Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal

Justinn Renelies-Hamilton; Marc Noguera-Julian; Mariona Parera; Roger Paredes; Liliana Pacheco; Elena Dacal; José M. Saugar; José M. Rubio; Michael Poulsen; Pamela C. Köster; David Carmena

doi:10.1016/j.meegid.2019.104010

Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal

Justinn Renelies-Hamilton^*, Marc Noguera-Julian, Mariona Parera, Roger Paredes, Liliana Pacheco, Elena Dacal, José M. Saugar, José M. Rubio, Michael Poulsen, Pamela C. Köster, David Carmena

^*Corresponding author for this work

6 Citations (Scopus)

Abstract

Background: Gut parasites exert an important influence on the gut microbiome, with many studies focusing on the human gut microbiome. It has, however, undergone severe richness depletion. Hygienic lifestyle, antimicrobial treatments and altered gut homeostasis (e.g., chronic inflammation) reduce gut microbiome richness and also parasite prevalence; which may confound results. Studying species closely related to humans could help overcome this problem by providing insights into the ancestral relationship between humans, their gut microbiome and their gut parasites. Chimpanzees are a particularly promising model as they have similar gut microbiomes to humans and many parasites infect both species. Aims: We study the interaction between gut microbiome and enteric parasites in chimpanzees. Investigating what novel insights a closely related species can reveal when compared to studies on humans. Methods: Using eighty-seven faecal samples from wild western chimpanzees (Pan troglodytes verus) in Senegal, we combine 16S rRNA gene amplicon sequencing for gut microbiome characterization with PCR detection of parasite taxa (Blastocystis sp., Strongyloides spp., Giardia duodenalis, Cryptosporidium spp., Plasmodium spp., Filariae and Trypanosomatidae). We test for differences in gut microbiota ecosystem traits and taxonomical composition between Blastocystis and Strongyloides bearing and non-bearing samples. Results: For Blastocystis, twelve differentially abundant taxa (e.g., Methanobrevibacter), including Prevotella and Ruminococcus-Methanobrevibacter enterotype markers, replicate findings in humans. However, several richness indices are lower in Blastocystis carriers, contradicting human studies. This indicates Blastocystis, unlike Strongyloides, is associated to a “poor health” gut microbiome, as does the fact that Faecalibacterium, a bacterium with gut protective traits, is absent in Blastocystis-positive samples. Strongyloides was associated to Alloprevotella and five other taxonomic groups. Each parasite had its unique impact on the gut microbiota indicating parasite-specific niches. Our results suggest that studying the gut microbiomes of wild chimpanzees could help disentangle biological from artefactual associations between gut microbiomes and parasites.

Original language	English
Article number	104010
Journal	Infection, Genetics and Evolution
Volume	74
Number of pages	9
ISSN	1567-1348
DOIs	https://doi.org/10.1016/j.meegid.2019.104010
Publication status	Published - 2019

Keywords

Ape
Faecalibacterium
Methanobrevibacter
Microbiota
Pan troglodytes
Parasite

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.meegid.2019.104010

Cite this

Renelies-Hamilton, J., Noguera-Julian, M., Parera, M., Paredes, R., Pacheco, L., Dacal, E., Saugar, J. M., Rubio, J. M., Poulsen, M., Köster, P. C., & Carmena, D. (2019). Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal. Infection, Genetics and Evolution, 74, Article 104010. https://doi.org/10.1016/j.meegid.2019.104010

Renelies-Hamilton, J, Noguera-Julian, M, Parera, M, Paredes, R, Pacheco, L, Dacal, E, Saugar, JM, Rubio, JM, Poulsen, M, Köster, PC & Carmena, D 2019, 'Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal', Infection, Genetics and Evolution, vol. 74, 104010. https://doi.org/10.1016/j.meegid.2019.104010

@article{5407d787507e4dbebdd1ae2b43c2c3df,

title = "Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal",

abstract = "Background: Gut parasites exert an important influence on the gut microbiome, with many studies focusing on the human gut microbiome. It has, however, undergone severe richness depletion. Hygienic lifestyle, antimicrobial treatments and altered gut homeostasis (e.g., chronic inflammation) reduce gut microbiome richness and also parasite prevalence; which may confound results. Studying species closely related to humans could help overcome this problem by providing insights into the ancestral relationship between humans, their gut microbiome and their gut parasites. Chimpanzees are a particularly promising model as they have similar gut microbiomes to humans and many parasites infect both species. Aims: We study the interaction between gut microbiome and enteric parasites in chimpanzees. Investigating what novel insights a closely related species can reveal when compared to studies on humans. Methods: Using eighty-seven faecal samples from wild western chimpanzees (Pan troglodytes verus) in Senegal, we combine 16S rRNA gene amplicon sequencing for gut microbiome characterization with PCR detection of parasite taxa (Blastocystis sp., Strongyloides spp., Giardia duodenalis, Cryptosporidium spp., Plasmodium spp., Filariae and Trypanosomatidae). We test for differences in gut microbiota ecosystem traits and taxonomical composition between Blastocystis and Strongyloides bearing and non-bearing samples. Results: For Blastocystis, twelve differentially abundant taxa (e.g., Methanobrevibacter), including Prevotella and Ruminococcus-Methanobrevibacter enterotype markers, replicate findings in humans. However, several richness indices are lower in Blastocystis carriers, contradicting human studies. This indicates Blastocystis, unlike Strongyloides, is associated to a “poor health” gut microbiome, as does the fact that Faecalibacterium, a bacterium with gut protective traits, is absent in Blastocystis-positive samples. Strongyloides was associated to Alloprevotella and five other taxonomic groups. Each parasite had its unique impact on the gut microbiota indicating parasite-specific niches. Our results suggest that studying the gut microbiomes of wild chimpanzees could help disentangle biological from artefactual associations between gut microbiomes and parasites.",

keywords = "Ape, Faecalibacterium, Methanobrevibacter, Microbiota, Pan troglodytes, Parasite",

author = "Justinn Renelies-Hamilton and Marc Noguera-Julian and Mariona Parera and Roger Paredes and Liliana Pacheco and Elena Dacal and Saugar, {Jos{\'e} M.} and Rubio, {Jos{\'e} M.} and Michael Poulsen and K{\"o}ster, {Pamela C.} and David Carmena",

year = "2019",

doi = "10.1016/j.meegid.2019.104010",

language = "English",

volume = "74",

journal = "Infection, Genetics and Evolution",

issn = "1567-1348",

publisher = "Elsevier",

}

TY - JOUR

T1 - Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal

AU - Renelies-Hamilton, Justinn

AU - Noguera-Julian, Marc

AU - Parera, Mariona

AU - Paredes, Roger

AU - Pacheco, Liliana

AU - Dacal, Elena

AU - Saugar, José M.

AU - Rubio, José M.

AU - Poulsen, Michael

AU - Köster, Pamela C.

AU - Carmena, David

PY - 2019

Y1 - 2019

N2 - Background: Gut parasites exert an important influence on the gut microbiome, with many studies focusing on the human gut microbiome. It has, however, undergone severe richness depletion. Hygienic lifestyle, antimicrobial treatments and altered gut homeostasis (e.g., chronic inflammation) reduce gut microbiome richness and also parasite prevalence; which may confound results. Studying species closely related to humans could help overcome this problem by providing insights into the ancestral relationship between humans, their gut microbiome and their gut parasites. Chimpanzees are a particularly promising model as they have similar gut microbiomes to humans and many parasites infect both species. Aims: We study the interaction between gut microbiome and enteric parasites in chimpanzees. Investigating what novel insights a closely related species can reveal when compared to studies on humans. Methods: Using eighty-seven faecal samples from wild western chimpanzees (Pan troglodytes verus) in Senegal, we combine 16S rRNA gene amplicon sequencing for gut microbiome characterization with PCR detection of parasite taxa (Blastocystis sp., Strongyloides spp., Giardia duodenalis, Cryptosporidium spp., Plasmodium spp., Filariae and Trypanosomatidae). We test for differences in gut microbiota ecosystem traits and taxonomical composition between Blastocystis and Strongyloides bearing and non-bearing samples. Results: For Blastocystis, twelve differentially abundant taxa (e.g., Methanobrevibacter), including Prevotella and Ruminococcus-Methanobrevibacter enterotype markers, replicate findings in humans. However, several richness indices are lower in Blastocystis carriers, contradicting human studies. This indicates Blastocystis, unlike Strongyloides, is associated to a “poor health” gut microbiome, as does the fact that Faecalibacterium, a bacterium with gut protective traits, is absent in Blastocystis-positive samples. Strongyloides was associated to Alloprevotella and five other taxonomic groups. Each parasite had its unique impact on the gut microbiota indicating parasite-specific niches. Our results suggest that studying the gut microbiomes of wild chimpanzees could help disentangle biological from artefactual associations between gut microbiomes and parasites.

AB - Background: Gut parasites exert an important influence on the gut microbiome, with many studies focusing on the human gut microbiome. It has, however, undergone severe richness depletion. Hygienic lifestyle, antimicrobial treatments and altered gut homeostasis (e.g., chronic inflammation) reduce gut microbiome richness and also parasite prevalence; which may confound results. Studying species closely related to humans could help overcome this problem by providing insights into the ancestral relationship between humans, their gut microbiome and their gut parasites. Chimpanzees are a particularly promising model as they have similar gut microbiomes to humans and many parasites infect both species. Aims: We study the interaction between gut microbiome and enteric parasites in chimpanzees. Investigating what novel insights a closely related species can reveal when compared to studies on humans. Methods: Using eighty-seven faecal samples from wild western chimpanzees (Pan troglodytes verus) in Senegal, we combine 16S rRNA gene amplicon sequencing for gut microbiome characterization with PCR detection of parasite taxa (Blastocystis sp., Strongyloides spp., Giardia duodenalis, Cryptosporidium spp., Plasmodium spp., Filariae and Trypanosomatidae). We test for differences in gut microbiota ecosystem traits and taxonomical composition between Blastocystis and Strongyloides bearing and non-bearing samples. Results: For Blastocystis, twelve differentially abundant taxa (e.g., Methanobrevibacter), including Prevotella and Ruminococcus-Methanobrevibacter enterotype markers, replicate findings in humans. However, several richness indices are lower in Blastocystis carriers, contradicting human studies. This indicates Blastocystis, unlike Strongyloides, is associated to a “poor health” gut microbiome, as does the fact that Faecalibacterium, a bacterium with gut protective traits, is absent in Blastocystis-positive samples. Strongyloides was associated to Alloprevotella and five other taxonomic groups. Each parasite had its unique impact on the gut microbiota indicating parasite-specific niches. Our results suggest that studying the gut microbiomes of wild chimpanzees could help disentangle biological from artefactual associations between gut microbiomes and parasites.

KW - Ape

KW - Faecalibacterium

KW - Methanobrevibacter

KW - Microbiota

KW - Pan troglodytes

KW - Parasite

U2 - 10.1016/j.meegid.2019.104010

DO - 10.1016/j.meegid.2019.104010

M3 - Journal article

C2 - 31442596

AN - SCOPUS:85071260153

SN - 1567-1348

VL - 74

JO - Infection, Genetics and Evolution

JF - Infection, Genetics and Evolution

M1 - 104010

ER -

Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal

Abstract

Keywords

UN SDGs

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