Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia
Abstract 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 identi...
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doaj-966fe11c1ea64f83b7363d58e28c3af52020-11-25T01:09:46ZengBMCMicrobiome2049-26182018-02-016111910.1186/s40168-018-0416-5Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and LiberiaBruce A. Rosa0Taniawati Supali1Lincoln Gankpala2Yenny Djuardi3Erliyani Sartono4Yanjiao Zhou5Kerstin Fischer6John Martin7Rahul Tyagi8Fatorma K. Bolay9Peter U. Fischer10Maria Yazdanbakhsh11Makedonka Mitreva12McDonnell Genome Institute, Washington UniversityDepartment of Parasitology, Faculty of Medicine, Universitas IndonesiaPublic Health and Medical Research, National Public Health Institute of LiberiaDepartment of Parasitology, Faculty of Medicine, Universitas IndonesiaDepartment of Parasitology, Leiden University Medical CenterMicrobial Genomics, The Jackson Laboratory for Genomic MedicineDepartment of Medicine, Washington University School of MedicineMcDonnell Genome Institute, Washington UniversityMcDonnell Genome Institute, Washington UniversityPublic Health and Medical Research, National Public Health Institute of LiberiaDepartment of Medicine, Washington University School of MedicineDepartment of Parasitology, Leiden University Medical CenterMcDonnell Genome Institute, Washington UniversityAbstract 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.http://link.springer.com/article/10.1186/s40168-018-0416-5HelminthNematodeMicrobiotaMetagenomeParasiteIntestine |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Bruce A. Rosa Taniawati Supali Lincoln Gankpala Yenny Djuardi Erliyani Sartono Yanjiao Zhou Kerstin Fischer John Martin Rahul Tyagi Fatorma K. Bolay Peter U. Fischer Maria Yazdanbakhsh Makedonka Mitreva |
spellingShingle |
Bruce A. Rosa Taniawati Supali Lincoln Gankpala Yenny Djuardi Erliyani Sartono Yanjiao Zhou Kerstin Fischer John Martin Rahul Tyagi Fatorma K. Bolay Peter U. Fischer Maria Yazdanbakhsh Makedonka Mitreva Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia Microbiome Helminth Nematode Microbiota Metagenome Parasite Intestine |
author_facet |
Bruce A. Rosa Taniawati Supali Lincoln Gankpala Yenny Djuardi Erliyani Sartono Yanjiao Zhou Kerstin Fischer John Martin Rahul Tyagi Fatorma K. Bolay Peter U. Fischer Maria Yazdanbakhsh Makedonka Mitreva |
author_sort |
Bruce A. Rosa |
title |
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_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_sort |
differential human gut microbiome assemblages during soil-transmitted helminth infections in indonesia and liberia |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2018-02-01 |
description |
Abstract 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. |
topic |
Helminth Nematode Microbiota Metagenome Parasite Intestine |
url |
http://link.springer.com/article/10.1186/s40168-018-0416-5 |
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