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Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia

BACKGROUND: The human intestine and its microbiota is the most common infection site for soil-transmitted helminths (STHs), which affect the well-being of ~ 1.5 billion people worldwide. The complex cross-kingdom interactions are not well understood. RESULTS: A cross-sectional analysis identified co...

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Autores principales: Rosa, Bruce A., Supali, Taniawati, Gankpala, Lincoln, Djuardi, Yenny, Sartono, Erliyani, Zhou, Yanjiao, Fischer, Kerstin, Martin, John, Tyagi, Rahul, Bolay, Fatorma K., Fischer, Peter U., Yazdanbakhsh, Maria, Mitreva, Makedonka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6389212/
https://www.ncbi.nlm.nih.gov/pubmed/29486796
http://dx.doi.org/10.1186/s40168-018-0416-5
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author Rosa, Bruce A.
Supali, Taniawati
Gankpala, Lincoln
Djuardi, Yenny
Sartono, Erliyani
Zhou, Yanjiao
Fischer, Kerstin
Martin, John
Tyagi, Rahul
Bolay, Fatorma K.
Fischer, Peter U.
Yazdanbakhsh, Maria
Mitreva, Makedonka
author_facet Rosa, Bruce A.
Supali, Taniawati
Gankpala, Lincoln
Djuardi, Yenny
Sartono, Erliyani
Zhou, Yanjiao
Fischer, Kerstin
Martin, John
Tyagi, Rahul
Bolay, Fatorma K.
Fischer, Peter U.
Yazdanbakhsh, Maria
Mitreva, Makedonka
author_sort Rosa, Bruce A.
collection PubMed
description BACKGROUND: The human intestine and its microbiota is the most common infection site for soil-transmitted helminths (STHs), which affect the well-being of ~ 1.5 billion people worldwide. The complex cross-kingdom interactions are not well understood. RESULTS: A cross-sectional analysis identified conserved microbial signatures positively or negatively associated with STH infections across Liberia and Indonesia, and longitudinal samples analysis from a double-blind randomized trial showed that the gut microbiota responds to deworming but does not transition closer to the uninfected state. The microbiomes of individuals able to self-clear the infection had more alike microbiome assemblages compared to individuals who remained infected. One bacterial taxon (Lachnospiracae) was negatively associated with infection in both countries, and 12 bacterial taxa were significantly associated with STH infection in both countries, including Olsenella (associated with reduced gut inflammation), which also significantly reduced in abundance following clearance of infection. Microbial community gene abundances were also affected by deworming. Functional categories identified as associated with STH infection included arachidonic acid metabolism; arachidonic acid is the precursor for pro-inflammatory leukotrienes that threaten helminth survival, and our findings suggest that some modulation of arachidonic acid activity in the STH-infected gut may occur through the increase of arachidonic acid metabolizing bacteria. CONCLUSIONS: For the first time, we identify specific members of the gut microbiome that discriminate between moderately/heavily STH-infected and non-infected states across very diverse geographical regions using two different statistical methods. We also identify microbiome-encoded biological functions associated with the STH infections, which are associated potentially with STH survival strategies, and changes in the host environment. These results provide a novel insight of the cross-kingdom interactions in the human gut ecosystem by unlocking the microbiome assemblages at taxonomic, genetic, and functional levels so that advances towards key mechanistic studies can be made. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0416-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-63892122019-03-19 Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia Rosa, Bruce A. Supali, Taniawati Gankpala, Lincoln Djuardi, Yenny Sartono, Erliyani Zhou, Yanjiao Fischer, Kerstin Martin, John Tyagi, Rahul Bolay, Fatorma K. Fischer, Peter U. Yazdanbakhsh, Maria Mitreva, Makedonka Microbiome Research BACKGROUND: The human intestine and its microbiota is the most common infection site for soil-transmitted helminths (STHs), which affect the well-being of ~ 1.5 billion people worldwide. The complex cross-kingdom interactions are not well understood. RESULTS: A cross-sectional analysis identified conserved microbial signatures positively or negatively associated with STH infections across Liberia and Indonesia, and longitudinal samples analysis from a double-blind randomized trial showed that the gut microbiota responds to deworming but does not transition closer to the uninfected state. The microbiomes of individuals able to self-clear the infection had more alike microbiome assemblages compared to individuals who remained infected. One bacterial taxon (Lachnospiracae) was negatively associated with infection in both countries, and 12 bacterial taxa were significantly associated with STH infection in both countries, including Olsenella (associated with reduced gut inflammation), which also significantly reduced in abundance following clearance of infection. Microbial community gene abundances were also affected by deworming. Functional categories identified as associated with STH infection included arachidonic acid metabolism; arachidonic acid is the precursor for pro-inflammatory leukotrienes that threaten helminth survival, and our findings suggest that some modulation of arachidonic acid activity in the STH-infected gut may occur through the increase of arachidonic acid metabolizing bacteria. CONCLUSIONS: For the first time, we identify specific members of the gut microbiome that discriminate between moderately/heavily STH-infected and non-infected states across very diverse geographical regions using two different statistical methods. We also identify microbiome-encoded biological functions associated with the STH infections, which are associated potentially with STH survival strategies, and changes in the host environment. These results provide a novel insight of the cross-kingdom interactions in the human gut ecosystem by unlocking the microbiome assemblages at taxonomic, genetic, and functional levels so that advances towards key mechanistic studies can be made. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0416-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-02-28 /pmc/articles/PMC6389212/ /pubmed/29486796 http://dx.doi.org/10.1186/s40168-018-0416-5 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research
Rosa, Bruce A.
Supali, Taniawati
Gankpala, Lincoln
Djuardi, Yenny
Sartono, Erliyani
Zhou, Yanjiao
Fischer, Kerstin
Martin, John
Tyagi, Rahul
Bolay, Fatorma K.
Fischer, Peter U.
Yazdanbakhsh, Maria
Mitreva, Makedonka
Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title_full Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title_fullStr Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title_full_unstemmed Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title_short Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
title_sort differential human gut microbiome assemblages during soil-transmitted helminth infections in indonesia and liberia
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6389212/
https://www.ncbi.nlm.nih.gov/pubmed/29486796
http://dx.doi.org/10.1186/s40168-018-0416-5
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