Gastrointestinal symbiont diversity in wild gorilla: A comparison of bacterial and strongylid communities across multiple localities

Abstract

Western lowland gorillas (Gorilla gorilla gorilla) are Critically Endangered and show continued population decline. Consequently, pressure is mounting to better understand their conservation threats and ecology. Gastrointestinal symbionts, such as bacterial and eukaryotic communities, are believed to play vital roles in the physiological landscape of the host. Gorillas host a broad spectrum of eucaryotes, so called parasites, with strongylid nematodes being particularly prevalent. While these communities are partially consistent, they are also shaped by various ecological factors, such as diet or habitat type. To investigate gastrointestinal symbionts of wild western lowland gorillas, we analysed 215 faecal samples from individuals in five distinct localities across the Congo Basin, using high‐throughput sequencing techniques. We describe the gut bacterial microbiome and genetic diversity of strongylid communities, including strain‐level identification of amplicon sequence variants (ASVs). We identified strongylid ASVs from eight genera and bacterial ASVs from 20 phyla. We compared these communities across localities, with reference to varying environmental factors among populations, finding differences in alpha diversity and community compositions of both gastrointestinal components. Moreover, we also investigated covariation between strongylid nematodes and the bacterial microbiome, finding correlations between strongylid taxa and Prevotellaceae and Rikenellaceae ASVs that were consistent across multiple localities. Our research highlights the complexity of the bacterial microbiome and strongylid communities in several gorilla populations and emphasizes potential interactions between these two symbiont communities. This study provides a framework for ongoing research into strongylid nematode diversity, and their interactions with the bacterial microbiome, among great apes.

High diversity and sharing of strongylid nematodes in humans and great apes co-habiting unprotected area in Cameroon

“…Overall, the composition of strongylid communities found in Dja remained generally consistent with previous studies, suggesting that Necator and Oesophagostomum are the most prevalent strongylid genera in African apes and humans (Cibot et al, 2015; Ghai et al, 2014; Hasegawa et al, 2017; Mason et al 2022, Pafčo et al, 2018, 2019), but unlike in previous studies, these were followed by Trichostrongylus and unassigned genera. Dja apes were mostly infected by variants of O. stephanostomum and N. gorillae , both commonly found in great apes (Cibot et al, 2015; Ghai et al, 2014; Mason et al 2022; Pafčo et al, 2019). Humans were mostly infected by N. americanus variants, confirming that N. americanus is the dominant human-specific hookworm in general (Hotez et al, 2005).…”

“…While N. americanus variants were found mostly in humans, four of them were shared with gorillas; this demonstrates that N. americanus is not a solely human-specific parasite. Moreover, such a finding was previously observed in African great apes (Hasegawa et al, 2014; Mason et al 2022; Pafčo et al, 2019). Necator gorillae variants were found predominantly in great apes, suggesting its probable ape origin, but it was also shared with humans.…”

“…Pafčo et al (2019) also reported O. stephanostomum infecting NHPs in DSPA, CAR, but not in humans, thus suggesting its ape origin. This is also supported by Mason et al (2022), who found O. stephanostomum in high prevalence in western lowland gorillas across several African localities. We only found the second Oesophagostomum group ( Oesophagostomum stephanostomum type II) in great apes; this group was previously described in western lowland gorillas in Moukalaba-Doudau National Park (MDNP), Gabon (Makouloutou et al, 2014) and in Dja FR, Cameroon (using the same gorilla dataset as was used for this study; Mason et al, 2022).…”

“…Additionally, we found a few variants of undetermined Necator sp. in Dja apes corresponding to variant III-1 first found in humans in DPSA, CAR by Hasegawa et al (2014), later reported in western lowland gorillas across several African localities (Hasegawa et al, 2017;Mason et al 2022). Hasegawa et al (2014) speculated that variant III-1 sequences may represent N. congolensis or N. exilidens, previously described in chimpanzees (Cummins, 1912;Gedoelst, 1916); however, the original descriptions of N. congolensis or N. exilidens were made at the beginning of the last century, and even "traditional" morphology-based taxonomy of Necator non-americanus species remain unclear (Kalousová et al, 2016).…”

“…HTS of standard phylogenetic markers amplified from complex target populations (metabarcoding) is inexpensive and allows efficient genotyping of hundreds of samples at a time, untangling mixed infections and detecting rare taxa (Valentini, Pompanon, & Taberlet, 2009; Von Bubnoff, 2008; Zhou et al, 2011). Exact delineation of operational taxonomic units (OTUs) can help understand the molecular epidemiology of pathogens and consequently HTS metagenomics has brought about a much deeper insight into the diversity of strongylid nematodes and has revealed hidden zoonotic transmissions or parasite sharing (Avramenko et al, 2017; Lott, Hose, & Power, 2015; Mason et al, 2022; Pafčo et al, 2018).…”