Exposure to Parasitic Protists and Helminths Changes the Intestinal Community Structure of Bacterial Communities in a Cohort of Mother-Child Binomials from a Semirural Setting in Mexico


Por: Partida-Rodriguez, Oswaldo, Nieves-Ramirez, Miriam, Laforest-Lapointe, Isabelle, Brown, Eric M., Parfrey, Laura, Valadez-Salazar, Alicia, Thorson, Lisa, Moran, Patricia, Gonzalez, Enrique, Rascon, Edgar, Magaña U., Hernandez, Eric, Rojas-Velazquez, Liliana, Torres, Javier, Arrieta, Marie Claire, Ximenez, Cecilia, Finlay, B. Brett

Publicada: 1 jul 2021
Resumen:
An estimated 3.5 billion people are colonized by intestinal parasites worldwide. Intestinal parasitic eukaryotes interact not only with the host but also with the intestinal microbiota. In this work, we studied the relationship between the presence of multiple enteric parasites and the community structures of gut bacteria and eukaryotes in an asymptomatic mother-child cohort from a semirural community in Mexico. Fecal samples were collected from 46 mothers and their respective children, with ages ranging from 2 to 20 months. Mothers and infants were found to be multiparasitized by Blastocystis hominis, Entamoeba dispar, Endolimax nana, Chilomastix mesnili, lodamoeba butshlii, Entamoeba coil, Hymenolepis nana, and Ascaris lumbricoides. Sequencing of bacterial 16S rRNA and eukaryotic 18S rRNA genes showed a significant effect of parasite exposure on bacterial beta-diversity, which explained between 5.2% and 15.0% of the variation of the bacterial community structure in the cohort. Additionally, exposure to parasites was associated with significant changes in the relative abundances of multiple bacterial taxa, characterized by an increase in Clostridiales and decreases in Actinobacteria and Bacteroidales. Parasite exposure was not associated with changes in intestinal eukaryote relative abundances. However, we found several significant positive correlations between intestinal bacteria and eukaryotes, including Osciliospira with Entamoeba coli and Prevotella stercorea with Entamoeba hartmanni, as well as the co-occurrence of the fungus Candida with Bacteroides and Actinomyces, Bihdobactedum, and Prevotella copri and the fungus Pichia with Oscillospira. The parasitic exposure-associated changes in the bacterial community structure suggest effects on microbial metabolic routes, host nutrient uptake abilities, and intestinal immunity regulation in host-parasite interactions. IMPORTANCE The impact of intestinal eukaryotes on the prokaryotic microbiome composition of asymptomatic carriers has not been extensively explored, especially in infants and mothers with multiple parasitic infections. In this work, we studied the relationship between protist and helminth parasite colonization and the intestinal microbiota structure in an asymptomatic population of mother-child binomials from a semirural community in Mexico. We found that the presence of parasitic eukaryotes correlated with changes in the bacterial gut community structure in the intestinal microbiota in an age-dependent way. Parasitic infection was associated with an increase in the relative abundance of the class Clostridia and decreases of Actinobacteria and Bacteroidia. Parasitic infection was not associated with changes in the eukaryote community structure. However, we observed strong positive correlations between bacterial and other eukaryote taxa, identifying novel relationships between prokaryotes and fungi reflecting interkingdom interactions within the human intestine.

Filiaciones:
Partida-Rodriguez, Oswaldo:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Nieves-Ramirez, Miriam:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Laforest-Lapointe, Isabelle:
 Department of Physiology and Pharmacology, University of Calgarygrid.22072.35, Calgary, AB, Canada

 Department of Pediatrics, University of Calgarygrid.22072.35, Calgary, AB, Canada

 Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada

Brown, Eric M.:
 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Parfrey, Laura:
 Department of Zoology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Botany, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Valadez-Salazar, Alicia:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Thorson, Lisa:
 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Moran, Patricia:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Gonzalez, Enrique:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Rascon, Edgar:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Magaña U.:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Hernandez, Eric:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Rojas-Velazquez, Liliana:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Torres, Javier:
 Unidad de Investigación en Enfermedades Infecciosas, UMAE Pediatria, IMSSMexico City, Mexico

Arrieta, Marie Claire:
 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Physiology and Pharmacology, University of Calgarygrid.22072.35, Calgary, AB, Canada

 Department of Pediatrics, University of Calgarygrid.22072.35, Calgary, AB, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

Ximenez, Cecilia:
 Laboratorio de Inmunología del Unidad de Medicina Experimental, UNAMMexico City, Mexico

Finlay, B. Brett:
 Michael Smith Laboratories, Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Biochemistry and Molecular Biology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada

 Department of Microbiology and Immunology, University of British Columbiagrid.17091.3e, Vancouver, BC, Canada
ISSN: 23795042





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AMER SOC MICROBIOLOGY, 1752 N ST NW, WASHINGTON, DC 20036-2904 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 6 Número: 4
Páginas: 8321
WOS Id: 000709948400014
ID de PubMed: 34406855
imagen gold, Green Published, All Open Access, Gold, Green

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