Exposure to parasitic protists and helminths changes the intestinal community structure of bacterial microbiota but not of eukaryotes in a cohort of mother-child binomial from a semi-rural setting in Mexico

Abstract

25Around 3.5 billion people are colonized by intestinal parasites worldwide. Intestinal parasitic 26 eukaryotes interact not only with the host, but also with the intestinal microbiota. In this work, we studied 27 the relationship between the presence of multiple enteric parasites and the community structure of the 28 bacterial and eukaryote intestinal microbiota in an asymptomatic cohort of mother-child binomials from a 29 semi-rural community in Mexico. The intestinal parasites identified were Blastocystis hominis, Entamoeba 30 histolytica/dispar, Endolimax nana, Chilomastix mesnili, Iodamoeba butshlii, Entamoeba coli, 31 Hymenolepis nana and Ascaris lumbricoides. We sequenced bacterial 16S rDNA and eukaryotic 18S 32 rDNA in fecal samples of 46 mothers and their respective children, with ages ranging from two to twenty 33 months. Although we did not find significant alpha-diversity changes, we found a significant effect of 34 parasite exposure on bacterial beta-diversity, which explained between 5.2% and 15.0% of the variation of 35 the bacterial community structure. Additionally, exposure to parasites was associated with significant 36 changes in relative abundances of bacterial taxa, characterized by increases in the Clostridia and decreased 37 Actinobacteria and Bacteroidia abundances. There were no significant changes of intestinal 38 microeukaryote abundances associated with parasite exposure. However, we found several significant 39 positive correlations between intestinal bacteria and eukaryotes, including co-occurrence of the fungi 40Candida tropicalis with Bacteroides and Actinomyces, and Saccharomycetales with Bifidobacterium and 41 Prevotella copri. These bacterial community structure changes associated with parasite exposure imply 42 effects on microbial metabolic routes, host nutrient uptake abilities and intestinal immunity regulation in 43 host-parasite interactions. 44 45 46 IMPORTANCE 47The impact of intestinal eukaryotes on the prokaryotic microbiome composition of asymptomatic 48 carriers has not been extensively explored, especially in children and in hosts with multiple parasites. In 49 this work, we studied the relationship between protist and helminth parasite colonization and intestinal 50 microbiota structure in an asymptomatic population of mother-child binomials from the semi-rural 51 community of Morelos in Mexico. We found that the presence of parasitic eukaryotes correlated with 52 changes in the bacterial community structure in the intestinal microbiota in an age-dependent way. This 53 was characterized by an increase of the relative abundance of the class Clostridia and the decrease of 54 Actinobacteria and Bacteroidia. While there were no significant associations between the presence of 55 parasites and microeukaryote community structure, we observed strong positive correlations between 56 bacterial and eukaryote taxa, identifying novel relationships between prokaryotes and fungi, and reflecting 57 the diet of the human population studied. 58 59 60 KEY WORDS 61 Parasites/Euk...

Detangling the Crosstalk Between Ascaris, Trichuris and Gut Microbiota: What´s Next?

“…Despite advances in sequencing technologies and bioinformatics tools, most studies involving the intestinal microbiota are still limited to bacterial communities and very little is known about how eukaryotes and virus influence and determine the composition, structure and functioning of the host gut microbiota and its interaction with parasites. To date, different protozoa and fungi have been linked with potential changes in the host gut microbiota ( Mason et al., 2012 ; Iebba et al., 2016 ; Nagel et al., 2016 ; Stensvold and van der Giezen, 2018 ; Partida-Rodriguez et al., 2019 ; Castañeda et al., 2020 ). Also, it is important to consider that helminth infections can coincide with other protozoa defining intestinal polyparasitism events ( Sayasone et al., 2011 ; Salcedo-Cifuentes et al., 2012 ; Cimino et al., 2015 ; Donohue et al., 2019 ; Geus et al., 2019 ; Gordon et al., 2020 ).…”