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 <i>Giardia lamblia</i>, 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 <i>Giardia</i> colonization shifts the balance of lactic acid bacteria, causing a relative decrease in <i>Lactobacillus spp</i>. and an increase in <i>Bifidobacterium spp</i>. This alteration corresponds with a decrease in multiple indicators of mucosal and nutritional homeostasis. Additionally, protein-deficient conditions coupled with <i>Giardia</i> infection exacerbate the rise of primary bile acids and susceptibility to bile acid-induced intestinal barrier damage. In epithelial cell monolayers, <i>Lactobacillus spp</i>. mitigated bile acid-induced permeability, showing strain-dependent protective effects. <i>In vivo, L. plantarum</i>, either alone or within a <i>Lactobacillus</i> spp consortium, facilitated growth in protein-deficient mice, an effect attenuated by <i>Giardia</i>, 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.
Authors
- Jamie Xiao
- Renay Ngobeni (ORCID: https://orcid.org/0000-0001-9235-1542)
- Muyiwa Awoniyi (ORCID: https://orcid.org/0000-0002-5811-070X)
- Jonathan R. Swann (ORCID: https://orcid.org/0000-0002-6485-4529)
- Ajay Gulati (ORCID: https://orcid.org/0000-0002-7612-6369)
- Brenna Hansen
- Verônica Feijoli Santiago (ORCID: https://orcid.org/0000-0002-0052-9532)
- Jason W. Arnold (ORCID: https://orcid.org/0000-0002-6363-6140)
- Kenneth Walsh (ORCID: https://orcid.org/0000-0001-7580-2276)
- Luther A. Bartelt (ORCID: https://orcid.org/0000-0002-7596-4272)
- Shan Sun (ORCID: https://orcid.org/0000-0003-0349-2664)
- M. Andrea Azcárate-Peril (ORCID: https://orcid.org/0000-0003-0325-1289)
- Pedro Henrique Quintela
- Deniz Coskuner
- Anthony A. Fodor (ORCID: https://orcid.org/0000-0002-9305-4264)
- Aadra P. Bhatt (ORCID: https://orcid.org/0000-0002-0134-6543)
- Ian M. Carroll
Institutions
- University of North Carolina at Charlotte (US)
- University of North Carolina at Chapel Hill (US)
- Cleveland Clinic (US)
- Duke University (US)
- Universidade Federal do Ceará (BR)
- Stellenbosch University (ZA)
- University of Southampton (GB)
Publication Details
- Journal
- Gut Microbes
- Published
- 2024-11-05
- DOI
- https://doi.org/10.1080/19490976.2024.2421623
- Citations
- 5
- Primary Topic
- Parasitic Infections and Diagnostics
- Type
- article
- Field-Weighted Citation Impact
- 2.58
Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases