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Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during protein deficiency

Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during protein deficiency
Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during protein deficiency

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.

bile acids, Giardia, gnotobiotic models, malnourishment, probiotics
1949-0976
2421623
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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Feijoli Santiago, Verônica
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Coskuner, Deniz
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Henrique Quintela, Pedro
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Walsh, Kenneth
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Xiao, Jamie
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Ngobeni-Nyambi, Renay
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Hansen, Brenna
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Gulati, Ajay S.
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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
67e36937-c87f-43ce-93a8-eecb9ec9d6f4
Feijoli Santiago, Verônica
36fa3e9e-e19b-41b4-b852-cbc1afae4f83
Coskuner, Deniz
2c054be9-35f8-43bf-8173-6b6e7f5642c7
Henrique Quintela, Pedro
d6681afc-7ee7-4e48-ada7-5c3851592588
Walsh, Kenneth
f38639d4-d604-41e8-9f9e-b5bfac922a45
Xiao, Jamie
9c402996-8efa-4830-ab48-3fd1a4fca449
Ngobeni-Nyambi, Renay
8dc1bc27-8369-4761-8c9c-4814f4e83375
Hansen, Brenna
4907b51a-a869-4174-af18-c67fb25efde9
Gulati, Ajay S.
863d0fc3-cfe7-4269-a085-aa34a7f945c3
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
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Bartelt, Luther A.
b1bf9b0e-8476-4594-9145-6ca797f8ef16

Bhatt, Aadra P., Arnold, Jason W., Awoniyi, Muyiwa, Sun, Shan, Feijoli Santiago, Verônica, Coskuner, Deniz, Henrique Quintela, Pedro, Walsh, Kenneth, Xiao, Jamie, Ngobeni-Nyambi, Renay, Hansen, Brenna, Gulati, Ajay S., Carroll, Ian M., Azcarate-Peril, M. Andrea, Fodor, Anthony A., Swann, Jonathan and Bartelt, Luther A. (2024) Giardia antagonizes beneficial functions of indigenous and therapeutic intestinal bacteria during protein deficiency. Gut Microbes, 16 (1), 2421623. (doi:10.1080/19490976.2024.2421623).

Record type: Article

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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Accepted/In Press date: 21 October 2024
Published date: 5 November 2024
Keywords: bile acids, Giardia, gnotobiotic models, malnourishment, probiotics

Identifiers

Local EPrints ID: 495619
URI: http://eprints.soton.ac.uk/id/eprint/495619
ISSN: 1949-0976
PURE UUID: ebfb11ca-1825-47fa-9117-550919a663d2
ORCID for Jonathan Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 19 Nov 2024 17:44
Last modified: 23 Nov 2024 03:00

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Contributors

Author: Aadra P. Bhatt
Author: Jason W. Arnold
Author: Muyiwa Awoniyi
Author: Shan Sun
Author: Verônica Feijoli Santiago
Author: Deniz Coskuner
Author: Pedro Henrique Quintela
Author: Kenneth Walsh
Author: Jamie Xiao
Author: Renay Ngobeni-Nyambi
Author: Brenna Hansen
Author: Ajay S. 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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