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Scientific reports2021; 11(1); 4332; doi: 10.1038/s41598-021-83783-z

The pelvic flexure separates distinct microbial communities in the equine hindgut.

Abstract: As hindgut fermenters, horses are especially dependent on the microbiota residing in their cecum and large intestines. Interactions between these microbial populations and the horse are critical for maintaining gut homeostasis, which supports proper digestion. The current project was motivated to determine if any features of the fecal microbiota are informative of the microbial communities from the cecum, ventral colon, or dorsal colon. Digesta from the cecum, ventral colon, dorsal colon and feces were collected from 6 yearling miniature horses. Microbial DNA was isolated and the microbiota from each sample was characterized by profiling the V4 region of the 16S rRNA. Principal coordinate analysis of the beta diversity results revealed significant (p = 0.0001; F = 5.2393) similarities between the microbial populations from cecal and ventral colon and the dorsal colon and fecal samples, however, there was little overlap between the proximal and distal ends of the hindgut. These distinct population structures observed in our results coincide with the pelvic flexure, which itself separates intestinal compartments with distinct roles in digestive physiology. An indicator species analysis confirmed the population differences, supported by the identification of several microbial families characteristic of the compartments upstream of the pelvic flexure that were not represented following it. Our data suggest that the fecal microbiota is not informative of the proximal hindgut but can provide insight into communities of the distal compartments. Further, our results suggest that the pelvic flexure might be an important anatomical landmark relative to the microbial communities in the equine large intestine.
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Publication Date: 2021-02-22 PubMed ID: 33619300PubMed Central: PMC7900177DOI: 10.1038/s41598-021-83783-zGoogle Scholar: Lookup
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  • Journal Article
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  • 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.

This research investigates the presence of distinct microbial communities in different parts of a horse’s gut, focusing specifically on the role of the pelvic flexure in separating these communities.

Research Motivation and Methodology

The research was motivated by the critical role microbiota play in the digestion process in horses, particularly in their cecum and large intestines. The team wanted to understand if any signs of the fecal microbiota could give information about the microbial communities in these segments of the horse’s hindgut.

Data was gathered by collecting samples from diverse regions of the gut, including the cecum, ventral colon, dorsal colon, and feces, from 6 yearling miniature horses. A molecular biology technique was employed, isolating microbial DNA and profiling the V4 region of the 16S rRNA to characterize the microbiota in each sample.

Findings

Analysing the beta diversity results, the team found significant similarities between the microbial populations in the cecal and ventral colon and between those in the dorsal colon and fecal samples. However, there was little overlap between the microbiota at the proximal (or earlier) and distal (or later) ends of the hindgut.

Interestingly, these different community populations align with the location of the pelvic flexure—an anatomical structure in the horse’s intestine. It separates the intestinal compartments, each of which has unique roles in digestive physiology.

Indicator Species Analysis and Conclusions

An indicator species analysis reaffirmed these population differences. Certain microbial families were found characteristic of the compartments situated upstream (or before) the pelvic flexure, with these families not evident in those located after it.

This led to two main conclusions:

  • The fecal microbiota cannot provide information about the microbiota in the proximal hindgut. However, it can offer insight into the microbial communities in the distal compartments.
  • The pelvic flexure appears to be a significant anatomical landmark related to the microbial communities in a horse’s large intestine.

This lays valuable groundwork for a more detailed understanding of the symbiotic relationship between horses and their internal microbial communities, which could have implications for the treatment of equine digestive diseases.

Cite This Article

APA
Reed KJ, Kunz IGZ, Scare JA, Nielsen MK, Turk PJ, Coleman RJ, Coleman SJ. (2021). The pelvic flexure separates distinct microbial communities in the equine hindgut. Sci Rep, 11(1), 4332. https://doi.org/10.1038/s41598-021-83783-z

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 11
Issue: 1
Pages: 4332
PII: 4332

Researcher Affiliations

Reed, Kailee J
  • Animal Sciences, Colorado State University, Fort Collins, CO, 80521, USA.
  • Cell and Molecular Biology Program, Colorado State University, Fort Collins, CO, 80521, USA.
Kunz, Isabelle G Z
  • Animal Sciences, Colorado State University, Fort Collins, CO, 80521, USA.
Scare, Jessica A
  • M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
Nielsen, Martin K
  • M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA.
Turk, Philip J
  • Animal Sciences, Colorado State University, Fort Collins, CO, 80521, USA.
  • Atrium Health, Charlotte, NC, 28203, USA.
Coleman, Robert J
  • Animal and Food Sciences, University of Kentucky, Lexington, KY, 40546, USA.
Coleman, Stephen J
  • Animal Sciences, Colorado State University, Fort Collins, CO, 80521, USA. stephen.coleman@colostate.edu.
  • Cell and Molecular Biology Program, Colorado State University, Fort Collins, CO, 80521, USA. stephen.coleman@colostate.edu.

MeSH Terms

  • Animals
  • Biodiversity
  • Gastrointestinal Microbiome
  • Horses
  • Intestine, Large
  • Metagenome
  • Metagenomics / methods
  • Pelvis / anatomy & histology

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 66 references
  1. Moore JN, Melton T, Carter WC, Wright AL, Smith ML. A new look at equine gastrointestinal anatomy, function, and selected intestinal displacements.. AAEP Proc 2001;47:53–60.
  2. Pilliner S. Horse Nutrition and Feeding. 1. New York: Blackwell Scientific Publications; 1993.
  3. Popesko P, Getty R. Atlas of topographical anatomy of the domestic animals, volumes I-III. (1971).
  4. Frape D. Equine Nutrition and Feeding. 4. New York: Wiley-Blackwell; 2010.
  5. Sneddon JC, Argenzio RA. Feeding strategy and water homeostasis in equids: The role of the hind gut. J. Arid Environ 1998;38:493–509.
    doi: 10.1006/jare.1997.0354google scholar: lookup
  6. Al Jassim RA, Andrews FM. The bacterial community of the horse gastrointestinal tract and its relation to fermentative acidosis, laminitis, colic, and stomach ulcers.. Vet Clin North Am Equine Pract 2009 Aug;25(2):199-215.
    doi: 10.1016/j.cveq.2009.04.005pubmed: 19580934google scholar: lookup
  7. Dicks LM, Botha M, Dicks E, Botes M. The equine gastro-intestinal tract: An overview of the microbiota, disease and treatment. Livestock Sci 2014;160:69–81.
    doi: 10.1016/j.livsci.2013.11.025google scholar: lookup
  8. 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.
    pmc: PMC3409227pubmed: 22859989doi: 10.1371/journal.pone.0041484google scholar: lookup
  9. D'Argenio V, Salvatore F. The role of the gut microbiome in the healthy adult status.. Clin Chim Acta 2015 Dec 7;451(Pt A):97-102.
    doi: 10.1016/j.cca.2015.01.003pubmed: 25584460google scholar: lookup
  10. Debelius J, Song SJ, Vazquez-Baeza Y, Xu ZZ, Gonzalez A, Knight R. Tiny microbes, enormous impacts: what matters in gut microbiome studies?. Genome Biol 2016 Oct 19;17(1):217.
    doi: 10.1186/s13059-016-1086-xpmc: PMC5072314pubmed: 27760558google scholar: lookup
  11. Elzinga SE, Weese JS, Adams AA. Comparison of the fecal microbiota in horses with equine metabolic syndrome and metabolically normal controls fed a similar all-forage diet. J. Equine Vet. Sci. 2016;44:9–16.
    doi: 10.1016/j.jevs.2016.05.010google scholar: lookup
  12. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system.. Cell 2007 Oct 5;131(1):33-45.
    doi: 10.1016/j.cell.2007.08.017pmc: PMC2169385pubmed: 17923086google scholar: lookup
  13. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project.. Nature 2007 Oct 18;449(7164):804-10.
    doi: 10.1038/nature06244pmc: PMC3709439pubmed: 17943116google scholar: lookup
  14. Yan W, Sun C, Zheng J, Wen C, Ji C, Zhang D, Chen Y, Hou Z, Yang N. Efficacy of Fecal Sampling as a Gut Proxy in the Study of Chicken Gut Microbiota.. Front Microbiol 2019;10:2126.
    doi: 10.3389/fmicb.2019.02126pmc: PMC6753641pubmed: 31572332google scholar: lookup
  15. Wang X, Tsai T, Deng F, Wei X, Chai J, Knapp J, Apple J, Maxwell CV, Lee JA, Li Y, Zhao J. Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria.. Microbiome 2019 Jul 30;7(1):109.
    doi: 10.1186/s40168-019-0721-7pmc: PMC6664762pubmed: 31362781google scholar: lookup
  16. Díaz-Sánchez S, Perrotta AR, Rockafellow I, Alm EJ, Okimoto R, Hawken R, Hanning I. Using fecal microbiota as biomarkers for predictions of performance in the selective breeding process of pedigree broiler breeders.. PLoS One 2019;14(5):e0216080.
    doi: 10.1371/journal.pone.0216080pmc: PMC6504170pubmed: 31063485google scholar: lookup
  17. Amitay EL, Krilaviciute A, Brenner H. Systematic review: Gut microbiota in fecal samples and detection of colorectal neoplasms.. Gut Microbes 2018 Jul 4;9(4):293-307.
    pmc: PMC6219654pubmed: 29543545doi: 10.1080/19490976.2018.1445957google scholar: lookup
  18. Hills RD Jr, Pontefract BA, Mishcon HR, Black CA, Sutton SC, Theberge CR. Gut Microbiome: Profound Implications for Diet and Disease.. Nutrients 2019 Jul 16;11(7).
    doi: 10.3390/nᄇ1613pmc: PMC6682904pubmed: 31315227google scholar: lookup
  19. Wang Z, Zolnik CP, Qiu Y, Usyk M, Wang T, Strickler HD, Isasi CR, Kaplan RC, Kurland IJ, Qi Q, Burk RD. Comparison of Fecal Collection Methods for Microbiome and Metabolomics Studies.. Front Cell Infect Microbiol 2018;8:301.
    doi: 10.3389/fcimb.2018.00301pmc: PMC6127643pubmed: 30234027google scholar: lookup
  20. Kauter A, Epping L, Semmler T, Antao EM, Kannapin D, Stoeckle SD, Gehlen H, Lübke-Becker A, Günther S, Wieler LH, Walther B. The gut microbiome of horses: current research on equine enteral microbiota and future perspectives.. Anim Microbiome 2019 Nov 13;1(1):14.
    doi: 10.1186/s42523-019-0013-3pmc: PMC7807895pubmed: 33499951google scholar: lookup
  21. Leng J, Proudman C, Darby A, Blow F, Townsend N, Miller A, Swann J. Exploration of the Fecal Microbiota and Biomarker Discovery in Equine Grass Sickness.. J Proteome Res 2018 Mar 2;17(3):1120-1128.
    doi: 10.1021/acs.jproteome.7b00784pubmed: 29364680google scholar: lookup
  22. 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
  23. Willing B, Vörös A, Roos S, Jones C, Jansson A, Lindberg JE. Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training.. Equine Vet J 2009 Dec;41(9):908-14.
    doi: 10.2746/042516409X447806pubmed: 20383990google scholar: lookup
  24. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC 2nd, Elzinga S, Newbold CJ. Characterisation of the faecal bacterial community in adult and elderly horses fed a high fibre, high oil or high starch diet using 454 pyrosequencing.. PLoS One 2014;9(2):e87424.
    doi: 10.1371/journal.pone.0087424pmc: PMC3913607pubmed: 24504261google scholar: lookup
  25. Sadet-Bourgeteau S, Philippeau C, Dequiedt S, Julliand V. Comparison of the bacterial community structure within the equine hindgut and faeces using Automated Ribosomal Intergenic Spacer Analysis (ARISA).. Animal 2014 Dec;8(12):1928-34.
    doi: 10.1017/S1751731114001943pubmed: 25075719google scholar: lookup
  26. Fliegerova K, Mura E, Mrázek J, Moniello G. A comparison of microbial profiles of different regions of the equine hindgut. Livestock Sci 2016;190:16–19.
    doi: 10.1016/j.livsci.2016.05.015google scholar: lookup
  27. Costa MC, Silva G, Ramos RV, Staempfli HR, Arroyo LG, Kim P, Weese JS. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.. Vet J 2015 Jul;205(1):74-80.
    doi: 10.1016/j.tvjl.2015.03.018pubmed: 25975855google scholar: lookup
  28. Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract.. PLoS One 2016;11(11):e0166523.
    pmc: PMC5112786pubmed: 27846295doi: 10.1371/journal.pone.0166523google scholar: lookup
  29. Dougal K, Harris PA, Edwards A, Pachebat JA, Blackmore TM, Worgan HJ, Newbold CJ. A comparison of the microbiome and the metabolome of different regions of the equine hindgut.. FEMS Microbiol Ecol 2012 Dec;82(3):642-52.
    doi: 10.1111/j.1574-6941.2012.01441.xpubmed: 22757649google scholar: lookup
  30. Su S, Zhao Y, Liu Z, Liu G, Du M, Wu J, Bai D, Li B, Bou G, Zhang X, Dugarjaviin M. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments of Mongolian horses.. Microbiologyopen 2020 Jun;9(6):1085-1101.
    doi: 10.1002/mbo3.1020pmc: PMC7294312pubmed: 32153142google scholar: lookup
  31. Schoster A, Arroyo LG, Staempfli HR, Weese JS. Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism.. BMC Res Notes 2013 Mar 12;6:91.
    doi: 10.1186/1756-0500-6-91pmc: PMC3622624pubmed: 23497580google scholar: lookup
  32. 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
  33. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Newbold CJ. Identification of a core bacterial community within the large intestine of the horse.. PLoS One 2013;8(10):e77660.
    doi: 10.1371/journal.pone.0077660pmc: PMC3812009pubmed: 24204908google scholar: lookup
  34. Debelius J, Song SJ, Vazquez-Baeza Y, Xu ZZ, Gonzalez A, Knight R. Tiny microbes, enormous impacts: what matters in gut microbiome studies?. Genome Biol 2016 Oct 19;17(1):217.
    doi: 10.1186/s13059-016-1086-xpmc: PMC5072314pubmed: 27760558google scholar: lookup
  35. Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, Feh C, Taberlet P, Coissac E, Amir A, Willerslev E, Knight R, McKenzie V, Orlando L. Evaluating the impact of domestication and captivity on the horse gut microbiome.. Sci Rep 2017 Nov 14;7(1):15497.
    doi: 10.1038/s41598-017-15375-9pmc: PMC5686199pubmed: 29138485google scholar: lookup
  36. Okumura R, Takeda K. Roles of intestinal epithelial cells in the maintenance of gut homeostasis.. Exp Mol Med 2017 May 26;49(5):e338.
    doi: 10.1038/emm.2017.20pmc: PMC5454438pubmed: 28546564google scholar: lookup
  37. Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, Comstock LE, Gandhi R, Weiner HL. The Host Shapes the Gut Microbiota via Fecal MicroRNA.. Cell Host Microbe 2016 Jan 13;19(1):32-43.
    doi: 10.1016/j.chom.2015.12.005pmc: PMC4847146pubmed: 26764595google scholar: lookup
  38. Belcheva A. MicroRNAs at the epicenter of intestinal homeostasis.. Bioessays 2017 Mar;39(3).
    doi: 10.1002/bies.201600200pubmed: 28155997google scholar: lookup
  39. Natividad JM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications.. Pharmacol Res 2013 Mar;69(1):42-51.
    doi: 10.1016/j.phrs.2012.10.007pubmed: 23089410google scholar: lookup
  40. Carignan V, Villard MA. Selecting indicator species to monitor ecological integrity: a review.. Environ Monit Assess 2002 Aug;78(1):45-61.
    doi: 10.1023/A:1016136723584pubmed: 12197640google scholar: lookup
  41. McCune B, Grace JB, Urban DL. Analysis of Ecological Communities. Gleneden Beach: MjM Software Design; 2002.
  42. Cariveau DP, Elijah Powell J, Koch H, Winfree R, Moran NA. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus).. ISME J 2014 Dec;8(12):2369-79.
    doi: 10.1038/ismej.2014.68pmc: PMC4260702pubmed: 24763369google scholar: lookup
  43. Cong X, Xu W, Janton S, Henderson WA, Matson A, McGrath JM, Maas K, Graf J. Gut Microbiome Developmental Patterns in Early Life of Preterm Infants: Impacts of Feeding and Gender.. PLoS One 2016;11(4):e0152751.
    doi: 10.1371/journal.pone.0152751pmc: PMC4844123pubmed: 27111847google scholar: lookup
  44. Antharam VC, McEwen DC, Garrett TJ, Dossey AT, Li EC, Kozlov AN, Mesbah Z, Wang GP. An Integrated Metabolomic and Microbiome Analysis Identified Specific Gut Microbiota Associated with Fecal Cholesterol and Coprostanol in Clostridium difficile Infection.. PLoS One 2016;11(2):e0148824.
    doi: 10.1371/journal.pone.0148824pmc: PMC4752508pubmed: 26871580google scholar: lookup
  45. Rosenberg E. The family Prevotellaceae. In the prokaryotes 825–827 (2014).
  46. Venable EB. Effects of feeding management on the equine cecal microbiota. J. Equine Vet. Sci. 2017;49:113–121.
    doi: 10.1016/j.jevs.2016.09.010google scholar: lookup
  47. Sonomoto K, Yokota A. Lactic Acid Bacteria and Bifidobacteria: Current Progress in Advanced Research. Poole: Horizon Scientific Press; 2011.
  48. Makarova KS, Koonin EV. Evolutionary genomics of lactic acid bacteria.. J Bacteriol 2007 Feb;189(4):1199-208.
    doi: 10.1128/JB.01351-06pmc: PMC1797341pubmed: 17085562google scholar: lookup
  49. Ormerod KL, Wood DL, Lachner N, Gellatly SL, Daly JN, Parsons JD, Dal'Molin CG, Palfreyman RW, Nielsen LK, Cooper MA, Morrison M, Hansbro PM, Hugenholtz P. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals.. Microbiome 2016 Jul 7;4(1):36.
    doi: 10.1186/s40168-016-0181-2pmc: PMC4936053pubmed: 27388460google scholar: lookup
  50. Palm NW, de Zoete MR, Cullen TW, Barry NA, Stefanowski J, Hao L, Degnan PH, Hu J, Peter I, Zhang W, Ruggiero E, Cho JH, Goodman AL, Flavell RA. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease.. Cell 2014 Aug 28;158(5):1000-1010.
    doi: 10.1016/j.cell.2014.08.006pmc: PMC4174347pubmed: 25171403google scholar: lookup
  51. Bunker JJ, Flynn TM, Koval JC, Shaw DG, Meisel M, McDonald BD, Ishizuka IE, Dent AL, Wilson PC, Jabri B, Antonopoulos DA, Bendelac A. Innate and Adaptive Humoral Responses Coat Distinct Commensal Bacteria with Immunoglobulin A.. Immunity 2015 Sep 15;43(3):541-53.
    doi: 10.1016/j.immuni.2015.08.007pmc: PMC4575282pubmed: 26320660google scholar: lookup
  52. Yoon J. Phylogenetic studies on the bacterial phylum ‘Verrucomicrobia’. Microbiol. Cult. Coll. 2011;27:61–65.
  53. Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, Latreille P, Kim K, Wilson RK, Gordon JI. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut.. Proc Natl Acad Sci U S A 2007 Jun 19;104(25):10643-8.
    doi: 10.1073/pnas.0704189104pmc: PMC1890564pubmed: 17563350google scholar: lookup
  54. Scanlan PD, Shanahan F, Marchesi JR. Human methanogen diversity and incidence in healthy and diseased colonic groups using mcrA gene analysis.. BMC Microbiol 2008 May 20;8:79.
    doi: 10.1186/1471-2180-8-79pmc: PMC2408590pubmed: 18492229google scholar: lookup
  55. Mihajlovski A, Doré J, Levenez F, Alric M, Brugère JF. Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity.. Environ Microbiol Rep 2010 Apr;2(2):272-80.
    doi: 10.1111/j.1758-2229.2009.00116.xpubmed: 23766078google scholar: lookup
  56. Lwin KO, Matsui H. Comparative analysis of the methanogen diversity in horse and pony by using mcrA gene and archaeal 16s rRNA gene clone libraries.. Archaea 2014;2014:483574.
    pmc: PMC3941164pubmed: 24678264doi: 10.1155/2014/483574google scholar: lookup
  57. Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, Benno Y. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR.. Appl Environ Microbiol 2001 Jun;67(6):2766-74.
    doi: 10.1128/AEM.67.6.2766-2774.2001pmc: PMC92937pubmed: 11375193google scholar: lookup
  58. Yanagita K, Kamagata Y, Kawaharasaki M, Suzuki T, Nakamura Y, Minato H. Phylogenetic analysis of methanogens in sheep rumen ecosystem and detection of Methanomicrobium mobile By fluorescence in situ hybridization.. Biosci Biotechnol Biochem 2000 Aug;64(8):1737-42.
    doi: 10.1271/bbb.64.1737pubmed: 10993166google scholar: lookup
  59. Lyons E. Population-S benzimidazole- and tetrahydropyrimidine-resistant small strongyles in a pony herd in Kentucky (1977-1999): effects of anthelmintic treatment on the parasites as determined in critical tests.. Parasitol Res 2003 Nov;91(5):407-11.
    doi: 10.1007/s00436-003-0983-6pubmed: 14530968google scholar: lookup
  60. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
    doi: 10.1038/nmeth.3869pmc: PMC4927377pubmed: 27214047google scholar: lookup
  61. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments.. PLoS One 2010 Mar 10;5(3):e9490.
    pmc: PMC2835736pubmed: 20224823doi: 10.1371/journal.pone.0009490google scholar: lookup
  62. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications.. BMC Bioinformatics 2009 Dec 15;10:421.
    doi: 10.1186/1471-2105-10-421pmc: PMC2803857pubmed: 20003500google scholar: lookup
  63. 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
  64. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 2001;26:32–46.
  65. De Cáceres M, Legendre P. Associations between species and groups of sites: indices and statistical inference.. Ecology 2009 Dec;90(12):3566-74.
    doi: 10.1890/08-1823.1pubmed: 20120823google scholar: lookup
  66. Oksanen J. vegan: Community ecology package. R package version 2011:117–8.

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    doi: 10.3389/fimmu.2022.1003247pubmed: 36466834google scholar: lookup
  2. Wei J, Wei L, Ullah A, Geng M, Zhang X, Wang C, Khan MZ, Wang C, Zhang Z. Metagenomic Applications to Herbivore Gut Microbiomes: A Comprehensive Review of Microbial Diversity and Host Interactions. Animals (Basel) 2025 Oct 10;15(20).
    doi: 10.3390/ani15202938pubmed: 41153865google scholar: lookup
  3. Li F, Kong X, Khan MZ, Wei L, Wei J, Zhu M, Liu G, Huang B, Wang C, Zhang Z. Gut microbiome regulation in equine animals: current understanding and future perspectives. Front Microbiol 2025;16:1602258.
    doi: 10.3389/fmicb.2025.1602258pubmed: 41070119google scholar: lookup
  4. Zhang W, Guo R, Sulayman A, Sun Y, Liu S. Research Progress on Influencing Factors of Gastrointestinal Microbial Diversity in Equine. Vet Med Sci 2025 May;11(3):e70271.
    doi: 10.1002/vms3.70271pubmed: 40145999google scholar: lookup
  5. Moss CD, Wilson AL, Reed KJ, Jennings KJ, Kunz IGZ, Landolt GA, Metcalf J, Engle TE, Coleman SJ. Gene Expression Analysis before and after the Pelvic Flexure in the Epithelium of the Equine Hindgut. Animals (Basel) 2024 Aug 8;14(16).
    doi: 10.3390/ani14162303pubmed: 39199837google scholar: lookup
  6. Żak-Bochenek A, Żebrowska-Różańska P, Bajzert J, Siwińska N, Madej JP, Kaleta-Kuratewicz K, Bochen P, Łaczmański Ł, Chełmońska-Soyta A. Comparison and characterization of the bacterial microbiota and SIgA production in different gastrointestinal segments in horses. Vet Res Commun 2024 Dec;48(6):3605-3620.
    doi: 10.1007/s11259-024-10489-8pubmed: 39180603google scholar: lookup
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