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Interaction between Intestinal Parasites and the Gut Microbiota: Implications for the Intestinal Immune Response and Host Defence

Grondin, Jensine A., Jamal, Asif, Mowna, Sadrina, Seto, Tyler, Khan, Waliul I.·2024·Pathogens
DOI 10.3390/pathogens13080608PMC PMC11356857
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Abstract

Intestinal parasites, including helminths and protozoa, account for a significant portion of the global health burden. The gastrointestinal (GI) tract not only serves as the stage for these parasitic infections but also as the residence for millions of microbes. As the intricacies of the GI microbial milieu continue to unfold, it is becoming increasingly apparent that the interactions between host, parasite, and resident microbes help dictate parasite survival and, ultimately, disease outcomes. Across both clinical and experimental models, intestinal parasites have been shown to impact microbial composition and diversity. Reciprocally, microbes can directly influence parasitic survival, colonization and expulsion. The gut microbiota can also indirectly impact parasites through the influence and manipulation of the host. Studying this host–parasite–microbiota axis may help bring about novel therapeutic strategies for intestinal parasitic infection as well as conditions such as inflammatory bowel disease (IBD). In this review, we explore the relationship between intestinal parasites, with a particular focus on common protozoa and helminths, and the gut microbiota, and how these interactions can influence the host defence and intestinal immune response. We will also explore the impact of this tripartite relationship in a clinical setting and its broader implications for human health.

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Figure 1 Overview of the impact that protozoan and helminthic infection can have on the gut microbiota. Protozoan and helminth intestinal infections have been reported to induce changes in microbial composition and diversity in both human and animal models. Helminths have been shown to impact the gut microbiota in a variety of ways, including (1) the release of excretory–secretory products (ESPs), (2) the release of extracellular vesicles (ECVs), and (3) modulating the release of host-derived antimicrobial peptides (AMPs) through toll-like receptors (TLRs). Both protozoan and helminth infection in the gut can (4) impact nutrient availability and (5) mucus barrier integrity, and thus, indirectly affect the microbes of the gut.
Figure 1 Overview of the impact that protozoan and helminthic infection can have on the gut microbiota. Protozoan and helminth intestinal infections have been reported to induce changes in microbial composition and diversity in both human and animal models. Helminths have been shown to impact the gut microbiota in a variety of ways, including (1) the release of excretory–secretory products (ESPs), (2) the release of extracellular vesicles (ECVs), and (3) modulating the release of host-derived antimicrobial peptides (AMPs) through toll-like receptors (TLRs). Both protozoan and helminth infection in the gut can (4) impact nutrient availability and (5) mucus barrier integrity, and thus, indirectly affect the microbes of the gut.CC BY · PubMed Central
Figure 2 Summary of the potential ways the gut microbiota can impact parasite fitness and infectivity. The gut microbiota can both directly and indirectly impact intestinal parasite establishment, survival, colonization and expulsion within the host. Microbes have been shown to (1) induce altered gene expression in helminths, (2) directly impact helminth fitness, and (3) promote helminth egg hatching. The microbiota can also (4) inhibit the growth of particular protozoa through the production of metabolites such as indoles. Further, microbes can influence the overall environment of the gut by (5) impacting mucus layer integrity and (6) sequestering nutrients, both of which impact parasite fitness.
Figure 2 Summary of the potential ways the gut microbiota can impact parasite fitness and infectivity. The gut microbiota can both directly and indirectly impact intestinal parasite establishment, survival, colonization and expulsion within the host. Microbes have been shown to (1) induce altered gene expression in helminths, (2) directly impact helminth fitness, and (3) promote helminth egg hatching. The microbiota can also (4) inhibit the growth of particular protozoa through the production of metabolites such as indoles. Further, microbes can influence the overall environment of the gut by (5) impacting mucus layer integrity and (6) sequestering nutrients, both of which impact parasite fitness.CC BY · PubMed Central
Figure 3 Overview of the various ways microbial manipulation can modulate host immune responses and parasitic defence. In addition to the direct manipulation of the luminal environment, the gut microbiota can also indirectly impact parasitic fitness and clearance through interactions with the host. These include, but are not limited to, (1) impacting the development of the immune system, (2) altering intestinal motility, impacting the mucus barrier integrity and mucin production through (3) NOD1/2 signalling and the production of (4) short-chain fatty acids (SCFAs). Microbes can also impact (5) the ratios of Th2/Treg cells, Treg proliferation and the production of the anti-inflammatory cytokine, IL-10. (6) The gut microbiota has also been shown to, through the TLR-MyD88 pathway, alter the production of IL-4 and IL-13 and, subsequently, the release of antimicrobial peptides like SPRR2A, key factors in parasite clearance.
Figure 3 Overview of the various ways microbial manipulation can modulate host immune responses and parasitic defence. In addition to the direct manipulation of the luminal environment, the gut microbiota can also indirectly impact parasitic fitness and clearance through interactions with the host. These include, but are not limited to, (1) impacting the development of the immune system, (2) altering intestinal motility, impacting the mucus barrier integrity and mucin production through (3) NOD1/2 signalling and the production of (4) short-chain fatty acids (SCFAs). Microbes can also impact (5) the ratios of Th2/Treg cells, Treg proliferation and the production of the anti-inflammatory cytokine, IL-10. (6) The gut microbiota has also been shown to, through the TLR-MyD88 pathway, alter the production of IL-4 and IL-13 and, subsequently, the release of antimicrobial peptides like SPRR2A, key factors in parasite clearance.CC BY · PubMed Central

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Cited by

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Metadata

Authors
Grondin, J. A., Jamal, A., Mowna, S., Seto, T., & Khan, W. I.
Venue
Pathogens
Publisher
MDPI AG
Published
2024-07-23
Volume
13
Issue
8
Pages
608
ISSN
2076-0817
DOI
10.3390/pathogens13080608
PMC
PMC11356857
Cited by
44
References
7
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-06739)

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