Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome

ABSTRACT Enteric parasitic infections are among the most prevalent infections in lower- and middle-income countries (LMICs) and have a profound impact on global public health. While the microbiome is increasingly recognized as a key determinant of gut health and human development, the impact of natu...

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Autores principales: Alexander S. F. Berry, Kaylynn Johnson, Rene Martins, Megan C. Sullivan, Camila Farias Amorim, Alexandra Putre, Aiysha Scott, Shuai Wang, Brianna Lindsay, Robert N. Baldassano, Thomas J. Nolan, Daniel P. Beiting
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:c157d7f326034b06be3611e20318d4a92021-11-15T15:30:51ZNatural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome10.1128/mSphere.00670-202379-5042https://doaj.org/article/c157d7f326034b06be3611e20318d4a92020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00670-20https://doaj.org/toc/2379-5042ABSTRACT Enteric parasitic infections are among the most prevalent infections in lower- and middle-income countries (LMICs) and have a profound impact on global public health. While the microbiome is increasingly recognized as a key determinant of gut health and human development, the impact of naturally acquired parasite infections on microbial community structure in the gut, and the extent to which parasite-induced changes in the microbiome may contribute to gastrointestinal symptoms, is poorly understood. Enteric parasites are routinely identified in companion animals in the United States, presenting a unique opportunity to leverage this animal model to investigate the impact of naturally acquired parasite infections on the microbiome. Clinical, parasitological, and microbiome profiling of a cohort of 258 dogs revealed a significant correlation between parasite infection and composition of the bacterial community in the gut. Relative to other enteric parasites, Giardia was associated with a more pronounced perturbation of the microbiome. To compare our findings to large-scale epidemiological studies of enteric diseases in humans, a database mining approach was employed to integrate clinical and microbiome data. Substantial and consistent alterations to microbiome structure were observed in Giardia-infected children. Importantly, infection was associated with a reduction in the relative abundance of potential pathobionts, including Gammaproteobacteria, and an increase in Prevotella—a profile often associated with gut health. Taken together, these data show that widespread Giardia infection in young animals and humans is associated with significant remodeling of the gut microbiome and provide a possible explanation for the high prevalence of asymptomatic Giardia infections observed across host species. IMPORTANCE While enteric parasitic infections are among the most important infections in lower- and middle-income countries, their impact on gut microbiota is poorly understood. We reasoned that clinical symptoms associated with these infections may be influenced by alterations of the microbiome that occur during infection. To explore this notion, we took a two-pronged approach. First, we studied a cohort of dogs naturally infected with various enteric parasites and found a strong association between parasite infection and altered gut microbiota composition. Giardia, one of the most prevalent parasite infections globally, had a particularly large impact on the microbiome. Second, we took a database-driven strategy to integrate microbiome data with clinical data from large human field studies and found that Giardia infection is also associated with marked alteration of the gut microbiome of children, suggesting a possible explanation for why Giardia has been reported to be associated with protection from moderate to severe diarrhea.Alexander S. F. BerryKaylynn JohnsonRene MartinsMegan C. SullivanCamila Farias AmorimAlexandra PutreAiysha ScottShuai WangBrianna LindsayRobert N. BaldassanoThomas J. NolanDaniel P. BeitingAmerican Society for MicrobiologyarticleGEMSGiardiaMAL-EDdatabasediarrheamicrobiomeMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic GEMS
Giardia
MAL-ED
database
diarrhea
microbiome
Microbiology
QR1-502
spellingShingle GEMS
Giardia
MAL-ED
database
diarrhea
microbiome
Microbiology
QR1-502
Alexander S. F. Berry
Kaylynn Johnson
Rene Martins
Megan C. Sullivan
Camila Farias Amorim
Alexandra Putre
Aiysha Scott
Shuai Wang
Brianna Lindsay
Robert N. Baldassano
Thomas J. Nolan
Daniel P. Beiting
Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
description ABSTRACT Enteric parasitic infections are among the most prevalent infections in lower- and middle-income countries (LMICs) and have a profound impact on global public health. While the microbiome is increasingly recognized as a key determinant of gut health and human development, the impact of naturally acquired parasite infections on microbial community structure in the gut, and the extent to which parasite-induced changes in the microbiome may contribute to gastrointestinal symptoms, is poorly understood. Enteric parasites are routinely identified in companion animals in the United States, presenting a unique opportunity to leverage this animal model to investigate the impact of naturally acquired parasite infections on the microbiome. Clinical, parasitological, and microbiome profiling of a cohort of 258 dogs revealed a significant correlation between parasite infection and composition of the bacterial community in the gut. Relative to other enteric parasites, Giardia was associated with a more pronounced perturbation of the microbiome. To compare our findings to large-scale epidemiological studies of enteric diseases in humans, a database mining approach was employed to integrate clinical and microbiome data. Substantial and consistent alterations to microbiome structure were observed in Giardia-infected children. Importantly, infection was associated with a reduction in the relative abundance of potential pathobionts, including Gammaproteobacteria, and an increase in Prevotella—a profile often associated with gut health. Taken together, these data show that widespread Giardia infection in young animals and humans is associated with significant remodeling of the gut microbiome and provide a possible explanation for the high prevalence of asymptomatic Giardia infections observed across host species. IMPORTANCE While enteric parasitic infections are among the most important infections in lower- and middle-income countries, their impact on gut microbiota is poorly understood. We reasoned that clinical symptoms associated with these infections may be influenced by alterations of the microbiome that occur during infection. To explore this notion, we took a two-pronged approach. First, we studied a cohort of dogs naturally infected with various enteric parasites and found a strong association between parasite infection and altered gut microbiota composition. Giardia, one of the most prevalent parasite infections globally, had a particularly large impact on the microbiome. Second, we took a database-driven strategy to integrate microbiome data with clinical data from large human field studies and found that Giardia infection is also associated with marked alteration of the gut microbiome of children, suggesting a possible explanation for why Giardia has been reported to be associated with protection from moderate to severe diarrhea.
format article
author Alexander S. F. Berry
Kaylynn Johnson
Rene Martins
Megan C. Sullivan
Camila Farias Amorim
Alexandra Putre
Aiysha Scott
Shuai Wang
Brianna Lindsay
Robert N. Baldassano
Thomas J. Nolan
Daniel P. Beiting
author_facet Alexander S. F. Berry
Kaylynn Johnson
Rene Martins
Megan C. Sullivan
Camila Farias Amorim
Alexandra Putre
Aiysha Scott
Shuai Wang
Brianna Lindsay
Robert N. Baldassano
Thomas J. Nolan
Daniel P. Beiting
author_sort Alexander S. F. Berry
title Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
title_short Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
title_full Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
title_fullStr Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
title_full_unstemmed Natural Infection with <italic toggle="yes">Giardia</italic> Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome
title_sort natural infection with <italic toggle="yes">giardia</italic> is associated with altered community structure of the human and canine gut microbiome
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/c157d7f326034b06be3611e20318d4a9
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