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

Hu, Dini; Chao, Yuzhu; Zhang, Boru; Wang, Chen; Qi, Yue; Ente, Make; Zhang, Dong; Li, Kai; Mok, Kai Meng

doi:10.1371/journal.pone.0251512

Cited by 8 publications

(19 citation statements)

References 77 publications

(87 reference statements)

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“…A total of 82 bacterial phyla were detected in FATPHs and PATPHs, which is far more than the 23 phyla identified with 16S rRNA sequencing, referencing with the 16S rRNA sequencing results by Hu et al ( 4 ), who did not find the presence of the Gemmatimonadetes phylum in FATPHs, but only a small 0.0012% in PATPHs. Results of the present metagenomic sequencing showed a successful detection of the Gemmatimonadetes in both FATPHs and PATPHs with relative abundances (percentage of read number in bacterial community) at 0.018 and 0.023%, respectively.…”

Section: Resultssupporting

confidence: 82%

“…In a previous study of the present research group ( 4 ), fecal samples of seven adult Przewalski's horses (four male, three female) of similar body weight in the KNR prior to (PATPH) and following (FATPH) anthelmintic treatment of ivermectin were collected for DNA extraction and 16S rRNA sequencing. The numbers of horse botfly larvae in the fecal samples of the FATPHs were also recorded for assessing their parasitic infection status before treatment.…”

Section: Methodsmentioning

confidence: 99%

“…The numbers of horse botfly larvae in the fecal samples of the FATPHs were also recorded for assessing their parasitic infection status before treatment. In this study, shotgun metagenomic sequencing was conducted on the same DNA extracts used for 16S rRNA sequencing in Hu et al ( 4 ). Out of the seven pairs of DNA samples, three pairs were chosen for this study based on their corresponding high to low and in between total fecal larva counts (FATPH3: 2,966, FATPH6: 1,928, FATPH1: 724).…”

Section: Methodsmentioning

confidence: 99%

“…(horse botfly) is a common parasite in equids (1,2). Their eggs and larvae can survive in the digestive system (e.g., stomach and intestine) of a host for 8-10 months (3,4). Infection of horse botfly can cause serious clinical diseases, such as dysphagia, gastric and intestinal ulceration, gastric obstruction, and volvulus; it could even lead to severe risks of anemia, diarrhea, gastric rupture, peritonitis, perforating ulcers, and other complications (5)(6)(7).…”

Section: Introductionmentioning

confidence: 99%

“…and Spirochaetes spp. For Przewalski's horses, Hu et al ( 4 ) found that the removal of horse botflies through anthelmintic treatment decreased the alpha diversity of the gut bacterial community, increased its Firmicutes to Bacteroidetes (F/B) ratio, and increased the genera of Streptococcus and Lactobacillus and some pathogenic bacteria. Nonetheless, these studies only explored the changes of the intestinal bacterial community associated with anthelmintic treatments.…”

Section: Introductionmentioning

confidence: 99%

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Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment

Yang²,

et al. 2021

Front. Vet. Sci.

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Intestinal microbiota is involved in immune response and metabolism of the host. The frequent use of anthelmintic compounds for parasite expulsion causes disturbance to the equine intestinal microbiota. However, most studies were on the effects of such treatment on the intestinal bacterial microbes; none is on the entire microbial community including archaea and eukaryotic and viral community in equine animals. This study is the first to explore the differences of the microbial community composition and structure in Przewalski's horses prior to and following anthelmintic treatment, and to determine the corresponding changes of their functional attributes based on metagenomic sequencing. Results showed that in archaea, the methanogen of Euryarchaeota was the dominant phylum. Under this phylum, anthelmintic treatment increased the Methanobrevibacter genus and decreased the Methanocorpusculum genus and two other dominant archaea species, Methanocorpusculum labreanum and Methanocorpusculum bavaricum. In bacteria, Firmicutes and Bacteroidetes were the dominant phyla. Anthelmintic treatment increased the genera of Clostridium and Eubacterium and decreased those of Bacteroides and Prevotella and dominant bacteria species. These altered genera were associated with immunity and digestion. In eukaryota, anthelmintic treatment also changed the genera related to digestion and substantially decreased the relative abundances of identified species. In virus, anthelmintic treatment increased the genus of unclassified_d__Viruses and decreased those of unclassified_f__Siphoviridae and unclassified_f__Myoviridae. Most of the identified viral species were classified into phage, which were more sensitive to anthelmintic treatment than other viruses. Furthermore, anthelmintic treatment was found to increase the number of pathogens related to some clinical diseases in horses. The COG and KEGG function analysis showed that the intestinal microbiota of Przewalski's horse mainly participated in the carbohydrate and amino acid metabolism. The anthelmintic treatment did not change their overall function; however, it displaced the population of the functional microbes involved in each function or pathway. These results provide a complete view on the changes caused by anthelmintic treatment in the intestinal microbiota of the Przewalski's horses.

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Section: Resultssupporting

confidence: 82%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment

Yang²,

et al. 2021

Front. Vet. Sci.

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Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses

Boisseau¹,

Dhorne–Pollet²,

Bars-Cortina³

et al. 2023

iScience

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The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies

Yu-jun²,

Wang³

et al. 2022

Front. Vet. Sci.

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The microbiota and its metabolites play an important role in regulating the host metabolism and immunity. However, the underlying mechanism is still not well studied. Thus, we conducted the LC-MS/MS analysis and RNA-seq analysis on Equus przewalskii with and without horse botfly infestation to determine the metabolites produced by intestinal microbiota in feces and differentially expressed genes (DEGs) related to the immune response in blood and attempted to link them together. The results showed that parasite infection could change the composition of microbial metabolites. These identified metabolites could be divided into six categories, including compounds with biological roles, bioactive peptides, endocrine-disrupting compounds, pesticides, phytochemical compounds, and lipids. The three pathways involving most metabolites were lipid metabolism, amino acid metabolism, and biosynthesis of other secondary metabolites. The significant differences between the host with and without parasites were shown in 31 metabolites with known functions, which were related to physiological activities of the host. For the gene analysis, we found that parasite infection could alarm the host immune response. The gene of “cathepsin W” involved in innate and adaptive immune responses was upregulated. The two genes of the following functions were downregulated: “protein S100-A8” and “protein S100-A9-like isoform X2” involved in chemokine and cytokine production, the toll-like receptor signaling pathway, and immune and inflammatory responses. GO and KEGG analyses showed that immune-related functions of defense response and Th17 cell differentiation had significant differences between the host with and without parasites, respectively. Last, the relationship between metabolites and genes was determined in this study. The purine metabolism and pyrimidine metabolism contained the most altered metabolites and DEGs, which mainly influenced the conversion of ATP, ADP, AMP, GTP, GMP, GDP, UTP, UDP, UMP, dTTP, dTDP, dTMP, and RNA. Thus, it could be concluded that parasitic infection can change the intestinal microbial metabolic activity and enhance immune response of the host through the pathway of purine and pyrimidine metabolism. This results will be a valuable contribution to understanding the bidirectional association of the parasite, intestinal microbiota, and host.

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

Cited by 8 publications

References 77 publications

Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment

Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment

Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses

The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies

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