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Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau

Intestinal parasitic infections, caused by helminths and protozoa, are globally distributed and major causes of worldwide morbidity. The gut microbiota may modulate parasite virulence and host response upon infection. The complex interplay between parasites and the gut microbiota is poorly understoo...

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Autores principales: von Huth, Sebastian, Thingholm, Louise B., Kofoed, Poul-Erik, Bang, Corinna, Rühlemann, Malte C., Franke, Andre, Holmskov, Uffe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7959362/
https://www.ncbi.nlm.nih.gov/pubmed/33657123
http://dx.doi.org/10.1371/journal.pntd.0009232
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author von Huth, Sebastian
Thingholm, Louise B.
Kofoed, Poul-Erik
Bang, Corinna
Rühlemann, Malte C.
Franke, Andre
Holmskov, Uffe
author_facet von Huth, Sebastian
Thingholm, Louise B.
Kofoed, Poul-Erik
Bang, Corinna
Rühlemann, Malte C.
Franke, Andre
Holmskov, Uffe
author_sort von Huth, Sebastian
collection PubMed
description Intestinal parasitic infections, caused by helminths and protozoa, are globally distributed and major causes of worldwide morbidity. The gut microbiota may modulate parasite virulence and host response upon infection. The complex interplay between parasites and the gut microbiota is poorly understood, partly due to sampling difficulties in remote areas with high parasite burden. In a large study of children in Guinea-Bissau, we found high prevalence of intestinal parasites. By sequencing of the 16S rRNA genes of fecal samples stored on filter paper from a total of 1,204 children, we demonstrate that the bacterial microbiota is not significantly altered by helminth infections, whereas it is shaped by the presence of both pathogenic and nonpathogenic protozoa, including Entamoeba (E.) spp. and Giardia (G.) lamblia. Within-sample diversity remains largely unaffected, whereas overall community composition is significantly affected by infection with both nonpathogenic E. coli (R(2) = 0.0131, P = 0.0001) and Endolimax nana (R(2) = 0.00902, P = 0.0001), and by pathogenic E. histolytica (R(2) = 0.0164, P = 0.0001) and G. lamblia (R(2) = 0.00676, P = 0.0001). Infections with multiple parasite species induces more pronounced shifts in microbiota community than mild ones. A total of 31 bacterial genera across all four major bacterial phyla were differentially abundant in protozoan infection as compared to noninfected individuals, including increased abundance of Prevotella, Campylobacter and two Clostridium clades, and decreased abundance of Collinsella, Lactobacillus, Ruminococcus, Veillonella and one Clostridium clade. In the present study, we demonstrate that the fecal bacterial microbiota is shaped by intestinal parasitic infection, with most pronounced associations for protozoan species. Our results provide insights into the interplay between the microbiota and intestinal parasites, which are valuable to understand infection biology and design further studies aimed at optimizing treatment strategies.
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spelling pubmed-79593622021-03-25 Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau von Huth, Sebastian Thingholm, Louise B. Kofoed, Poul-Erik Bang, Corinna Rühlemann, Malte C. Franke, Andre Holmskov, Uffe PLoS Negl Trop Dis Research Article Intestinal parasitic infections, caused by helminths and protozoa, are globally distributed and major causes of worldwide morbidity. The gut microbiota may modulate parasite virulence and host response upon infection. The complex interplay between parasites and the gut microbiota is poorly understood, partly due to sampling difficulties in remote areas with high parasite burden. In a large study of children in Guinea-Bissau, we found high prevalence of intestinal parasites. By sequencing of the 16S rRNA genes of fecal samples stored on filter paper from a total of 1,204 children, we demonstrate that the bacterial microbiota is not significantly altered by helminth infections, whereas it is shaped by the presence of both pathogenic and nonpathogenic protozoa, including Entamoeba (E.) spp. and Giardia (G.) lamblia. Within-sample diversity remains largely unaffected, whereas overall community composition is significantly affected by infection with both nonpathogenic E. coli (R(2) = 0.0131, P = 0.0001) and Endolimax nana (R(2) = 0.00902, P = 0.0001), and by pathogenic E. histolytica (R(2) = 0.0164, P = 0.0001) and G. lamblia (R(2) = 0.00676, P = 0.0001). Infections with multiple parasite species induces more pronounced shifts in microbiota community than mild ones. A total of 31 bacterial genera across all four major bacterial phyla were differentially abundant in protozoan infection as compared to noninfected individuals, including increased abundance of Prevotella, Campylobacter and two Clostridium clades, and decreased abundance of Collinsella, Lactobacillus, Ruminococcus, Veillonella and one Clostridium clade. In the present study, we demonstrate that the fecal bacterial microbiota is shaped by intestinal parasitic infection, with most pronounced associations for protozoan species. Our results provide insights into the interplay between the microbiota and intestinal parasites, which are valuable to understand infection biology and design further studies aimed at optimizing treatment strategies. Public Library of Science 2021-03-03 /pmc/articles/PMC7959362/ /pubmed/33657123 http://dx.doi.org/10.1371/journal.pntd.0009232 Text en © 2021 von Huth et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
von Huth, Sebastian
Thingholm, Louise B.
Kofoed, Poul-Erik
Bang, Corinna
Rühlemann, Malte C.
Franke, Andre
Holmskov, Uffe
Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title_full Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title_fullStr Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title_full_unstemmed Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title_short Intestinal protozoan infections shape fecal bacterial microbiota in children from Guinea-Bissau
title_sort intestinal protozoan infections shape fecal bacterial microbiota in children from guinea-bissau
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7959362/
https://www.ncbi.nlm.nih.gov/pubmed/33657123
http://dx.doi.org/10.1371/journal.pntd.0009232
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