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Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians

BACKGROUND: African populations provide a unique opportunity to interrogate host-microbe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity. We integrate gut microbiome 16S rRNA amplicon and shotgun metagenomic sequence data with quantificatio...

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Autores principales: Rubel, Meagan A., Abbas, Arwa, Taylor, Louis J., Connell, Andrew, Tanes, Ceylan, Bittinger, Kyle, Ndze, Valantine N., Fonsah, Julius Y., Ngwang, Eric, Essiane, André, Fokunang, Charles, Njamnshi, Alfred K., Bushman, Frederic D., Tishkoff, Sarah A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7249393/
https://www.ncbi.nlm.nih.gov/pubmed/32450885
http://dx.doi.org/10.1186/s13059-020-02020-4
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author Rubel, Meagan A.
Abbas, Arwa
Taylor, Louis J.
Connell, Andrew
Tanes, Ceylan
Bittinger, Kyle
Ndze, Valantine N.
Fonsah, Julius Y.
Ngwang, Eric
Essiane, André
Fokunang, Charles
Njamnshi, Alfred K.
Bushman, Frederic D.
Tishkoff, Sarah A.
author_facet Rubel, Meagan A.
Abbas, Arwa
Taylor, Louis J.
Connell, Andrew
Tanes, Ceylan
Bittinger, Kyle
Ndze, Valantine N.
Fonsah, Julius Y.
Ngwang, Eric
Essiane, André
Fokunang, Charles
Njamnshi, Alfred K.
Bushman, Frederic D.
Tishkoff, Sarah A.
author_sort Rubel, Meagan A.
collection PubMed
description BACKGROUND: African populations provide a unique opportunity to interrogate host-microbe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity. We integrate gut microbiome 16S rRNA amplicon and shotgun metagenomic sequence data with quantification of pathogen burden and measures of immune parameters for 575 ethnically diverse Africans from Cameroon. Subjects followed pastoralist, agropastoralist, and hunter-gatherer lifestyles and were compared to an urban US population from Philadelphia. RESULTS: We observe significant differences in gut microbiome composition across populations that correlate with subsistence strategy and country. After these, the variable most strongly associated with gut microbiome structure in Cameroonians is the presence of gut parasites. Hunter-gatherers have high frequencies of parasites relative to agropastoralists and pastoralists. Ascaris lumbricoides, Necator americanus, Trichuris trichiura, and Strongyloides stercoralis soil-transmitted helminths (“ANTS” parasites) significantly co-occur, and increased frequency of gut parasites correlates with increased gut microbial diversity. Gut microbiome composition predicts ANTS positivity with 80% accuracy. Colonization with ANTS, in turn, is associated with elevated levels of TH1, TH2, and proinflammatory cytokines, indicating an association with multiple immune mechanisms. The unprecedented size of this dataset allowed interrogation of additional questions—for example, we find that Fulani pastoralists, who consume high levels of milk, possess an enrichment of gut bacteria that catabolize galactose, an end product of lactose metabolism, and of bacteria that metabolize lipids. CONCLUSIONS: These data document associations of bacterial microbiota and eukaryotic parasites with each other and with host immune responses; each of these is further correlated with subsistence practices.
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spelling pubmed-72493932020-06-04 Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians Rubel, Meagan A. Abbas, Arwa Taylor, Louis J. Connell, Andrew Tanes, Ceylan Bittinger, Kyle Ndze, Valantine N. Fonsah, Julius Y. Ngwang, Eric Essiane, André Fokunang, Charles Njamnshi, Alfred K. Bushman, Frederic D. Tishkoff, Sarah A. Genome Biol Research BACKGROUND: African populations provide a unique opportunity to interrogate host-microbe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity. We integrate gut microbiome 16S rRNA amplicon and shotgun metagenomic sequence data with quantification of pathogen burden and measures of immune parameters for 575 ethnically diverse Africans from Cameroon. Subjects followed pastoralist, agropastoralist, and hunter-gatherer lifestyles and were compared to an urban US population from Philadelphia. RESULTS: We observe significant differences in gut microbiome composition across populations that correlate with subsistence strategy and country. After these, the variable most strongly associated with gut microbiome structure in Cameroonians is the presence of gut parasites. Hunter-gatherers have high frequencies of parasites relative to agropastoralists and pastoralists. Ascaris lumbricoides, Necator americanus, Trichuris trichiura, and Strongyloides stercoralis soil-transmitted helminths (“ANTS” parasites) significantly co-occur, and increased frequency of gut parasites correlates with increased gut microbial diversity. Gut microbiome composition predicts ANTS positivity with 80% accuracy. Colonization with ANTS, in turn, is associated with elevated levels of TH1, TH2, and proinflammatory cytokines, indicating an association with multiple immune mechanisms. The unprecedented size of this dataset allowed interrogation of additional questions—for example, we find that Fulani pastoralists, who consume high levels of milk, possess an enrichment of gut bacteria that catabolize galactose, an end product of lactose metabolism, and of bacteria that metabolize lipids. CONCLUSIONS: These data document associations of bacterial microbiota and eukaryotic parasites with each other and with host immune responses; each of these is further correlated with subsistence practices. BioMed Central 2020-05-25 /pmc/articles/PMC7249393/ /pubmed/32450885 http://dx.doi.org/10.1186/s13059-020-02020-4 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Rubel, Meagan A.
Abbas, Arwa
Taylor, Louis J.
Connell, Andrew
Tanes, Ceylan
Bittinger, Kyle
Ndze, Valantine N.
Fonsah, Julius Y.
Ngwang, Eric
Essiane, André
Fokunang, Charles
Njamnshi, Alfred K.
Bushman, Frederic D.
Tishkoff, Sarah A.
Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title_full Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title_fullStr Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title_full_unstemmed Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title_short Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
title_sort lifestyle and the presence of helminths is associated with gut microbiome composition in cameroonians
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7249393/
https://www.ncbi.nlm.nih.gov/pubmed/32450885
http://dx.doi.org/10.1186/s13059-020-02020-4
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