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 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. Author summary Infections with enteric parasites, including helminths and protozoa, are among the most common infections in poor countries. These infections continue to have enormous impact on both mortality and morbidity worldwide. Enteric parasites inhabit the gut of the infected host, but how infections with these parasites may change the composition of bacteria within the gut remains more or less unclear. Here, we explore how the bacterial composition in stool from children from Guinea-Bissau (Western Africa) is altered by infection with different enteric parasite species. We find that infections with multiple parasite species induces more pronounced changes in the bacterial composition, and that certain parasite species significantly changes the diversity of bacteria. Furthermore, we demonstrate that fecal samples stored at room temperature on filter papers for months can be used in field studies of gut bacteria composition. Our study provides new insights into the complex relationship between enteric parasites and fecal bacteria composition, and may pave the way for new treatment options and help explain why some people are more susceptible to infection compared to others.

Automated summary

This study shows that infections with intestinal parasites significantly affect the composition of the gut microbiota, especially infections with protozoa. Multiple parasite species induce more pronounced changes in the bacterial composition, and specific parasite species alter the diversity of bacteria. This research provides valuable insights into the relationship between enteric parasites and fecal bacteria composition, which could lead to new treatment strategies and a better understanding of susceptibility differences in individuals.