Relationships Between Gastrointestinal Parasite Infections and the Fecal Microbiome in Free-Ranging Western Lowland Gorillas

Vlčková, Klára; Pafčo, Barbora; Petrželková, Klára J.; Modrý, David; Todd, Angelique; Yeoman, Carl J.; Torralba, Manolito; Wilson, Brenda A.; Stumpf, Rebecca M.; White, Bryan A.; Nelson, Karen E.; Leigh, Steven R.; Gómez, Andrés

doi:10.3389/fmicb.2018.01202

Cited by 17 publications

(16 citation statements)

References 83 publications

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“…Given the known effects of low gut microbiota diversity in human health and laboratory animals, the loss of natural levels of micro-biodiversity could have wide-ranging and devastating effects on the survival of wild animal species, but the drivers and rate of loss in free-living populations is virtually unknown. Our study provides a novel addition to the rare studies 36 , 37 , 39 investigating the associations between bacterial communities and helminth presence in wild non-human primates, and, for the first time, including fungal communities in the analyses.…”

Section: Discussionmentioning

confidence: 99%

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

Barelli

Donati

Albanese

et al. 2021

Sci Rep

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The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Although most microbiota research focuses on the variation of single gut components, the crosstalk between components is still poorly characterized, especially in hosts living under natural conditions. We investigated the gut micro-biodiversity (bacteria, fungi and helminths) of 158 individuals of two wild non-human primates, the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species have contrasting diets and lifestyles, but live sympatrically in both human-impacted and pristine forests in the Udzungwa Mountains of Tanzania. Using non-invasive faecal pellets, helminths were identified using standard microscopy while bacteria and fungi were characterized by sequencing the V1–V3 variable region of the 16S rRNA gene for bacteria and the ITS1–ITS2 fragment for fungi. Our results show that both diversity and composition of bacteria and fungi are associated with variation in helminth presence. Although interactions differed by habitat type, in both primates we found that Strongyloides was negatively associated and Trichuris was positively associated with bacterial and fungal richness. To our knowledge, this is one of the few studies demonstrating an interaction between helminth and gut microbiota communities in wild non-human primates.

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Section: Discussionmentioning

confidence: 99%

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

Barelli

Donati

Albanese

et al. 2021

Sci Rep

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“…For example, the presence of the protozoan Entamoeba spp. is associated with differences in the abundance of bacterial taxa that are likely involved in nutrition and metabolism (e.g., fiber degradation and fermentation) in western lowland gorillas ( Gorilla gorilla gorilla ) (Vlčková et al, 2018). In mouse lemurs ( Microcebus rufus ), the presence of intracellular parasites is related to increased bacterial diversity (Aivelo & Norberg, 2018).…”

Section: Discussionmentioning

confidence: 99%

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra)

Martínez-Mota

Righini

Mallott

et al. 2021

American J Primatol

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Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay.

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“…EPG is used to characterize C. sinensis infection ( Vlčková et al, 2018 ). Based on EPG and age, the 89 subjects in this study were assigned to one of four groups:…”

Section: Methodsmentioning

confidence: 99%

Altered Gut Microbiota Composition in Subjects Infected With Clonorchis sinensis

Jiang

Huang

et al. 2018

Front. Microbiol.

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Clonorchiasis is an infectious disease caused by helminths of Clonorchis sinensis (C. sinensis). The adult parasite mainly inhabits the bile duct and gall bladder, and results in various complications to the hepatobiliary system. The amount of bile secreted into the intestine is reduced in cases of C. sinensis infection, which may alter the pH of the gut and decrease the amount of surfactant protein D released from the gallbladder. However, the impact of parasitic infection on the human gut microbiome remains unclear. To this end, we examined the gut microbiota composition in 47 modified Kato–Katz thick smear-positive (egg-positive) volunteers and 42 healthy controls from five rural communities. Subjects were grouped into four sub-populations based on age and infection status. High-throughput 16S rRNA gene sequencing revealed significant changes in alpha diversity between EP1 and EN1. The beta diversity showed alterations between C. sinensis-infected subjects and healthy controls. In C. sinensis infected patients, we found the significant reduction of certain taxa, such as Bacteroides and anti-inflammatory Bifidobacterium (P < 0.05). Bacteroides, a predominant gut bacteria in healthy populations, was negatively correlated with the number of C. sinensis eggs per gram (EPG, r = −0.37, P adjust < 0.01 in 20–60 years old group; r = −0.64, P adjust = 0.04 in the 60+ years old group). What’s more, the reduction in the abundance of Bifidobacterium, a common probiotic, was decreased particularly in the 60 + years old group (r = −0.50, P = 0.04). The abundance of Dorea, a potentially pro-inflammatory microbe, was higher in infected subjects than in healthy individuals (P < 0.05). Variovorax was a unique bacteria that was only detected in infected subjects. These results clearly demonstrate the significant influence of C. sinensis infection on the human gut microbiota and provided new insights into the control, prevention, diagnosis, and clinical study of clonorchiasis through the human gut microbiota.

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Relationships Between Gastrointestinal Parasite Infections and the Fecal Microbiome in Free-Ranging Western Lowland Gorillas

Cited by 17 publications

References 83 publications

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra)

Altered Gut Microbiota Composition in Subjects Infected With Clonorchis sinensis

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