Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns

ABSTRACT Blastocystis is the most prevalent protist of the human intestine, colonizing approximately 20% of the North American population and up to 100% in some nonindustrialized settings. Blastocystis is associated with gastrointestinal and systemic disease but can also be an asymptomatic colonizer...

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Autores principales: M. E. Nieves-Ramírez, O. Partida-Rodríguez, I. Laforest-Lapointe, L. A. Reynolds, E. M. Brown, A. Valdez-Salazar, P. Morán-Silva, L. Rojas-Velázquez, E. Morien, L. W. Parfrey, M. Jin, J. Walter, J. Torres, M. C. Arrieta, C. Ximénez-García, B. B. Finlay
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:6b684f8d8ee3403f884603f0a2f7baf42021-12-02T18:39:15ZAsymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns10.1128/mSystems.00007-182379-5077https://doaj.org/article/6b684f8d8ee3403f884603f0a2f7baf42018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00007-18https://doaj.org/toc/2379-5077ABSTRACT Blastocystis is the most prevalent protist of the human intestine, colonizing approximately 20% of the North American population and up to 100% in some nonindustrialized settings. Blastocystis is associated with gastrointestinal and systemic disease but can also be an asymptomatic colonizer in large populations. While recent findings in humans have shown bacterial microbiota changes associated with this protist, it is unknown whether these occur due to the presence of Blastocystis or as a result of inflammation. To explore this, we evaluated the fecal bacterial and eukaryotic microbiota in 156 asymptomatic adult subjects from a rural population in Xoxocotla, Mexico. Colonization with Blastocystis was strongly associated with an increase in bacterial alpha diversity and broad changes in beta diversity and with more discrete changes to the microbial eukaryome. More than 230 operational taxonomic units (OTUs), including those of dominant species Prevotella copri and Ruminococcus bromii, were differentially abundant in Blastocystis-colonized individuals. Large functional changes accompanied these observations, with differential abundances of 202 (out of 266) predicted metabolic pathways (PICRUSt), as well as lower fecal concentrations of acetate, butyrate, and propionate in colonized individuals. Fecal calprotectin was markedly decreased in association with Blastocystis colonization, suggesting that this ecological shift induces subclinical immune consequences to the asymptomatic host. This work is the first to show a direct association between the presence of Blastocystis and shifts in the gut bacterial and eukaryotic microbiome in the absence of gastrointestinal disease or inflammation. These results prompt further investigation of the role Blastocystis and other eukaryotes play within the human microbiome. IMPORTANCE Given the results of our study and other reports of the effects of the most common human gut protist on the diversity and composition of the bacterial microbiome, Blastocystis and, possibly, other gut protists should be studied as ecosystem engineers that drive community diversity and composition.M. E. Nieves-RamírezO. Partida-RodríguezI. Laforest-LapointeL. A. ReynoldsE. M. BrownA. Valdez-SalazarP. Morán-SilvaL. Rojas-VelázquezE. MorienL. W. ParfreyM. JinJ. WalterJ. TorresM. C. ArrietaC. Ximénez-GarcíaB. B. FinlayAmerican Society for MicrobiologyarticleBlastocystisgut microbiomeeukaryomehost-microbe interactionsmicrobial ecologyMicrobiologyQR1-502ENmSystems, Vol 3, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic Blastocystis
gut microbiome
eukaryome
host-microbe interactions
microbial ecology
Microbiology
QR1-502
spellingShingle Blastocystis
gut microbiome
eukaryome
host-microbe interactions
microbial ecology
Microbiology
QR1-502
M. E. Nieves-Ramírez
O. Partida-Rodríguez
I. Laforest-Lapointe
L. A. Reynolds
E. M. Brown
A. Valdez-Salazar
P. Morán-Silva
L. Rojas-Velázquez
E. Morien
L. W. Parfrey
M. Jin
J. Walter
J. Torres
M. C. Arrieta
C. Ximénez-García
B. B. Finlay
Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
description ABSTRACT Blastocystis is the most prevalent protist of the human intestine, colonizing approximately 20% of the North American population and up to 100% in some nonindustrialized settings. Blastocystis is associated with gastrointestinal and systemic disease but can also be an asymptomatic colonizer in large populations. While recent findings in humans have shown bacterial microbiota changes associated with this protist, it is unknown whether these occur due to the presence of Blastocystis or as a result of inflammation. To explore this, we evaluated the fecal bacterial and eukaryotic microbiota in 156 asymptomatic adult subjects from a rural population in Xoxocotla, Mexico. Colonization with Blastocystis was strongly associated with an increase in bacterial alpha diversity and broad changes in beta diversity and with more discrete changes to the microbial eukaryome. More than 230 operational taxonomic units (OTUs), including those of dominant species Prevotella copri and Ruminococcus bromii, were differentially abundant in Blastocystis-colonized individuals. Large functional changes accompanied these observations, with differential abundances of 202 (out of 266) predicted metabolic pathways (PICRUSt), as well as lower fecal concentrations of acetate, butyrate, and propionate in colonized individuals. Fecal calprotectin was markedly decreased in association with Blastocystis colonization, suggesting that this ecological shift induces subclinical immune consequences to the asymptomatic host. This work is the first to show a direct association between the presence of Blastocystis and shifts in the gut bacterial and eukaryotic microbiome in the absence of gastrointestinal disease or inflammation. These results prompt further investigation of the role Blastocystis and other eukaryotes play within the human microbiome. IMPORTANCE Given the results of our study and other reports of the effects of the most common human gut protist on the diversity and composition of the bacterial microbiome, Blastocystis and, possibly, other gut protists should be studied as ecosystem engineers that drive community diversity and composition.
format article
author M. E. Nieves-Ramírez
O. Partida-Rodríguez
I. Laforest-Lapointe
L. A. Reynolds
E. M. Brown
A. Valdez-Salazar
P. Morán-Silva
L. Rojas-Velázquez
E. Morien
L. W. Parfrey
M. Jin
J. Walter
J. Torres
M. C. Arrieta
C. Ximénez-García
B. B. Finlay
author_facet M. E. Nieves-Ramírez
O. Partida-Rodríguez
I. Laforest-Lapointe
L. A. Reynolds
E. M. Brown
A. Valdez-Salazar
P. Morán-Silva
L. Rojas-Velázquez
E. Morien
L. W. Parfrey
M. Jin
J. Walter
J. Torres
M. C. Arrieta
C. Ximénez-García
B. B. Finlay
author_sort M. E. Nieves-Ramírez
title Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
title_short Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
title_full Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
title_fullStr Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
title_full_unstemmed Asymptomatic Intestinal Colonization with Protist <italic toggle="yes">Blastocystis</italic> Is Strongly Associated with Distinct Microbiome Ecological Patterns
title_sort asymptomatic intestinal colonization with protist <italic toggle="yes">blastocystis</italic> is strongly associated with distinct microbiome ecological patterns
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/6b684f8d8ee3403f884603f0a2f7baf4
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