Alteration of the rat cecal microbiome during colonization with the helminth<i>Hymenolepis diminuta</i>

Animals maintain complex associations with a diverse microbiota living in their guts. Our understanding of the ecology of these associations is extremely limited in reptiles. Here, we report an in-depth study into the microbial ecology of gut communities in three syntopic and viviparous lizard species (two omnivores: Liolaemus parvus and Liolaemus ruibali and an herbivore: Phymaturus williamsi). Using 16S rRNA gene sequencing to inventory various bacterial communities, we elucidate four major findings: (i) closely related lizard species harbour distinct gut bacterial microbiota that remain distinguishable in captivity; a considerable portion of gut bacterial diversity (39.1%) in nature overlap with that found on plant material, (ii) captivity changes bacterial community composition, although host-specific communities are retained, (iii) faecal samples are largely representative of the hindgut bacterial community and thus represent acceptable sources for nondestructive sampling, and (iv) lizards born in captivity and separated from their mothers within 24 h shared 34.3% of their gut bacterial diversity with their mothers, suggestive of maternal or environmental transmission. Each of these findings represents the first time such a topic has been investigated in lizard hosts. Taken together, our findings provide a foundation for comparative analyses of the faecal and gastrointestinal microbiota of reptile hosts.

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“…; McKenney et al . ). Large‐scale inventories of microbial diversity have been conducted across mammals (Ley et al .…”

Section: Introductionmentioning

confidence: 97%

Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission

et al. 2016

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“…Jani & Briggs, ; Mshelia et al, ). Host characteristics such as sex, body condition and the presence or absence of pathogens are recognized as important for shaping microbial communities (Britton & Young, ; Cheng et al, ; Ganz et al, ; Hooper, Littman, & Macpherson, ; Jani & Briggs, , ; McKenney et al, ; Mshelia et al, ; Näpflin & Schmid‐Hempel, ). For example, horses in poor body condition have greater microbial diversity and a different suite of microbial species present compared to horses in good body condition (Mshelia et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…Jani & Briggs, 2014;Mshelia et al, 2018). Host characteristics such as sex, body condition and the presence or absence of pathogens are recognized as important for shaping microbial communities (Britton & Young, 2014;Cheng et al, 2015;Ganz et al, 2017;Hooper, Littman, & Macpherson, 2012;Jani & Briggs, 2014, 2018McKenney et al, 2015;Mshelia et al, 2018;Näpflin & Schmid-Hempel, 2018).…”

Section: Introductionmentioning

confidence: 99%

Microbial associations and spatial proximity predict North American moose (Alces alces) gastrointestinal community composition

Fountain-Jones

Clark

Kinsley

et al. 2020

Journal of Animal Ecology

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Microbial communities are increasingly recognized as crucial for animal health. However, our understanding of how microbial communities are structured across wildlife populations is poor. Mechanisms such as interspecific associations are important in structuring free‐living communities, but we still lack an understanding of how important interspecific associations are in structuring gut microbial communities in comparison with other factors such as host characteristics or spatial proximity of hosts. Here, we ask how gut microbial communities are structured in a population of North American moose Alces alces. We identify key microbial interspecific associations within the moose gut and quantify how important they are relative to key host characteristics, such as body condition, for predicting microbial community composition. We sampled gut microbial communities from 55 moose in a population experiencing decline due to a myriad of factors, including pathogens and malnutrition. We examined microbial community dynamics in this population utilizing novel graphical network models that can explicitly incorporate spatial information. We found that interspecific associations were the most important mechanism structuring gut microbial communities in moose and detected both positive and negative associations. Models only accounting for associations between microbes had higher predictive value compared to models including moose sex, evidence of previous pathogen exposure or body condition. Adding spatial information on moose location further strengthened our model and allowed us to predict microbe occurrences with ~90% accuracy. Collectively, our results suggest that microbial interspecific associations coupled with host spatial proximity are vital in shaping gut microbial communities in a large herbivore. In this case, previous pathogen exposure and moose body condition were not as important in predicting gut microbial community composition. The approach applied here can be used to quantify interspecific associations and gain a more nuanced understanding of the spatial and host factors shaping microbial communities in non‐model hosts.

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“…In particular, given the primary role played by gastrointestinal dysbiosis in the pathogenesis of CeD12, it has been proposed that one of the mechanisms by which hookworms can support intestinal immune homeostasis in inflammatory disorders (such as CeD), is via the alteration of the composition of the gut microbiota and relative abundance of individual microbial species81314151617. This hypothesis is based on the results of recent studies by us and others, in which experimental infections with gastrointestinal helminths were accompanied by detectable changes in commensal bacterial composition of both human and animal hosts131417181920, as well as of the metabolic profiles of bacterial communities which indirectly promote the development of host regulatory T-cell responses21. In our previous study, experimental hookworm infection of human volunteers with CeD and administration of progressively increasing doses of dietary gluten resulted in maintenance of the composition of the gut flora, as determined from faecal samples from these subjects14.…”

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confidence: 99%

Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease

Giacomin

Zakrzewski

Jenkins

et al. 2016

Sci Rep

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A reduced diversity of the gastrointestinal commensal microbiota is associated with the development of several inflammatory diseases. Recent reports in humans and animal models have demonstrated the beneficial therapeutic effects of infections by parasitic worms (helminths) in some inflammatory disorders, such as inflammatory bowel disease (IBD) and coeliac disease (CeD). Interestingly, these studies have described how helminths may alter the intestinal microbiota, potentially representing a mechanism by which they regulate inflammation. However, for practical reasons, these reports have primarily analysed the faecal microbiota. In the present investigation, we have assessed, for the first time, the changes in the microbiota at the site of infection by a parasitic helminth (hookworm) and gluten-dependent inflammation in humans with CeD using biopsy tissue from the duodenum. Hookworm infection and gluten exposure were associated with an increased abundance of species within the Bacteroides phylum, as well as increases in the richness and diversity of the tissue-resident microbiota within the intestine, results that are consistent with previous reports using other helminth species in humans and animal models. Hence, this may represent a mechanism by which parasitic helminths may restore intestinal immune homeostasis and exert a therapeutic benefit in CeD, and potentially other inflammatory disorders.

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Alteration of the rat cecal microbiome during colonization with the helminthHymenolepis diminuta

Cited by 84 publications

References 29 publications

Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission

Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission

Microbial associations and spatial proximity predict North American moose (Alces alces) gastrointestinal community composition

Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease

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