Analyze Diet
Animal microbiome2020; 2(1); 8; doi: 10.1186/s42523-020-00027-7

Domesticated equine species and their derived hybrids differ in their fecal microbiota.

Abstract: Compared to horses and ponies, donkeys have increased degradation of dietary fiber. The longer total mean retention time of feed in the donkey gut has been proposed to be the basis of this, because of the increased time available for feed to be acted upon by enzymes and the gut microbiota. However, differences in terms of microbial concentrations and/or community composition in the hindgut may also underpin the increased degradation of fiber in donkeys. Therefore, a study was conducted to assess if differences existed between the fecal microbiota of pony, donkey and hybrids derived from them (i.e. pony × donkey) when fed the same forage diet. Results: Fecal community composition of prokaryotes and anaerobic fungi significantly differed between equine types. The relative abundance of two bacterial genera was significantly higher in donkey compared to both pony and pony x donkey: Lachnoclostridium 10 and 'probable genus 10' from the Lachnospiraceae family. The relative abundance of Piromyces was significantly lower in donkey compared to pony × donkey, with pony not significantly differing from either of the other equine types. In contrast, the uncultivated genus SK3 was only found in donkey (4 of the 8 animals). The number of anaerobic fungal OTUs was also significantly higher in donkey than in the other two equine types, with no significant differences found between pony and pony × donkey. Equine types did not significantly differ with respect to prokaryotic alpha diversity, fecal dry matter content or fecal concentrations of bacteria, archaea and anaerobic fungi. Conclusions: Donkey fecal microbiota differed from that of both pony and pony × donkey. These differences related to a higher relative abundance and diversity of taxa with known, or speculated, roles in plant material degradation. These findings are consistent with the previously reported increased fiber degradation in donkeys compared to ponies, and suggest that the hindgut microbiota plays a role. This offers novel opportunities for pony and pony × donkey to extract more energy from dietary fiber via microbial mediated strategies. This could potentially decrease the need for energy dense feeds which are a risk factor for gut-mediated disease.
Publication Date: 2020-03-16 PubMed ID: 33499942PubMed Central: PMC7807894DOI: 10.1186/s42523-020-00027-7Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

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 paper explores the differences in the fecal microbiota of ponies, donkeys, and their crossbreed hybrids when fed the same forage diet. The study reveals that donkeys have a higher and more diverse range of bacteria that help in the degradation of dietary fiber as compared to ponies and hybrids, potentially making them more capable of extracting energy from dietary fiber.

Study Methodology and Results

  • The study was conducted to examine if differences exist in the fecal microbiota of ponies, donkeys, and their hybrids when fed the same forage diet. This was measured based on the community composition of prokaryotes and anaerobic fungi in their gut.
  • Results indicated that the fecal community composition significantly differed among the three equine types. Specifically, donkeys had a significantly higher relative abundance of two bacterial genera (Lachnoclostridium 10 and a ‘probable genus 10’ from the Lachnospiraceae family) compared to ponies and pony-donkey hybrids.
  • The study also found that the genus Piromyces was significantly lower in donkeys than pony-donkey hybrids. However, there was no significant difference in the presence of Piromyces between ponies and the other two types.
  • Additionally, the uncultivated genus SK3 was only found in donkeys, and the number of anaerobic fungal OTUs (Operational Taxonomic Units) was significantly higher in donkeys compared to ponies and their hybrids.
  • It should, however, be noted that the diversity of prokaryotic species, fecal dry matter content, and fecal concentrations of bacteria, archaea, and anaerobic fungi did not significantly differ among the equine types.

Interpretation and Implications

  • The presence of a higher and more diverse range of microbial species in donkeys, especially those known or speculated to play a role in plant material degradation, aligns with previous reports of increased fiber degradation in donkeys compared to ponies.
  • These findings suggest that the higher efficiency in fiber degradation in donkeys can be attributed to the microbiota in their gut, which would ultimately lead to more efficient energy extraction from dietary fiber.
  • If these microbial-enhanced strategies for energy extraction could be replicated or induced in ponies and hybrids, these equine types may be able to gain more energy from dietary fiber, potentially reducing the need for energy-dense feeds which are associated with gut-mediated disease risk.

Cite This Article

APA
Edwards JE, Schennink A, Burden F, Long S, van Doorn DA, Pellikaan WF, Dijkstra J, Saccenti E, Smidt H. (2020). Domesticated equine species and their derived hybrids differ in their fecal microbiota. Anim Microbiome, 2(1), 8. https://doi.org/10.1186/s42523-020-00027-7

Publication

ISSN: 2524-4671
NlmUniqueID: 101759457
Country: England
Language: English
Volume: 2
Issue: 1
Pages: 8
PII: 8

Researcher Affiliations

Edwards, J E
  • Laboratory of Microbiology, Wageningen University & Research, 6708 WE, Wageningen, Netherlands. joanee2002@hotmail.com.
Schennink, A
  • Laboratory of Microbiology, Wageningen University & Research, 6708 WE, Wageningen, Netherlands.
  • Present address: Micreos Human Health B.V, Bilthoven, Netherlands.
Burden, F
  • The Donkey Sanctuary, Sidmouth, Devon, EX10 ONU, UK.
Long, S
  • The Donkey Sanctuary, Sidmouth, Devon, EX10 ONU, UK.
van Doorn, D A
  • Division of Nutrition, Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, 3584 CM, Utrecht, Netherlands.
  • Department of Equine Health, Faculty of Veterinary Medicine, Utrecht University, 3584 CL, Utrecht, Netherlands.
Pellikaan, W F
  • Animal Nutrition Group, Wageningen University & Research, 6708 WD, Wageningen, Netherlands.
Dijkstra, J
  • Animal Nutrition Group, Wageningen University & Research, 6708 WD, Wageningen, Netherlands.
Saccenti, E
  • Laboratory of Systems and Synthetic Biology, Wageningen University & Research, Wageningen, the Netherlands.
Smidt, H
  • Laboratory of Microbiology, Wageningen University & Research, 6708 WE, Wageningen, Netherlands. hauke.smidt@wur.nl.

Grant Funding

  • 706899 / H2020 Marie Sku0142odowska-Curie Actions

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 81 references
  1. Argenzio RA, Southworth M, Stevens CE. Sites of organic acid production and absorption in the equine gastrointestinal tract.. Am J Physiol 1974 May;226(5):1043-50.
  2. Glinsky MJ, Smith RM, Spires HR, Davis CL. Measurement of volatile fatty acid production rates in the cecum of the pony.. J Anim Sci 1976 Jun;42(6):1465-70.
    doi: 10.2527/jas1976.4261465xpubmed: 931822google scholar: lookup
  3. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.. Physiol Rev 1990 Apr;70(2):567-90.
    doi: 10.1152/physrev.1990.70.2.567pubmed: 2181501google scholar: lookup
  4. Durham AE. Intestinal disease. In: Geor RJ, Harris PA, Coenen M, editors. Equine applied and clinical nutrition: health, welfare and performance. Philadelphia: Saunders Elsevier Ltd; 2013. pp. 568–581.
  5. Julliand V, Grimm P. The impact of diet on the hindgut microbiome. J Equine Vet Sci 2017;52:23–28.
  6. . Food and Agriculture Organization for the United Nations, Rome. FAOSTAT 2017.
  7. Burden F, Thiemann A. Donkeys are different. J Equine Vet Sci 2015;35:376–382.
  8. Pearson RA, Merritt JB. Intake, digestion and gastrointestinal transit time in resting donkeys and ponies and exercised donkeys given ad libitum hay and straw diets.. Equine Vet J 1991 Sep;23(5):339-43.
  9. Cí·¯ord D, Pearson RA, Archibald RF, Muirhead R. Digestibility and gastro-intestinal transit time of diets containing different proportions of alfalfa and oat straw given to thoroughbreds, Shetland ponies, Highland ponies and donkeys. Anim Sci 1995;61:407–417.
    doi: 10.1017/S1357729800013953google scholar: lookup
  10. Smith DG, Pearson RA. A review of the factors affecting the survival of donkeys in semi-arid regions of sub-Saharan Africa.. Trop Anim Health Prod 2005 Nov;37 Suppl 1:1-19.
    doi: 10.1007/s11250-005-9002-5pubmed: 16335068google scholar: lookup
  11. Li Z, Wright AG, Si H, Wang X, Qian W, Zhang Z, Li G. Changes in the rumen microbiome and metabolites reveal the effect of host genetics on hybrid crosses.. Environ Microbiol Rep 2016 Dec;8(6):1016-1023.
    doi: 10.1111/1758-2229.12482pubmed: 27717170google scholar: lookup
  12. 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
  13. Moore BE, Dehority BA. Effects of diet and hindgut defaunation on diet digestibility and microbial concentrations in the cecum and colon of the horse.. J Anim Sci 1993 Dec;71(12):3350-8.
    doi: 10.2527/1993.71123350xpubmed: 8294287google scholar: lookup
  14. Julliand V, de Vaux A, Millet L, Fonty G. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species of the equine cecum.. Appl Environ Microbiol 1999 Aug;65(8):3738-41.
  15. Julliand V, Riondet C, De Vaux A, Alcaraz G, Fonty G. Comparison of metabolic activities between Piromyces citronii, an equine fungal species, and Piromyces communis, a ruminal species. Anim Feed Sci Technol 1998;70:161–168.
  16. Solomon KV, Haitjema CH, Henske JK, Gilmore SP, Borges-Rivera D, Lipzen A, Brewer HM, Purvine SO, Wright AT, Theodorou MK, Grigoriev IV, Regev A, Thompson DA, O'Malley MA. Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes.. Science 2016 Mar 11;351(6278):1192-5.
    doi: 10.1126/science.aad1431pmc: PMC5098331pubmed: 26912365google scholar: lookup
  17. Gruninger RJ, Puniya AK, Callaghan TM, Edwards JE, Youssef N, Dagar SS, Fliegerova K, Griffith GW, Forster R, Tsang A, McAllister T, Elshahed MS. Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential.. FEMS Microbiol Ecol 2014 Oct;90(1):1-17.
    doi: 10.1111/1574-6941.12383pubmed: 25046344google scholar: lookup
  18. Gordon GL, Phillips MW. The role of anaerobic gut fungi in ruminants.. Nutr Res Rev 1998 Jun;11(1):133-68.
    doi: 10.1079/NRR19980009pubmed: 19087463google scholar: lookup
  19. Blackmore TM, Dugdale A, Argo CM, Curtis G, Pinloche E, Harris PA, Worgan HJ, Girdwood SE, Dougal K, Newbold CJ, McEwan NR. Strong stability and host specific bacterial community in faeces of ponies.. PLoS One 2013;8(9):e75079.
  20. 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 Age and Obesity.. Front Microbiol 2018;9:3017.
    doi: 10.3389/fmicb.2018.03017pmc: PMC6293011pubmed: 30581426google scholar: lookup
  21. Grimm P, Philippeau C, Julliand V. Faecal parameters as biomarkers of the equine hindgut microbial ecosystem under dietary change.. Animal 2017 Jul;11(7):1136-1145.
    doi: 10.1017/S1751731116002779pubmed: 28065211google scholar: lookup
  22. Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes. FEMS Microbiol Ecol 2001;38:141–151.
  23. Shepherd ML, Swecker WS Jr, Jensen RV, Ponder MA. Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons.. FEMS Microbiol Lett 2012 Jan;326(1):62-8.
  24. Costa MC, Stämpfli HR, Allen-Vercoe E, Weese JS. Development of the faecal microbiota in foals.. Equine Vet J 2016 Nov;48(6):681-688.
    doi: 10.1111/evj.12532pubmed: 26518456google scholar: lookup
  25. Costa MC, Stämpfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs.. BMC Vet Res 2015 Feb 3;11:19.
    doi: 10.1186/s12917-015-0335-7pmc: PMC4323147pubmed: 25644524google scholar: lookup
  26. Rodriguez C, Taminiau B, Brévers B, Avesani V, Van Broeck J, Leroux A, Gallot M, Bruwier A, Amory H, Delmée M, Daube G. Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of clostridium difficile at hospital admission.. BMC Microbiol 2015 Sep 16;15:181.
    doi: 10.1186/s12866-015-0514-5pmc: PMC4573688pubmed: 26377067google scholar: lookup
  27. Fernandes KA, Kittelmann S, Rogers CW, Gee EK, Bolwell CF, Bermingham EN, Thomas DG. Faecal microbiota of forage-fed horses in New Zealand and the population dynamics of microbial communities following dietary change.. PLoS One 2014;9(11):e112846.
  28. Steelman SM, Chowdhary BP, Dowd S, Suchodolski J, Janečka JE. Pyrosequencing of 16S rRNA genes in fecal samples reveals high diversity of hindgut microflora in horses and potential links to chronic laminitis.. BMC Vet Res 2012 Nov 27;8:231.
    doi: 10.1186/1746-6148-8-231pmc: PMC3538718pubmed: 23186268google scholar: lookup
  29. Dougal K, Harris PA, Girdwood SE, Creevey CJ, Curtis GC, Barfoot CF, Argo CM, Newbold CJ. Changes in the Total Fecal Bacterial Population in Individual Horses Maintained on a Restricted Diet Over 6 Weeks.. Front Microbiol 2017;8:1502.
    doi: 10.3389/fmicb.2017.01502pmc: PMC5554519pubmed: 28848517google scholar: lookup
  30. 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.
  31. 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.
  32. Liu X, Fan H, Ding X, Hong Z, Nei Y, Liu Z, Li G, Guo H. Analysis of the gut microbiota by high-throughput sequencing of the V5-V6 regions of the 16S rRNA gene in donkey.. Curr Microbiol 2014 May;68(5):657-62.
    doi: 10.1007/s00284-014-0528-5pubmed: 24452427google scholar: lookup
  33. Gao H, Chi X, Qin W, Wang L, Song P, Cai Z, Zhang J, Zhang T. Comparison of the gut microbiota composition between the wild and captive Tibetan wild ass (Equus kiang).. J Appl Microbiol 2019 Jun;126(6):1869-1878.
    doi: 10.1111/jam.14240pmc: PMC6849810pubmed: 30825354google scholar: lookup
  34. Jónsson H, Schubert M, Seguin-Orlando A, Ginolhac A, Petersen L, Fumagalli M, Albrechtsen A, Petersen B, Korneliussen TS, Vilstrup JT, Lear T, Myka JL, Lundquist J, Miller DC, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, Stagegaard J, Strauss G, Bertelsen MF, Sicheritz-Ponten T, Antczak DF, Bailey E, Nielsen R, Willerslev E, Orlando L. Speciation with gene flow in equids despite extensive chromosomal plasticity.. Proc Natl Acad Sci U S A 2014 Dec 30;111(52):18655-60.
    doi: 10.1073/pnas.1412627111pmc: PMC4284605pubmed: 25453089google scholar: lookup
  35. 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.
  36. 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.
  37. 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
  38. Warnick TA, Methé BA, Leschine SB. Clostridium phytofermentans sp. nov., a cellulolytic mesophile from forest soil.. Int J Syst Evol Microbiol 2002 Jul;52(Pt 4):1155-1160.
    doi: 10.1099/00207713-52-4-1155pubmed: 12148621google scholar: lookup
  39. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia.. Environ Microbiol 2013 Oct;15(10):2631-41.
    pmc: PMC4056668pubmed: 23834245doi: 10.1111/1462-2920.12173google scholar: lookup
  40. Petit E, Coppi MV, Hayes JC, Tolonen AC, Warnick T, Latouf WG, Amisano D, Biddle A, Mukherjee S, Ivanova N, Lykidis A, Land M, Hauser L, Kyrpides N, Henrissat B, Lau J, Schnell DJ, Church GM, Leschine SB, Blanchard JL. Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels.. PLoS One 2015;10(6):e0118285.
  41. Seshadri R, Leahy SC, Attwood GT, Teh KH, Lambie SC, Cookson AL, Eloe-Fadrosh EA, Pavlopoulos GA, Hadjithomas M, Varghese NJ, Paez-Espino D, Perry R, Henderson G, Creevey CJ, Terrapon N, Lapebie P, Drula E, Lombard V, Rubin E, Kyrpides NC, Henrissat B, Woyke T, Ivanova NN, Kelly WJ. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection.. Nat Biotechnol 2018 Apr;36(4):359-367.
    doi: 10.1038/nbt.4110pmc: PMC6118326pubmed: 29553575google scholar: lookup
  42. Nyonyo T, Shinkai T, Mitsumori M. Improved culturability of cellulolytic rumen bacteria and phylogenetic diversity of culturable cellulolytic and xylanolytic bacteria newly isolated from the bovine rumen.. FEMS Microbiol Ecol 2014 Jun;88(3):528-37.
    doi: 10.1111/1574-6941.12318pubmed: 24612331google scholar: lookup
  43. Nyonyo T, Shinkai T, Tajima A, Mitsumori M. Effect of media composition, including gelling agents, on isolation of previously uncultured rumen bacteria.. Lett Appl Microbiol 2013 Jan;56(1):63-70.
    doi: 10.1111/lam.12019pubmed: 23106798google scholar: lookup
  44. Kenters N, Henderson G, Jeyanathan J, Kittelmann S, Janssen PH. Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium.. J Microbiol Methods 2011 Jan;84(1):52-60.
    doi: 10.1016/j.mimet.2010.10.011pubmed: 21034781google scholar: lookup
  45. Hanafy RA, Elshahed MS, Youssef NH. Feramyces austinii, gen. nov., sp. nov., an anaerobic gut fungus from rumen and fecal samples of wild Barbary sheep and fallow deer.. Mycologia 2018 May-Jun;110(3):513-525.
    doi: 10.1080/00275514.2018.1466610pubmed: 29969376google scholar: lookup
  46. Edwards JE, Hermes GDA, Kittelmann S, Nijsse B, Smidt H. Assessment of the Accuracy of High-Throughput Sequencing of the ITS1 Region of Neocallimastigomycota for Community Composition Analysis.. Front Microbiol 2019;10:2370.
    doi: 10.3389/fmicb.2019.02370pmc: PMC6813465pubmed: 31681229google scholar: lookup
  47. Koetschan C, Kittelmann S, Lu J, Al-Halbouni D, Jarvis GN, Müller T, Wolf M, Janssen PH. Internal transcribed spacer 1 secondary structure analysis reveals a common core throughout the anaerobic fungi (Neocallimastigomycota).. PLoS One 2014;9(3):e91928.
  48. Kittelmann S, Naylor GE, Koolaard JP, Janssen PH. A proposed taxonomy of anaerobic fungi (class neocallimastigomycetes) suitable for large-scale sequence-based community structure analysis.. PLoS One 2012;7(5):e36866.
  49. Fliegerová K, Mrázek J, Hoffmann K, Zábranská J, Voigt K. Diversity of anaerobic fungi within cow manure determined by ITS1 analysis.. Folia Microbiol (Praha) 2010 Jul;55(4):319-25.
    doi: 10.1007/s12223-010-0049-ypubmed: 20680562google scholar: lookup
  50. Mura E, Edwards J, Kittelmann S, Kaerger K, Voigt K, Mrázek J, Moniello G, Fliegerova K. Anaerobic fungal communities differ along the horse digestive tract.. Fungal Biol 2019 Mar;123(3):240-246.
    doi: 10.1016/j.funbio.2018.12.004pubmed: 30798879google scholar: lookup
  51. Liggenstoffer AS, Youssef NH, Couger MB, Elshahed MS. Phylogenetic diversity and community structure of anaerobic gut fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores.. ISME J 2010 Oct;4(10):1225-35.
    doi: 10.1038/ismej.2010.49pubmed: 20410935google scholar: lookup
  52. Gold JJ, Heath IB, Bauchop T. Ultrastructural description of a new chytrid genus of caecum anaerobe, Caecomyces equi gen. nov., sp. nov., assigned to the Neocallimasticaceae.. Biosystems 1988;21(3-4):403-15.
    doi: 10.1016/0303-2647(88)90039-1pubmed: 3395694google scholar: lookup
  53. Orpin CG. Isolation of cellulolytic phycomycete fungi from the caecum of the horse.. J Gen Microbiol 1981 Apr;123(2):287-96.
    doi: 10.1099/00221287-123-2-287pubmed: 7033458google scholar: lookup
  54. Li J, Heath IB, Bauchop T. Piromyces mae and Piromyces dumbonica , two new species of uniflagellate anaerobic chytridiomycete fungi from the hindgut of the horse and elephant. Can J Bot 1990;68:1021–1033.
    doi: 10.1139/b90-129google scholar: lookup
  55. Gaillard-Martinie B, Breton A, Dusser M, Julliand V. Piromyces citronii sp. nov., a strictly anaerobic fungus from the equine caecum: a morphological, metabolic, and ultrastructural study. FEMS Microbiol Lett 1995;130:321–326.
  56. Callaghan TM, Podmirseg SM, Hohlweck D, Edwards JE, Puniya AK, Dagar SS. Buwchfawromyces eastonii gen. nov., sp. nov.: a new anaerobic fungus (Neocallimastigomycota) isolated from buffalo faeces. MycoKeys 2015;9:11–28.
    doi: 10.3897/mycokeys.9.9032google scholar: lookup
  57. Francis-Smith K, Wood-Gush DG. Coprophagia as seen in thoroughbred foals.. Equine Vet J 1977 Jul;9(3):155-7.
  58. Marinier SL, Alexander AJ. Coprophagy as an avenue for foals of the domestic horse to learn food preferences from their dams. J Theor Biol 1995;173:121–124.
    doi: 10.1006/jtbi.1995.0049google scholar: lookup
  59. van Lingen HJ, Edwards JE, Vaidya JD, van Gastelen S, Saccenti E, van den Bogert B, Bannink A, Smidt H, Plugge CM, Dijkstra J. Diurnal Dynamics of Gaseous and Dissolved Metabolites and Microbiota Composition in the Bovine Rumen.. Front Microbiol 2017;8:425.
    pmc: PMC5355475pubmed: 28367142doi: 10.3389/fmicb.2017.00425google scholar: lookup
  60. Lane D. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Wiley: New York; 1991. pp. 115–148.
  61. Suzuki MT, Taylor LT, DeLong EF. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays.. Appl Environ Microbiol 2000 Nov;66(11):4605-14.
  62. Dojka MA, Hugenholtz P, Haack SK, Pace NR. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation.. Appl Environ Microbiol 1998 Oct;64(10):3869-77.
  63. Edwards JE, Kingston-Smith AH, Jimenez HR, Huws SA, Skøt KP, Griffith GW, McEwan NR, Theodorou MK. Dynamics of initial colonization of nonconserved perennial ryegrass by anaerobic fungi in the bovine rumen.. FEMS Microbiol Ecol 2008 Dec;66(3):537-45.
  64. Dollhofer V, Callaghan TM, Griffith GW, Lebuhn M, Bauer J. Presence and transcriptional activity of anaerobic fungi in agricultural biogas plants.. Bioresour Technol 2017 Jul;235:131-139.
  65. Ramiro-Garcia J, Hermes GDA, Giatsis C, Sipkema D, Zoetendal EG, Schaap PJ, Smidt H. NG-Tax, a highly accurate and validated pipeline for analysis of 16S rRNA amplicons from complex biomes.. F1000Res 2016;5:1791.
  66. Poncheewin W, Hermes GDA, van Dam JCJ, Koehorst JJ, Smidt H, Schaap PJ. NG-Tax 2.0: A Semantic Framework for High-Throughput Amplicon Analysis.. Front Genet 2019;10:1366.
    pmc: PMC6989550pubmed: 32117417doi: 10.3389/fgene.2019.01366google scholar: lookup
  67. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.. Nucleic Acids Res 2013 Jan;41(Database issue):D590-6.
    doi: 10.1093/nar/gks1219pmc: PMC3531112pubmed: 23193283google scholar: lookup
  68. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2013.
  69. Neuwirth E. RColorBrewer: ColorBrewer palettes. R package version 1.1–2. 2014.
  70. Milton Bache S, Wickham H. magrittr: a forward-pipe operator for R. R package version 1.5. 2014.
  71. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
  72. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. Picante: R tools for integrating phylogenies and ecology.. Bioinformatics 2010 Jun 1;26(11):1463-4.
    doi: 10.1093/bioinformatics/btq166pubmed: 20395285google scholar: lookup
  73. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. _nlme: linear and nonlinear mixed effects models_. R package version 3.1–131. 2017.
  74. Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D. vegan: community ecology package. R package version 2.5–3. 2018.
  75. Deepayan S. Lattice: multivariate data visualization with R. New York: Springer; 2008.
  76. Simpson GL. permute: functions for generating restricted permutations of data. 2016.
  77. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language.. Bioinformatics 2004 Jan 22;20(2):289-90.
    doi: 10.1093/bioinformatics/btg412pubmed: 14734327google scholar: lookup
  78. Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2016.
  79. Kassambara A. ggpubr: “ggplot2” based publication ready plots. R package version 0.2.
  80. 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
  81. Šmilauer P, Leps J. Multivariate analysis of ecological data using Canoco 5. 2. New York: Cambridge University Press; 2014.

Citations

This article has been cited 8 times.
  1. Indraningrat AAG, Steinert G, Becking LE, Mueller B, de Goeij JM, Smidt H, Sipkema D. Sponge holobionts shift their prokaryotic communities and antimicrobial activity from shallow to lower mesophotic depths.. Antonie Van Leeuwenhoek 2022 Oct;115(10):1265-1283.
    doi: 10.1007/s10482-022-01770-4pubmed: 35998007google scholar: lookup
  2. Cui X, Zhang Q, Zhang Q, Zhang Y, Chen H, Liu G, Zhu L. Research Progress of the Gut Microbiome in Hybrid Fish.. Microorganisms 2022 Apr 24;10(5).
  3. Zhang Z, Huang B, Shi X, Wang T, Wang Y, Zhu M, Wang C. Comparative Analysis of Bacterial Diversity between the Liquid Phase and Adherent Fraction within the Donkey Caeco-Colic Ecosystem.. Animals (Basel) 2022 Apr 26;12(9).
    doi: 10.3390/ani12091116pubmed: 35565542google scholar: lookup
  4. Zhang Z, Wang Y, Huang B, Zhu M, Wang C. The Fibrolytic Enzyme Profiles and the Composition of Fungal Communities in Donkey Cecum-Colon Ecosystem.. Animals (Basel) 2022 Feb 9;12(4).
    doi: 10.3390/ani12040412pubmed: 35203120google scholar: lookup
  5. Miller AK, Westlake CS, Cross KL, Leigh BA, Bordenstein SR. The microbiome impacts host hybridization and speciation.. PLoS Biol 2021 Oct;19(10):e3001417.
    doi: 10.1371/journal.pbio.3001417pubmed: 34699520google scholar: lookup
  6. Laustsen L, Edwards JE, Hermes GDA, Lúthersson N, van Doorn DA, Okrathok S, Kujawa TJ, Smidt H. Free Faecal Water: Analysis of Horse Faecal Microbiota and the Impact of Faecal Microbial Transplantation on Symptom Severity.. Animals (Basel) 2021 Sep 23;11(10).
    doi: 10.3390/ani11102776pubmed: 34679798google scholar: lookup
  7. Cross KL, Leigh BA, Hatmaker EA, Mikaelyan A, Miller AK, Bordenstein SR. Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown.. mSystems 2021 Apr 6;6(2).
    doi: 10.1128/mSystems.01342-20pubmed: 33824199google scholar: lookup
  8. Cersosimo LM, Sullivan KE, Valdes EV. Species and individual rhinoceros affect the bacterial communities, metabolites, and nutrient composition in faeces from Southern black rhinoceros (Diceros bicornis minor) and Southern white rhinoceros (Ceratotherium simum simum) under managed care.. J Anim Physiol Anim Nutr (Berl) 2022 Jan;106(1):181-193.
    doi: 10.1111/jpn.13520pubmed: 33655648google scholar: lookup