shan
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Santiago, Verônica Feijoli
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Quintela, Pedro Henrique
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Walsh, Kenneth
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Ngobeni, Renay
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Hansen, Brenna
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Gulati, Ajay
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Carroll, Ian M.
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Azcarate-Peril, M. Andrea
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Fodor, Anthony A.
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Swann, Jonathan
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Bartelt, Luther A.
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Bhatt, Aadra P.
dee53ae0-af2c-4fd0-97ea-e256e0242cd8
Arnold, Jason W.
e7b964c7-4c9b-44e4-bc78-8cd930f34feb
Awoniyi, Muyiwa
5429d9d1-b1e7-4ae6-99ea-f1a9864e267b
Sun, Shan
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Santiago, Verônica Feijoli
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Quintela, Pedro Henrique
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Walsh, Kenneth
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Ngobeni, Renay
5f558c66-9d14-4f2a-994e-904300c84308
Hansen, Brenna
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Gulati, Ajay
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Carroll, Ian M.
1c377eec-e4f1-4235-84ab-8887a91cd3a1
Azcarate-Peril, M. Andrea
4681819d-3a7f-48e5-87f5-71271bce520c
Fodor, Anthony A.
f11385bc-e11b-4efd-9c79-a28ea6d90b1a
Swann, Jonathan
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Bartelt, Luther A.
b1bf9b0e-8476-4594-9145-6ca797f8ef16

[Unknown type: UNSPECIFIED]

Record type: UNSPECIFIED

Abstract

Undernutrition in children commonly disrupts the structure and function of the small intestinal microbial community, leading to enteropathies, compromised metabolic health, and impaired growth and development. The mechanisms by which diet and microbes mediate the balance between commensal and pathogenic intestinal flora remain elusive. In a murine model of undernutrition, we investigated the direct interactions Giardia lamblia, a prevalent small intestinal pathogen, on indigenous microbiota and specifically on Lactobacillus strains known for their mucosal and growth homeostatic properties. Our research reveals that Giardia colonization shifts the balance of lactic acid bacteria, causing a relative decrease in Lactobacillus spp . and an increase in Bifidobacterium spp . This alteration corresponds with a decrease in multiple indicators of mucosal and nutritional homeostasis. Additionally, protein-deficient conditions coupled with Giardia infection exacerbate the rise of primary bile acids and susceptibility to bile acid-induced intestinal barrier damage. In epithelial cell monolayers, Lactobacillus spp . mitigated bile acid-induced permeability, showing strain-dependent protective effects. In vivo, L. plantarum, either alone or within a Lactobacillus spp consortium, facilitated growth in protein-deficient mice, an effect attenuated by Giardia , despite not inhibiting Lactobacillus colonization. These results highlight Giardia's potential role as a disruptor of probiotic functional activity, underscoring the imperative for further research into the complex interactions between parasites and bacteria under conditions of nutritional deficiency.

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Published date: 23 January 2024

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Local EPrints ID: 495181
URI: http://eprints.soton.ac.uk/id/eprint/495181
PURE UUID: fe364cf4-05a0-4071-bad8-b1fd228db8a7
ORCID for Jonathan Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 31 Oct 2024 17:35
Last modified: 01 Nov 2024 02:58

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Contributors

Author: Aadra P. Bhatt
Author: Jason W. Arnold
Author: Muyiwa Awoniyi
Author: Shan Sun
Author: Verônica Feijoli Santiago
Author: Pedro Henrique Quintela
Author: Kenneth Walsh
Author: Renay Ngobeni
Author: Brenna Hansen
Author: Ajay Gulati
Author: Ian M. Carroll
Author: M. Andrea Azcarate-Peril
Author: Anthony A. Fodor
Author: Jonathan Swann ORCID iD
Author: Luther A. Bartelt

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