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...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: BMC 2018-02-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-018-0416-5
id doaj-966fe11c1ea64f83b7363d58e28c3af5
record_format Article
spelling 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
work_keys_str_mv AT brucearosa differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT taniawatisupali differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT lincolngankpala differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT yennydjuardi differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT erliyanisartono differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT yanjiaozhou differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT kerstinfischer differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT johnmartin differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT rahultyagi differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT fatormakbolay differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT peterufischer differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT mariayazdanbakhsh differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
AT makedonkamitreva differentialhumangutmicrobiomeassemblagesduringsoiltransmittedhelminthinfectionsinindonesiaandliberia
_version_ 1725176764319137792