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PloS one2021; 16(5); e0251512; doi: 10.1371/journal.pone.0251512

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

Abstract: 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.
Publication Date: 2021-05-11 PubMed ID: 33974667PubMed Central: PMC8112688DOI: 10.1371/journal.pone.0251512Google Scholar: Lookup
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  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on understanding the effects of Gasterophilus pecorum infestation, a horse botfly, on the intestinal microbiota of the rewilded Przewalski’s horses in China. The study is significant as it reveals for the first time, the changes in the host’s intestinal microbial community due to parasitic infestation.

Study Objectives and Methodology

  • The study aimed to evaluate the effects of G. pecorum infestation on the microbiota in the intestines of the rewilded Przewalski’s horses specifically in the Kalamaili Nature Reserve.
  • The study targeted 7 rewilded Przewalski’s horses, infected severely with G. pecorum, and analyzed their intestinal microbiota structure both pre and post anthelmintic treatment.
  • Through the use of amplicon high throughput sequencing of bacterial 16S rRNA genes, the researchers provided a bioinformatics analysis of the sequence data obtained.

Key Findings

  • The study found a significant increase in the richness of the intestinal microbial community due to G. pecorum infestation, but it did not affect the diversity of the microbial community.
  • In both the infested and non-infested horses, Firmicutes and Bacteroidetes were found to be the dominant phyla. The study found that parasitic infestation led to a large decrease in the ratio of Firmicutes to Bacteroidetes (F/B ratio) by over 50%.
  • The study found a large decrease in the relative abundance of two genera, Streptococcus and Lactobacillus, suggesting possible changes in colic and digestion-related conditions of the infected horses.
  • There were variations in the relative abundance of certain groups of genus, understood to be either pathogenic or symbiotic, indicating that the adverse impact of G. pecorum infestation could be linked with the reduction of the symbiotic genera – Lactobacillus and Bifidobacterium. These two genera are known to promote immunity against parasitic infection.

Conclusion

  • This study for the first time gives an insight into the changes in the intestinal microbiota of rewilded Przewalski’s horses due to horse botfly infestation, indicating a possible negative effect on horse health. The findings serve as a foundation for future targeted treatments and preservation strategies.

Cite This Article

APA
Hu D, Chao Y, Zhang B, Wang C, Qi Y, Ente M, Zhang D, Li K, Mok KM. (2021). Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China. PLoS One, 16(5), e0251512. https://doi.org/10.1371/journal.pone.0251512

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 16
Issue: 5
Pages: e0251512
PII: e0251512

Researcher Affiliations

Hu, Dini
  • School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Chao, Yuzhu
  • School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Zhang, Boru
  • Qinhuangdao Forestry Bureau, Qinhuangdao, China.
Wang, Chen
  • Altay Management Station of Mt. Kalamaili Ungulate Nature Reserve, Altay, China.
Qi, Yingjie
  • Altay Management Station of Mt. Kalamaili Ungulate Nature Reserve, Altay, China.
Ente, Make
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Urumqi, China.
Zhang, Dong
  • School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Li, Kai
  • School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
Mok, Kai Meng
  • Department of Civil and Environmental Engineering, University of Macau, Macao, China.

MeSH Terms

  • Animals
  • Animals, Wild
  • Antiparasitic Agents / therapeutic use
  • China
  • DNA, Bacterial / isolation & purification
  • Diptera / growth & development
  • Feces / microbiology
  • Feces / parasitology
  • Gastrointestinal Microbiome
  • Horse Diseases / drug therapy
  • Horse Diseases / microbiology
  • Horse Diseases / parasitology
  • Horses / microbiology
  • Horses / parasitology
  • Intestinal Diseases, Parasitic / drug therapy
  • Intestinal Diseases, Parasitic / microbiology
  • Intestinal Diseases, Parasitic / parasitology
  • Intestinal Diseases, Parasitic / veterinary
  • Ivermectin / therapeutic use
  • Lactobacillus / isolation & purification
  • Lactobacillus / physiology
  • Larva
  • Myiasis / drug therapy
  • Myiasis / microbiology
  • Myiasis / veterinary
  • Streptococcus / isolation & purification
  • Streptococcus / physiology
  • Symbiosis

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 86 references
  1. King SRB, Boyd L, Zimmermann W, Kendall BE. Equus ferus (errata version published in 2016). The IUCN red list of threatened species 2015: e. T41763A97204950. 2015.
  2. Jiang Z, Zong H. Reintroduction of the Przewalski’s horse in China: status quo and outlook. Nature conservation research 2019, 4:15–22.
  3. Gao X, Gu J, Zhou J. The change on the distribution area of the wild horse in the modern times. Arid zone research 1989, 6:49–54.
  4. Xia C, Cao J, Zhang H, Gao X, Yang W, Blank D. Reintroduction of Przewalski’s horse (Equus ferus przewalskii) in Xinjiang, China: the status and experience. Biological conservation 2014, 177, 142–147.
  5. Wakefield S, Knowles J, Zimmermann W, Van Dierendonck MC. Status and action plan for the Przewalski’s horse (Equus ferus przewalskii). 2002, In: Moehlman P. (Ed.), Equids: Zebras, Asses and Horses. IUCN Publications Services Unit, Cambridge, UK, IUCN/SSC Equid Specialist Group, 82–92.
  6. Kaczensky P, Ganbaatar O, von Wehrden H, Enksaikhan N, Lkhagvasuren D, Walzer C. Przewalski's Horse (Equus ferus przewalskii) Re-introduction in the Great Gobi B Strictly Protected Area: from Species to Ecosystem Conservation.. Mong J Biol Sci 2007 Dec;5(1-2):13-18.
    doi: 10.22353/mjbs.2007.05.03pmc: PMC3207201pubmed: 22064815google scholar: lookup
  7. Duncan P. Zebras, asses, and horses: an action plan for the conservation of wild equids. 1992, IUCN Gland, Switzerland.
  8. Chen J, Weng Q, Chao J, Hu D, Taya K. Reproduction and Development of the Released Przewalski's Horses (Equus przewalskii) in Xinjiang, China.. J Equine Sci 2008;19(1):1-7.
    doi: 10.1294/jes.19.1pmc: PMC4019202pubmed: 24833949google scholar: lookup
  9. Xu X, Huang Y, Hu J, Qi C. Parasites and their repelling of Equus przewalskii in Xinjiang. Chinese journal of veterinary medicine 1995, 7:16.
  10. Li K, Wu Z, Hu D, Cao J, Wang C. A report on new causative agent (Gasterophilus spp.) of the myiasis of Przewalski’s horse occurred in China. Chinese journal of animal and veterinary sciences 2007, 38(8): 837–840.
  11. Zhang H, Li K, Chen J, Hu D. Monitoring of Equus przewalskii parasites. Gansu animal and veterinary sciences 2007, 27: 94–96.
  12. Liu S. Morphology and epidemiological investigation and the mitochondrial cytochrome oxidase I (COI) and 16S rRNA gene phylogenetic of Gasterophilus. 2012, Beijing Forestry University, Beijing.
  13. Wang W, Zhang D, Hu D, Chu H, Cao J, Ente M, Jiang G, Li K. Population genetic structure of Gasterophilus pecorum in the Kalamaili Nature Reserve, Xinjiang, based on mitochondrial cytochrome oxidase (COI) gene sequence.. Med Vet Entomol 2014 Aug;28 Suppl 1:75-82.
    doi: 10.1111/mve.12073pubmed: 25171609google scholar: lookup
  14. Liu SH, Hu DF, Li K. Oviposition site selection by Gasterophilus pecorum (Diptera: Gasterophilidae) in its habitat in Kalamaili Nature Reserve, Xinjiang, China.. Parasite 2015;22:34.
    doi: 10.1051/parasite/2015034pmc: PMC4664853pubmed: 26621549google scholar: lookup
  15. Liu SH, Li K, Hu DF. The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China.. Vet Parasitol 2016 Feb 15;217:36-8.
    doi: 10.1016/j.vetpar.2015.12.028pubmed: 26827858google scholar: lookup
  16. Huang H, Zhang B, Chu H, Zhang D, Li K. Gasterophilus (Diptera, Gasterophilidae) infestation of equids in the Kalamaili Nature Reserve, China.. Parasite 2016;23:36.
    doi: 10.1051/parasite/2016036pmc: PMC5018932pubmed: 27593434google scholar: lookup
  17. Zumpt F. Myasis in man and animals in the old world. 1965, Butterworts, London, UK.
    doi: 10.1007/BF00329589google scholar: lookup
  18. Sequeira JL, Tostes RA, Oliveira-Sequeira TC. Prevalence and macro- and microscopic lesions produced by Gasterophilus nasalis (Diptera: Oestridae) in the Botucatu Region, SP, Brazil.. Vet Parasitol 2001 Dec 13;102(3):261-6.
    doi: 10.1016/s0304-4017(01)00536-2pubmed: 11777606google scholar: lookup
  19. Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
    doi: 10.1016/j.cveq.2017.11.005pubmed: 29402480google scholar: lookup
  20. Srivastava A, Lall R, Talukder J, DuBourdieu D, Gupta RC. Iron Transport Tocopheryl Polyethylene Glycol Succinate in Animal Health and Diseases.. Molecules 2019 Nov 25;24(23).
    doi: 10.3390/molecules24234289pmc: PMC6930530pubmed: 31775281google scholar: lookup
  21. Julliand V, Grimm P. HORSE SPECIES SYMPOSIUM: The microbiome of the horse hindgut: History and current knowledge.. J Anim Sci 2016 Jun;94(6):2262-74.
    doi: 10.2527/jas.2015-0198pubmed: 27285903google scholar: lookup
  22. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions.. Science 2012 Jun 8;336(6086):1262-7.
    doi: 10.1126/science.1223813pubmed: 22674330google scholar: lookup
  23. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.. Science 2011 May 20;332(6032):970-4.
    doi: 10.1126/science.1198719pmc: PMC3303602pubmed: 21596990google scholar: lookup
  24. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Doré J, Antolín M, Artiguenave F, Blottiere HM, Almeida M, Brechot C, Cara C, Chervaux C, Cultrone A, Delorme C, Denariaz G, Dervyn R, Foerstner KU, Friss C, van de Guchte M, Guedon E, Haimet F, Huber W, van Hylckama-Vlieg J, Jamet A, Juste C, Kaci G, Knol J, Lakhdari O, Layec S, Le Roux K, Maguin E, Mérieux A, Melo Minardi R, M'rini C, Muller J, Oozeer R, Parkhill J, Renault P, Rescigno M, Sanchez N, Sunagawa S, Torrejon A, Turner K, Vandemeulebrouck G, Varela E, Winogradsky Y, Zeller G, Weissenbach J, Ehrlich SD, Bork P. Enterotypes of the human gut microbiome.. Nature 2011 May 12;473(7346):174-80.
    doi: 10.1038/nature09944pmc: PMC3728647pubmed: 21508958google scholar: lookup
  25. Costea PI, Hildebrand F, Arumugam M, Bäckhed F, Blaser MJ, Bushman FD, de Vos WM, Ehrlich SD, Fraser CM, Hattori M, Huttenhower C, Jeffery IB, Knights D, Lewis JD, Ley RE, Ochman H, O'Toole PW, Quince C, Relman DA, Shanahan F, Sunagawa S, Wang J, Weinstock GM, Wu GD, Zeller G, Zhao L, Raes J, Knight R, Bork P. Enterotypes in the landscape of gut microbial community composition.. Nat Microbiol 2018 Jan;3(1):8-16.
    doi: 10.1038/s41564-017-0072-8pmc: PMC5832044pubmed: 29255284google scholar: lookup
  26. Sepulveda J, Moeller AH. The Effects of Temperature on Animal Gut Microbiomes.. Front Microbiol 2020;11:384.
    doi: 10.3389/fmicb.2020.00384pmc: PMC7076155pubmed: 32210948google scholar: lookup
  27. Nelson TM, Rogers TL, Brown MV. The gut bacterial community of mammals from marine and terrestrial habitats.. PLoS One 2013;8(12):e83655.
  28. Hong PY, Wheeler E, Cann IK, Mackie RI. Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing.. ISME J 2011 Sep;5(9):1461-70.
    doi: 10.1038/ismej.2011.33pmc: PMC3160690pubmed: 21451584google scholar: lookup
  29. Waligora-Dupriet AJ, Lafleur S, Charrueau C, Choisy C, Cynober L, Butel MJ, Moinard C. Head injury profoundly affects gut microbiota homeostasis: Results of a pilot study.. Nutrition 2018 Jan;45:104-107.
    doi: 10.1016/j.nut.2017.06.026pubmed: 29129229google scholar: lookup
  30. Yoon MY, Yoon SS. Disruption of the Gut Ecosystem by Antibiotics.. Yonsei Med J 2018 Jan;59(1):4-12.
    doi: 10.3349/ymj.2018.59.1.4pmc: PMC5725362pubmed: 29214770google scholar: lookup
  31. Garrett LA, Brown R, Poxton IR. A comparative study of the intestinal microbiota of healthy horses and those suffering from equine grass sickness.. Vet Microbiol 2002 Jun 5;87(1):81-8.
    doi: 10.1016/s0378-1135(02)00018-4pubmed: 12079749google scholar: lookup
  32. Milinovich GJ, Burrell PC, Pollitt CC, Klieve AV, Blackall LL, Ouwerkerk D, Woodland E, Trott DJ. Microbial ecology of the equine hindgut during oligofructose-induced laminitis.. ISME J 2008 Nov;2(11):1089-100.
    doi: 10.1038/ismej.2008.67pubmed: 18580970google scholar: lookup
  33. Costa MC, Arroyo LG, Allen-Vercoe E, Stämpfli HR, Kim PT, Sturgeon A, Weese JS. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene.. PLoS One 2012;7(7):e41484.
  34. Yoshida N, Yamashita T, Hirata KI. Gut Microbiome and Cardiovascular Diseases.. Diseases 2018 Jun 29;6(3).
    doi: 10.3390/diseases6030056pmc: PMC6164700pubmed: 29966270google scholar: lookup
  35. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases.. Proc Natl Acad Sci U S A 2007 Aug 21;104(34):13780-5.
    doi: 10.1073/pnas.0706625104pmc: PMC1959459pubmed: 17699621google scholar: lookup
  36. Aydin Ö, Nieuwdorp M, Gerdes V. The Gut Microbiome as a Target for the Treatment of Type 2 Diabetes.. Curr Diab Rep 2018 Jun 21;18(8):55.
    doi: 10.1007/s11892-018-1020-6pmc: PMC6013535pubmed: 29931613google scholar: lookup
  37. Scher JU, Abramson SB. The microbiome and rheumatoid arthritis.. Nat Rev Rheumatol 2011 Aug 23;7(10):569-78.
    doi: 10.1038/nrrheum.2011.121pmc: PMC3275101pubmed: 21862983google scholar: lookup
  38. Zalar B, Haslberger A, Peterlin B. The Role of Microbiota in Depression - a brief review.. Psychiatr Danub 2018 Jun;30(2):136-141.
    doi: 10.24869/psyd.2018.136pubmed: 29930222google scholar: lookup
  39. Dart A. Gut microbiota bile acid metabolism controls cancer immunosurveillance.. Nat Rev Microbiol 2018 Aug;16(8):453.
    doi: 10.1038/s41579-018-0053-9pubmed: 29946123google scholar: lookup
  40. Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA, Jalali M, Wismer SE. Changes in the faecal microbiota of mares precede the development of post partum colic.. Equine Vet J 2015 Nov;47(6):641-9.
    doi: 10.1111/evj.12361pubmed: 25257320google scholar: lookup
  41. Clark A, Sallé G, Ballan V, Reigner F, Meynadier A, Cortet J, Koch C, Riou M, Blanchard A, Mach N. Strongyle Infection and Gut Microbiota: Profiling of Resistant and Susceptible Horses Over a Grazing Season.. Front Physiol 2018;9:272.
    doi: 10.3389/fphys.2018.00272pmc: PMC5871743pubmed: 29618989google scholar: lookup
  42. Peachey LE, Molena RA, Jenkins TP, Di Cesare A, Traversa D, Hodgkinson JE, Cantacessi C. The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins.. Int J Parasitol 2018 May;48(6):403-412.
  43. Li Y, Zhang K, Liu Y, Li K, Hu D, Wronski T. Community Composition and Diversity of Intestinal Microbiota in Captive and Reintroduced Przewalski's Horse (Equus ferus przewalskii).. Front Microbiol 2019;10:1821.
    doi: 10.3389/fmicb.2019.01821pmc: PMC6693443pubmed: 31440229google scholar: lookup
  44. Tang L, Li Y, Srivathsan A, Gao Y, Li K, Hu D, Zhang D. Gut Microbiomes of Endangered Przewalski's Horse Populations in Short- and Long-Term Captivity: Implication for Species Reintroduction Based on the Soft-Release Strategy.. Front Microbiol 2020;11:363.
    doi: 10.3389/fmicb.2020.00363pmc: PMC7081077pubmed: 32226419google scholar: lookup
  45. Russell WMS, Burch R. The Principles of humane experimental technique. 1959, London, UK: Methuen.
  46. Keane J, Avery L. Mechanosensory inputs influence Caenorhabditis elegans pharyngeal activity via ivermectin sensitivity genes.. Genetics 2003 May;164(1):153-62.
    pmc: PMC1462566pubmed: 12750328doi: 10.1093/genetics/164.1.153google scholar: lookup
  47. Martin RJ, Robertson AP, Choudhary S. Ivermectin: An Anthelmintic, an Insecticide, and Much More.. Trends Parasitol 2021 Jan;37(1):48-64.
    doi: 10.1016/j.pt.2020.10.008pmc: PMC7853155pubmed: 33189582google scholar: lookup
  48. Kunz IGZ, Reed KJ, Metcalf JL, Hassel DM, Coleman RJ, Hess TM, Coleman SJ. Equine Fecal Microbiota Changes Associated With Anthelmintic Administration.. J Equine Vet Sci 2019 Jun;77:98-106.
    doi: 10.1016/j.jevs.2019.01.018pubmed: 31133326google scholar: lookup
  49. Riquelme J, Cazanga V, Jeldres J, Pérez R. Pharmacokinetics of ivermectin in sheep following pretreatment with Escherichia coli endotoxin.. J Vet Pharmacol Ther 2018 Oct;41(5):755-759.
    doi: 10.1111/jvp.12665pubmed: 29889311google scholar: lookup
  50. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, Gaskins HR, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes.. ISME J 2013 Jul;7(7):1344-53.
    doi: 10.1038/ismej.2013.16pmc: PMC3695285pubmed: 23486247google scholar: lookup
  51. Salem SE, Maddox TW, Berg A, Antczak P, Ketley JM, Williams NJ, Archer DC. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period.. Sci Rep 2018 May 31;8(1):8510.
    doi: 10.1038/s41598-018-26930-3pmc: PMC5981443pubmed: 29855517google scholar: lookup
  52. Lin H, Peddada SD. Analysis of microbial compositions: a review of normalization and differential abundance analysis.. NPJ Biofilms Microbiomes 2020 Dec 2;6(1):60.
    doi: 10.1038/s41522-020-00160-wpmc: PMC7710733pubmed: 33268781google scholar: lookup
  53. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
    doi: 10.1038/nmeth.f.303pmc: PMC3156573pubmed: 20383131google scholar: lookup
  54. Walshe N, Duggan V, Cabrera-Rubio R, Crispie F, Cotter P, Feehan O, Mulcahy G. Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses.. Int J Parasitol 2019 May;49(6):489-500.
    doi: 10.1016/j.ijpara.2019.02.003pubmed: 30986403google scholar: lookup
  55. Jovel J, Patterson J, Wang W, Hotte N, O'Keefe S, Mitchel T, Perry T, Kao D, Mason AL, Madsen KL, Wong GK. Characterization of the Gut Microbiome Using 16S or Shotgun Metagenomics.. Front Microbiol 2016;7:459.
    doi: 10.3389/fmicb.2016.00459pmc: PMC4837688pubmed: 27148170google scholar: lookup
  56. DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M. Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil.. Appl Environ Microbiol 2011 Sep;77(17):6295-300.
    doi: 10.1128/AEM.05005-11pmc: PMC3165389pubmed: 21764958google scholar: lookup
  57. Hanada S, Sekiguchi Y. The phylum Gemmatimonadetes. In the Prokaryotes 2014, Springer, 4th edition, 11, 677–681.
  58. Jenkins TP, Peachey LE, Ajami NJ, MacDonald AS, Hsieh MH, Brindley PJ, Cantacessi C, Rinaldi G. Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.. Sci Rep 2018 Aug 13;8(1):12072.
    doi: 10.1038/s41598-018-30412-xpmc: PMC6089957pubmed: 30104612google scholar: lookup
  59. Kim JY, Kim EM, Yi MH, Lee J, Lee S, Hwang Y, Yong D, Sohn WM, Yong TS. Intestinal fluke Metagonimus yokogawai infection increases probiotic Lactobacillus in mouse cecum.. Exp Parasitol 2018 Oct;193:45-50.
    doi: 10.1016/j.exppara.2018.08.002pubmed: 30149004google scholar: lookup
  60. Williams AR, Krych L, Fauzan Ahmad H, Nejsum P, Skovgaard K, Nielsen DS, Thamsborg SM. A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs.. PLoS One 2017;12(10):e0186546.
  61. Peachey LE, Jenkins TP, Cantacessi C. This Gut Ain't Big Enough for Both of Us. Or Is It? Helminth-Microbiota Interactions in Veterinary Species.. Trends Parasitol 2017 Aug;33(8):619-632.
    doi: 10.1016/j.pt.2017.04.004pubmed: 28506779google scholar: lookup
  62. Biddle AS, Tomb JF, Fan Z. Microbiome and Blood Analyte Differences Point to Community and Metabolic Signatures in Lean and Obese Horses.. Front Vet Sci 2018;5:225.
    doi: 10.3389/fvets.2018.00225pmc: PMC6158370pubmed: 30294603google scholar: lookup
  63. Xu Y, Yang H, Zhang L, Su Y, Shi D, Xiao H, Tian Y. High-throughput sequencing technology to reveal the composition and function of cecal microbiota in Dagu chicken.. BMC Microbiol 2016 Nov 4;16(1):259.
    doi: 10.1186/s12866-016-0877-2pmc: PMC5097418pubmed: 27814685google scholar: lookup
  64. Wu X, Zhang H, Chen J, Shang S, Wei Q, Yan J, Tu X. Comparison of the fecal microbiota of dholes high-throughput Illumina sequencing of the V3-V4 region of the 16S rRNA gene.. Appl Microbiol Biotechnol 2016 Apr;100(8):3577-86.
    doi: 10.1007/s00253-015-7257-ypubmed: 26728019google scholar: lookup
  65. Han X, Yang Y, Yan H, Wang X, Qu L, Chen Y. Rumen bacterial diversity of 80 to 110-day-old goats using 16S rRNA sequencing.. PLoS One 2015;10(2):e0117811.
  66. Kim HB, Isaacson RE. The pig gut microbial diversity: Understanding the pig gut microbial ecology through the next generation high throughput sequencing.. Vet Microbiol 2015 Jun 12;177(3-4):242-51.
    doi: 10.1016/j.vetmic.2015.03.014pubmed: 25843944google scholar: lookup
  67. Guo W, Li Y, Wang L, Wang J, Xu Q, Yan T, Xue B. Evaluation of composition and individual variability of rumen microbiota in yaks by 16S rRNA high-throughput sequencing technology.. Anaerobe 2015 Aug;34:74-9.
  68. Stewart HL, Southwood LL, Indugu N, Vecchiarelli B, Engiles JB, Pitta D. Differences in the equine faecal microbiota between horses presenting to a tertiary referral hospital for colic compared with an elective surgical procedure.. Equine Vet J 2019 May;51(3):336-342.
    pubmed: 30153353doi: 10.1111/evj.13010google scholar: lookup
  69. Dicks LMT, Botha M, Dicks E, Botes M. The equine gastro-intestinal tract: an overview of the microbiota, disease and treatment. Livestock science 2014, 160, 69–81.
  70. Cortés A, Rooney J, Bartley DJ, Nisbet AJ, Cantacessi C. Helminths, hosts, and their microbiota: new avenues for managing gastrointestinal helminthiases in ruminants.. Expert Rev Anti Infect Ther 2020 Oct;18(10):977-985.
    doi: 10.1080/14787210.2020.1782188pubmed: 32530331google scholar: lookup
  71. Gilchrist CA, Petri SE, Schneider BN, Reichman DJ, Jiang N, Begum S, Watanabe K, Jansen CS, Elliott KP, Burgess SL, Ma JZ, Alam M, Kabir M, Haque R, Petri WA Jr. Role of the Gut Microbiota of Children in Diarrhea Due to the Protozoan Parasite Entamoeba histolytica.. J Infect Dis 2016 May 15;213(10):1579-85.
    doi: 10.1093/infdis/jiv772pmc: PMC4837909pubmed: 26712950google scholar: lookup
  72. Wu S, Li RW, Li W, Beshah E, Dawson HD, Urban JF Jr. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection.. PLoS One 2012;7(4):e35470.
  73. Murakami S, Kobayashi T, Sekigawa Y, Torii Y, Kanesaki Y, Ishige T, Yokoyama E, Ishiwata H, Hamada M, Tamura T. Actinomyces denticolens as a causative agent of actinomycosis in animals.. J Vet Med Sci 2018 Nov 9;80(11):1650-1656.
    doi: 10.1292/jvms.18-0207pmc: PMC6261818pubmed: 30224576google scholar: lookup
  74. Marinkovic D, Aleksic-Kovacevic S, Plamenac P. Cellular basis of chronic obstructive pulmonary disease in horses.. Int Rev Cytol 2007;257:213-47.
    doi: 10.1016/S0074-7696(07)57006-3pubmed: 17280899google scholar: lookup
  75. Morrison PK, Newbold CJ, Jones E, Worgan HJ, Grove-White DH, Dugdale AH, Barfoot C, Harris PA, Argo CM. The equine gastrointestinal microbiome: impacts of weight-loss.. BMC Vet Res 2020 Mar 4;16(1):78.
    doi: 10.1186/s12917-020-02295-6pmc: PMC7057583pubmed: 32131835google scholar: lookup
  76. Schoster A, Staempfli HR, Guardabassi LG, Jalali M, Weese JS. Comparison of the fecal bacterial microbiota of healthy and diarrheic foals at two and four weeks of life.. BMC Vet Res 2017 May 30;13(1):144.
    doi: 10.1186/s12917-016-0931-1pmc: PMC5450145pubmed: 28558788google scholar: lookup
  77. Rifici C, Attili AR, De Biase D, Gonçalves Dos Santos R, Seyffert N, De Paula Castro TL, Pereira Figueiredo HC, Scaramozzino C, Reale S, Paciello O, Cuteri V, Spier SJ, Azevedo V, Mazzullo G. Atypical Multibacterial Granulomatous Myositis in a Horse: First Report in Italy.. Vet Sci 2020 Apr 21;7(2).
    pmc: PMC7355418pubmed: 32326275doi: 10.3390/vetsci7020047google scholar: lookup
  78. Sykora S, Pieber K, Simhofer H, Hackl V, Brodesser D, Brandt S. Isolation of Treponema and Tannerella spp. from equine odontoclastic tooth resorption and hypercementosis related periodontal disease.. Equine Vet J 2014 May;46(3):358-63.
    doi: 10.1111/evj.12115pubmed: 23742079google scholar: lookup
  79. Maul C, Suchowski M, Klose K, Antov V, Pfeffer M, Schwarz BA. [Detection of Actinobacillus equuli ssp. equuli in piglets with purulent polyarthritis and tendovaginitis].. Tierarztl Prax Ausg G Grosstiere Nutztiere 2020 Feb;48(1):51-58.
    pubmed: 32059237doi: 10.1055/a-1067-3908google scholar: lookup
  80. Kobayashi R, Nagaoka K, Nishimura N, Koike S, Takahashi E, Niimi K, Murase H, Kinjo T, Tsukahara T, Inoue R. Comparison of the fecal microbiota of two monogastric herbivorous and five omnivorous mammals.. Anim Sci J 2020 Jan-Dec;91(1):e13366.
    doi: 10.1111/asj.13366pmc: PMC7216987pubmed: 32285557google scholar: lookup
  81. Sheng T, Zhao L, Gao LF, Liu WZ, Cui MH, Guo ZC, Ma XD, Ho SH, Wang AJ. Lignocellulosic saccharification by a newly isolated bacterium, Ruminiclostridium thermocellum M3 and cellular cellulase activities for high ratio of glucose to cellobiose.. Biotechnol Biofuels 2016;9:172.
    doi: 10.1186/s13068-016-0585-zpmc: PMC4982309pubmed: 27525041google scholar: lookup
  82. Mukhopadhyay B, Ganguly NK. The unexplored role of probiotics on the parasitic pathogens. Food and nutrition sciences 2014, 5, 2177–2184.
  83. Travers MA, Florent I, Kohl L, Grellier P. Probiotics for the control of parasites: an overview.. J Parasitol Res 2011;2011:610769.
    doi: 10.1155/2011/610769pmc: PMC3182331pubmed: 21966589google scholar: lookup
  84. Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic.. Poult Sci 2003 Jan;82(1):62-6.
    doi: 10.1093/ps/82.1.62pubmed: 12580246google scholar: lookup
  85. Holm JB, Sorobetea D, Kiilerich P, Ramayo-Caldas Y, Estellé J, Ma T, Madsen L, Kristiansen K, Svensson-Frej M. Chronic Trichuris muris Infection Decreases Diversity of the Intestinal Microbiota and Concomitantly Increases the Abundance of Lactobacilli.. PLoS One 2015;10(5):e0125495.
  86. Pace F, Carvalho BM, Zanotto TM, Santos A, Guadagnini D, Silva KLC, Mendes MCS, Rocha GZ, Alegretti SM, Santos GA, Catharino RR, Paroni R, Folli F, Saad MJA. Helminth infection in mice improves insulin sensitivity via modulation of gut microbiota and fatty acid metabolism.. Pharmacol Res 2018 Jun;132:33-46.
    doi: 10.1016/j.phrs.2018.04.008pubmed: 29653264google scholar: lookup

Citations

This article has been cited 7 times.
  1. Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, Lluch J, Gesbert A, Reigner F, Sallé G, Mach N. Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses.. iScience 2023 Feb 17;26(2):106044.
    doi: 10.1016/j.isci.2023.106044pubmed: 36818309google scholar: lookup
  2. Turghan MA, Jiang Z, Niu Z. An Update on Status and Conservation of the Przewalski's Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects.. Animals (Basel) 2022 Nov 15;12(22).
    doi: 10.3390/ani12223158pubmed: 36428386google scholar: lookup
  3. Hu D, Wang C, Ente M, Zhang K, Zhang D, Li X, Li K, Chu H. Assessment of Adaptation Status of Reintroduced Equus Przewalskii Based on Comparative Analysis of Fecal Bacteria with Those of Captive E. Przewalskii, Domestic Horse and Mongolian Wild Ass.. Animals (Basel) 2022 Oct 21;12(20).
    doi: 10.3390/ani12202874pubmed: 36290262google scholar: lookup
  4. Wen X, Luo S, Lv D, Jia C, Zhou X, Zhai Q, Xi L, Yang C. Variations in the fecal microbiota and their functions of Thoroughbred, Mongolian, and Hybrid horses.. Front Vet Sci 2022;9:920080.
    doi: 10.3389/fvets.2022.920080pubmed: 35968025google scholar: lookup
  5. Hu D, Tang Y, Wang C, Qi Y, Ente M, Li X, Zhang D, Li K, Chu H. The Role of Intestinal Microbial Metabolites in the Immunity of Equine Animals Infected With Horse Botflies.. Front Vet Sci 2022;9:832062.
    doi: 10.3389/fvets.2022.832062pubmed: 35812868google scholar: lookup
  6. Tang Y, Liu G, Zhao S, Li K, Zhang D, Liu S, Hu D. Major Histocompatibility Complex (MHC) Diversity of the Reintroduction Populations of Endangered Przewalski's Horse.. Genes (Basel) 2022 May 23;13(5).
    doi: 10.3390/genes13050928pubmed: 35627313google scholar: lookup
  7. Hu D, Yang J, Qi Y, Li B, Li K, Mok KM. Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment.. Front Vet Sci 2021;8:708512.
    doi: 10.3389/fvets.2021.708512pubmed: 34490397google scholar: lookup