Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians
Abstract 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 quant...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-05-01
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| Series: | Genome Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s13059-020-02020-4 |
| _version_ | 1829141669440651264 |
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| author | Meagan A. Rubel Arwa Abbas Louis J. Taylor Andrew Connell Ceylan Tanes Kyle Bittinger Valantine N. Ndze Julius Y. Fonsah Eric Ngwang André Essiane Charles Fokunang Alfred K. Njamnshi Frederic D. Bushman Sarah A. Tishkoff |
| author_facet | Meagan A. Rubel Arwa Abbas Louis J. Taylor Andrew Connell Ceylan Tanes Kyle Bittinger Valantine N. Ndze Julius Y. Fonsah Eric Ngwang André Essiane Charles Fokunang Alfred K. Njamnshi Frederic D. Bushman Sarah A. Tishkoff |
| author_sort | Meagan A. Rubel |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-14T20:18:19Z |
| format | Article |
| id | doaj.art-822abe7d9c97481fb69cfafe5ca79625 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-14T20:18:19Z |
| publishDate | 2020-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-822abe7d9c97481fb69cfafe5ca796252022-12-21T22:48:48ZengBMCGenome Biology1474-760X2020-05-0121113210.1186/s13059-020-02020-4Lifestyle and the presence of helminths is associated with gut microbiome composition in CamerooniansMeagan A. Rubel0Arwa Abbas1Louis J. Taylor2Andrew Connell3Ceylan Tanes4Kyle Bittinger5Valantine N. Ndze6Julius Y. Fonsah7Eric Ngwang8André Essiane9Charles Fokunang10Alfred K. Njamnshi11Frederic D. Bushman12Sarah A. Tishkoff13Department of Anthropology, University of PennsylvaniaDepartment of Microbiology, Perelman School of Medicine, University of PennsylvaniaDepartment of Microbiology, Perelman School of Medicine, University of PennsylvaniaDepartment of Microbiology, Perelman School of Medicine, University of PennsylvaniaDivision of Gastroenterology, Hepatology, and Nutrition, The Children’s Hospital of PhiladelphiaDivision of Gastroenterology, Hepatology, and Nutrition, The Children’s Hospital of PhiladelphiaJohns Hopkins Cameroon ProgramDepartment of Neurology, Faculty of Medicine and Biomedical Sciences, Yaoundé Central HospitalDepartment of Anthropology, Faculty of Arts, Letters and Social Sciences, University of Yaoundé IMbalmayo District HospitalDepartment of Pharmacotoxicology and Pharmacokinetics, Faculty of Medicine and Biomedical Sciences, University of Yaoundé IDepartment of Neurology, Central Hospital YaoundéDepartment of Microbiology, Perelman School of Medicine, University of PennsylvaniaDepartment of Genetics, Perelman School of Medicine, University of PennsylvaniaAbstract 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.http://link.springer.com/article/10.1186/s13059-020-02020-4Gut microbiomeHunter-gatherersParasitesHelminthsIndustrializationHIV |
| spellingShingle | Meagan A. Rubel Arwa Abbas Louis J. Taylor Andrew Connell Ceylan Tanes Kyle Bittinger Valantine N. Ndze Julius Y. Fonsah Eric Ngwang André Essiane Charles Fokunang Alfred K. Njamnshi Frederic D. Bushman Sarah A. Tishkoff Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians Genome Biology Gut microbiome Hunter-gatherers Parasites Helminths Industrialization HIV |
| 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 | Gut microbiome Hunter-gatherers Parasites Helminths Industrialization HIV |
| url | http://link.springer.com/article/10.1186/s13059-020-02020-4 |
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