Contents lists available at ScienceDirect
Infection, Genetics and Evolution
journal homepage: www.elsevier.com/locate/meegid
Research Paper
Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut
microbiomes of wild chimpanzees in Senegal
Justinn Renelies-Hamilton
a,b,
⁎
, Marc Noguera-Julian
c,d
, Mariona Parera
c
, Roger Paredes
c,d
,
Liliana Pacheco
b
, Elena Dacal
e
, José M. Saugar
e
, José M. Rubio
e
, Michael Poulsen
a
,
Pamela C. Köster
e
, David Carmena
e
a
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark
b
Jane Goodall Institute Spain, Station Biologique Fouta Djallon, Dindéfélo, Kédougou, Senegal
c
IrsiCaixa AIDS Research Institute-HIVACAT, Hospital Germans Trias i Pujol, Badalona, Spain
d
Chair in AIDS and Related Illnesses, Centre for Health and Social Care Research (CESS), Faculty of Medicine, University of Vic – Central University of Catalonia (UVic –
UCC), Vic, Spain
e
Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, Health Institute Carlos III, Majadahonda, Spain
ARTICLE INFO
Keywords:
Ape
Faecalibacterium
Microbiota
Methanobrevibacter
Pan troglodytes
Parasite
ABSTRACT
Background: Gut parasites exert an important infuence 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 infammation) 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 diferences in gut microbiota ecosystem traits and taxonomical
composition between Blastocystis and Strongyloides bearing and non-bearing samples.
Results: For Blastocystis, twelve diferentially abundant taxa (e.g., Methanobrevibacter), including Prevotella and
Ruminococcus-Methanobrevibacter enterotype markers, replicate fndings 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 fve other taxonomic groups. Each parasite had its unique impact on the gut microbiota indicating parasite-
specifc niches. Our results suggest that studying the gut microbiomes of wild chimpanzees could help disen-
tangle biological from artefactual associations between gut microbiomes and parasites.
1. Introduction
Ecosystems contain multitudes of interacting species. The great ape
gut microbiome (GM), home to trillions of prokaryote and eukaryote
cells, is no exception. Research into microbiomes is starting to reveal
the complex interactions amongst diferent members of the GM and
their interplay with hosts: intestinal eukaryotes are associated to
particular GM communities (e.g., reviewed in Leung et al., 2018).
Blastocystis and Strongyloides, traditionally deemed parasites (Brumpt,
1912; Campbell, 1893), have been described recently, by some, as
benefcial members of the GM due to their correlation with certain
microbial markers such as α diversity (e.g., reviewed by Stensvold and
Van Der Giezen, 2018 and Zaiss and Harris, 2016). GM markers are
assumed to refect the ecological states of the microbial ecosystem: for
https://doi.org/10.1016/j.meegid.2019.104010
Received 11 March 2019; Received in revised form 2 July 2019; Accepted 18 August 2019
⁎
Corresponding author at: Universitetsparken 15, Building 3, 1st Floor, Section for Ecology and Evolution, Department of Biology, University of Copenhagen,
Copenhagen, Denmark.
E-mail address: claxon71@gmail.com (J. Renelies-Hamilton).
Infection, Genetics and Evolution 74 (2019) 104010
Available online 20 August 2019
1567-1348/ © 2019 Elsevier B.V. All rights reserved.
T