Helminths, hosts, and their microbiota: new avenues for managing gastrointestinal helminthiases in ruminants

Cortés, Alba; Rooney, James; Bartley, Dave; Nisbet, Alasdair J.; Cantacessi, Cinzia

doi:10.1080/14787210.2020.1782188

Cited by 29 publications

(30 citation statements)

References 76 publications

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“…pecorum infestation. It is believed that parasites are detrimental to the host [ 70 ] due to their impact on the groups of pathobionts and symbionts in the intestinal microbiota. Jenkins et al (2018) [ 58 ] showed that the potentially pathogenic Pseudomonas and the lactic acid production related Leuconostocaceae in the human gut microbiome would decrease when infected by Strongyloides stercoralis .…”

Section: Resultsmentioning

confidence: 99%

Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China

Chao

Zhang

et al. 2021

PLoS ONE

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Horse botflies have been a threat to the Przewalski’s horses in the Kalamaili Nature Reserve in Xinjiang of China since their reintroduction to the original range. As larvae of these parasites could infest the intestine of a horse for months, they could interact with and alter the structure and composition of its intestinal microbiota, affecting adversely its health. Nonetheless, there are no such studies on the rewilded Przewalski’s horses yet. For the first time, this study characterizes the composition of the intestinal microbiota of 7 rewilded Przewalski’s horses infected severely by Gasterophilus pecorum following and prior to their anthelmintic treatment. Bioinformatics analyses of the sequence data obtained by amplicon high throughput sequencing of bacterial 16S rRNA genes showed that G. pecorum infestation significantly increased the richness of the intestinal microbial community but not its diversity. Firmicutes and Bacteroidetes were found the dominant phyla as in other animals, and the parasitic infestation decreased the F/B ratio largely by over 50%. Large reduction in relative abundances of the two genera Streptococcus and Lactobacillus observed with G. pecorum infestation suggested possible changes in colic and digestion related conditions of the infected horses. Variations on the relative abundance of the genus groups known to be pathogenic or symbiotic showed that adverse impact of the G. pecorum infestation could be associated with reduction of the symbiotic genera Lactobacillus and Bifidobacterium that are probiotics and able to promote immunity against parasitic infection.

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Section: Resultsmentioning

confidence: 99%

Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China

Chao

Zhang

et al. 2021

PLoS ONE

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“…Recent investigations have revealed alterations in the gastrointestinal microbial communities as a consequence of helminth infections in the host [ 5 , 46 ]. We examined these changes at the relative abundance level by Fasciola states using LEfSe.…”

Section: Resultsmentioning

confidence: 99%

“…In the Firmicutes phylum, the dominant taxa were Lachnospiraceae , Peptostreptococcaceae and Carnobacteriaceae , which all play important roles in ruminal fermentation, as well as in other digestion-associated processes ( S3 Fig ) [ 48 , 49 ]. However, our LEfSe analysis pointed towards a reduction in the relative abundance of commensal taxa such as Carnobacteriaceae (LDA score> 3.6) in the Fasciola -negative cattle group, which might suggest a reduction in ruminal fermentation capacity associated with the function of these microorganisms that should be evaluated in future studies [ 5 , 49 ]. The same analysis revealed Peptostreptococcaceae as a potential biomarker for the positive status of F .…”

Section: Discussionmentioning

confidence: 99%

“…The findings from this study revealed associations between the expansion of populations of pro-inflammatory bacteria and the presence of the parasite, as well as longitudinal changes in the abundance of certain taxa such as Bacteroidales RF16, the Porphyromonadaceae family, and the Porphyromonas genus. All of these studies, however, have focused on the role of intestinal helminths while neglecting the impact of extra intestinal helminths which, as part of the same system, interact with their host [ 5 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

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Describing the intestinal microbiota of Holstein Fasciola-positive and -negative cattle from a hyperendemic area of fascioliasis in central Colombia

et al. 2021

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The ability to identify compositional changes in the intestinal microbiota of parasitized hosts is important for understanding the physiological processes that may affect animal productivity. Within the field of host–parasite interactions, many studies have suggested that helminths can influence the microbial composition of their hosts via their immunomodulatory effects. Bovine fascioliasis is a helminthiasis widely studied by immunologists, but with little information available regarding gut microbial communities. Thus, we aimed to describe the composition of the intestinal microbiota of Holstein Fasciola-positive and -negative cattle using parasitological methods and ELISA (enzyme-linked immunosorbent assay). Bovine fecal samples (n = 65) were obtained from livestock slaughter plants in the Cundi-Boyacense Colombian highlands (a hyperendemic region for bovine fascioliasis) and studied by amplicon-based next-generation 16S-rRNA and 18S-rRNA gene sequencing. From these samples, 35 were Fasciola hepatica-negative and, 30 were F. hepatica-positive in our detection analysis. Our results showed a reduction in the relative abundance of Bacteroidetes and Ascomycota in the Fasciola-positive samples, along with decreased relative abundances of the commensal taxa previously associated with fermentation and digestion processes. However, metabolomic approaches and functional analyzes of the intestinal microbiota are necessary to support this hypothesis. These findings are a small first step in the development of research aimed at understanding how microbial populations in bovines are modulated in liver helminth infections.

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“…Nevertheless, our findings call for caution when interpreting data generated from in vivo helminth-microbiome interaction studies that may be influenced, amongst others, by factors including sampling site (e.g. mucosally associated vs. faecal microbiota), parasite infective dose, sampling protocols, environmental conditions and diet [ 28 , 37 , 40 , 42 , 59 ]. In particular, whilst in vivo studies of the vertebrate gut microbiome often rely on analyses of faecal samples for both ethical and practical reasons, qualitative and quantitative changes in selected populations of low-abundant bacteria inhabiting proximal sections of the GI system (e.g.…”

Section: Discussionmentioning

confidence: 99%

Vaccination against the brown stomach worm, Teladorsagia circumcincta, followed by parasite challenge, induces inconsistent modifications in gut microbiota composition of lambs

et al. 2021

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Background Growing evidence points towards a role of gastrointestinal (GI) helminth parasites of ruminants in modifying the composition of the host gut flora, with likely repercussions on the pathophysiology of worm infection and disease, and on animal growth and productivity. However, a thorough understanding of the mechanisms governing helminth-microbiota interactions and of their impact on host health and welfare relies on reproducibility and replicability of findings. To this aim, in this study, we analysed quantitative and qualitative fluctuations in the faecal microbiota composition of lambs vaccinated against, and experimentally infected with, the parasitic GI nematode Teladorsagia circumcincta over the course of two separate trials performed over two consecutive years. Methods Two trials were conducted under similar experimental conditions in 2017 and 2018, respectively. In each trial, lambs were randomly assigned to one of the following experimental groups: (i) vaccinated/infected, (ii) unvaccinated/infected and (iii) unvaccinated/uninfected. Faecal samples collected from individual animals were subjected to DNA extraction followed by high-throughput sequencing of the V3-V4 region of the bacterial 16S rRNA gene and bioinformatics and biostatistical analyses of sequence data. Results Substantial differences in the populations of bacteria affected by immunisation against and infection by T. circumcincta were detected when comparing data from the two trials. Nevertheless, the abundance of Prevotella spp. was significantly linked to helminth infection in both trials. Conclusions Despite the largely conflicting findings between the two trials, our data revealed that selected gut microbial populations are consistently affected by T. circumcincta infection and/or vaccination. Nevertheless, our study calls for caution when interpreting data generated from in vivo helminth-microbiome interaction studies that may be influenced by several intrinsic and extrinsic host-, parasite- and environment-related factors.

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Helminths, hosts, and their microbiota: new avenues for managing gastrointestinal helminthiases in ruminants

Cited by 29 publications

References 76 publications

Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China

Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China

Describing the intestinal microbiota of Holstein Fasciola-positive and -negative cattle from a hyperendemic area of fascioliasis in central Colombia

Vaccination against the brown stomach worm, Teladorsagia circumcincta, followed by parasite challenge, induces inconsistent modifications in gut microbiota composition of lambs

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