Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths

ABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infect...

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Autores principales:	Alice V. Easton, Mayra Raciny-Aleman, Victor Liu, Erica Ruan, Christian Marier, Adriana Heguy, Maria Fernanda Yasnot, Ana Rodriguez, P’ng Loke
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Colombia Plasmodium vivax STH soil-transmitted helminths Trichuris trichiura malaria Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ea1ee9d4557e4aadbe57d74532554d83
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spelling	oai:doaj.org-article:ea1ee9d4557e4aadbe57d74532554d832021-11-15T16:19:08ZImmune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths10.1128/mBio.01705-202150-7511https://doaj.org/article/ea1ee9d4557e4aadbe57d74532554d832020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01705-20https://doaj.org/toc/2150-7511ABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infected with STH alone, or not infected with either P. vivax or STH. In addition to a complete blood count (CBC) with differential, transcriptional profiling of peripheral blood samples was performed by transcriptome sequencing (RNA-Seq), fecal microbial communities were determined by 16S rRNA gene sequencing, and circulating cytokine levels were measured by bead-based immunoassays. Differences in blood cell counts, including an increased percentage of neutrophils, associated with a transcriptional signature of neutrophil activation, were driven primarily by P. vivax infection. P. vivax infection was also associated with increased levels of interleukin 6 (IL-6), IL-8, and IL-10; these cytokine levels were not affected by STH coinfection. Surprisingly, P. vivax infection was more strongly associated with differences in the microbiota than STH infection. Children infected with only P. vivax exhibited elevated Bacteroides and reduced Prevotella and Clostridiaceae levels, but these differences were not observed in individuals coinfected with STH. We also observed that P. vivax parasitemia was higher in the STH-infected population. When we used machine learning to identify the most important predictors of the P. vivax parasite burden (among P. vivax-infected individuals), bacterial taxa were the strongest predictors of parasitemia. In contrast, circulating transforming growth factor β (TGF-β) was the strongest predictor of the Trichuris trichiura egg burden. This study provides unexpected evidence that the gut microbiota may have a stronger link with P. vivax than with STH infection. IMPORTANCE Plasmodium (malaria) and helminth parasite coinfections are frequent, and both infections can be affected by the host gut microbiota. However, the relationship between coinfection and the gut microbiota is unclear. By performing comprehensive analyses on blood/stool samples from 130 individuals in Colombia, we found that the gut microbiota may have a stronger relationship with the number of P. vivax (malaria) parasites than with the number of helminth parasites infecting a host. Microbiota analysis identified more predictors of the P. vivax parasite burden, whereas analysis of blood samples identified predictors of the helminth parasite burden. These results were unexpected, because we expected each parasite to be associated with greater differences in its biological niche (blood for P. vivax and the intestine for helminths). Instead, we find that bacterial taxa were the strongest predictors of P. vivax parasitemia levels, while circulating TGF-β levels were the strongest predictor of helminth parasite burdens.Alice V. EastonMayra Raciny-AlemanVictor LiuErica RuanChristian MarierAdriana HeguyMaria Fernanda YasnotAna RodriguezP’ng LokeAmerican Society for MicrobiologyarticleColombiaPlasmodium vivaxSTHsoil-transmitted helminthsTrichuris trichiuramalariaMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Colombia Plasmodium vivax STH soil-transmitted helminths Trichuris trichiura malaria Microbiology QR1-502
spellingShingle	Colombia Plasmodium vivax STH soil-transmitted helminths Trichuris trichiura malaria Microbiology QR1-502 Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
description	ABSTRACT The role of the gut microbiota during coinfection with soil-transmitted helminths (STH) and Plasmodium spp. is poorly understood. We examined peripheral blood and fecal samples from 130 individuals who were either infected with Plasmodium vivax only, coinfected with P. vivax and STH, infected with STH alone, or not infected with either P. vivax or STH. In addition to a complete blood count (CBC) with differential, transcriptional profiling of peripheral blood samples was performed by transcriptome sequencing (RNA-Seq), fecal microbial communities were determined by 16S rRNA gene sequencing, and circulating cytokine levels were measured by bead-based immunoassays. Differences in blood cell counts, including an increased percentage of neutrophils, associated with a transcriptional signature of neutrophil activation, were driven primarily by P. vivax infection. P. vivax infection was also associated with increased levels of interleukin 6 (IL-6), IL-8, and IL-10; these cytokine levels were not affected by STH coinfection. Surprisingly, P. vivax infection was more strongly associated with differences in the microbiota than STH infection. Children infected with only P. vivax exhibited elevated Bacteroides and reduced Prevotella and Clostridiaceae levels, but these differences were not observed in individuals coinfected with STH. We also observed that P. vivax parasitemia was higher in the STH-infected population. When we used machine learning to identify the most important predictors of the P. vivax parasite burden (among P. vivax-infected individuals), bacterial taxa were the strongest predictors of parasitemia. In contrast, circulating transforming growth factor β (TGF-β) was the strongest predictor of the Trichuris trichiura egg burden. This study provides unexpected evidence that the gut microbiota may have a stronger link with P. vivax than with STH infection. IMPORTANCE Plasmodium (malaria) and helminth parasite coinfections are frequent, and both infections can be affected by the host gut microbiota. However, the relationship between coinfection and the gut microbiota is unclear. By performing comprehensive analyses on blood/stool samples from 130 individuals in Colombia, we found that the gut microbiota may have a stronger relationship with the number of P. vivax (malaria) parasites than with the number of helminth parasites infecting a host. Microbiota analysis identified more predictors of the P. vivax parasite burden, whereas analysis of blood samples identified predictors of the helminth parasite burden. These results were unexpected, because we expected each parasite to be associated with greater differences in its biological niche (blood for P. vivax and the intestine for helminths). Instead, we find that bacterial taxa were the strongest predictors of P. vivax parasitemia levels, while circulating TGF-β levels were the strongest predictor of helminth parasite burdens.
format	article
author	Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke
author_facet	Alice V. Easton Mayra Raciny-Aleman Victor Liu Erica Ruan Christian Marier Adriana Heguy Maria Fernanda Yasnot Ana Rodriguez P’ng Loke
author_sort	Alice V. Easton
title	Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
title_short	Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
title_full	Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
title_fullStr	Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
title_full_unstemmed	Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths
title_sort	immune response and microbiota profiles during coinfection with <named-content content-type="genus-species">plasmodium vivax</named-content> and soil-transmitted helminths
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/ea1ee9d4557e4aadbe57d74532554d83
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Immune Response and Microbiota Profiles during Coinfection with <named-content content-type="genus-species">Plasmodium vivax</named-content> and Soil-Transmitted Helminths

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