Effect of age and the individual on the gastrointestinal bacteriome of ponies fed a high-starch diet.
Abstract: Bacteria residing in the gastrointestinal tract of mammals are crucial for the digestion of dietary nutrients. Bacterial community composition is modified by age and diet in other species. Although horses are adapted to consuming fibre-based diets, high-energy, often high-starch containing feeds are increasingly used. The current study assessed the impact of age on the faecal bacteriome of ponies transitioning from a hay-based diet to a high-starch diet. Over two years, 23 Welsh Section A pony mares were evaluated (Controls, 5-15 years, n = 6/year, 12 in total; Aged, ≥19 years, n = 6 Year 1; n = 5 Year 2, 11 in total). Across the same 30-week (May to November) period in each year, animals were randomly assigned to a 5-week period of study and were individually fed the same hay to maintenance (2% body mass as daily dry matter intake) for 4-weeks. During the final week, 2g starch per kg body mass (micronized steam-flaked barley) was incorporated into the diet (3-day transition and 5 days at maximum). Faecal samples were collected for 11 days (final 3 days hay and 8 days hay + barley feeding). Bacterial communities were determined using Ion Torrent Sequencing of amplified V1-V2 hypervariable regions of 16S rRNA. Age had a minimal effect on the bacteriome response to diet. The dietary transition increased Candidatus Saccharibacteria and Firmicutes phyla abundance and reduced Fibrobactres abundance. At the genera level, Streptococcus abundance was increased but not consistently across individual animals. Bacterial diversity was reduced during dietary transition in Streptococcus 'responders'. Faecal pH and VFA concentrations were modified by diet but considerable inter-individual variation was present. The current study describes compositional changes in the faecal bacteriome associated with the transition from a fibre-based to a high-starch diet in ponies and emphasises the individual nature of dietary responses, which may reflect functional differences in the bacterial populations present in the hindgut.
Publication Date: 2020-05-08 PubMed ID: 32384105PubMed Central: PMC7209120DOI: 10.1371/journal.pone.0232689Google 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
- 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 investigates how age influences the digestive bacteria in ponies when their diet changes from hay-based to high-starch. The study found age had little effect on bacterial response, though diet change did influence certain types of digestive bacteria, even though the response varied among individuals.
Study Design and Methodology
- The study was conducted over two years with 23 Welsh Section A pony mares divided into two groups – Controls (5-15 years, 12 in total) and Aged (≥19 years, 11 in total).
- During a 30-week period of each year, ponies were randomly assigned a 5-week study period where they were fed hay to sustain normal body mass for 4 weeks. In the final week, 2g starch per kg body mass was incorporated into the diet.
- Faecal samples were collected for 11 days (the last 3 days of hay feeding and 8 days of hay + barley feeding).
- The bacterial communities in the faecal samples were analysed using Ion Torrent Sequencing of amplified V1-V2 hypervariable regions of 16S rRNA.
Key Findings
- The effect of age on bacterial response to diet was minimal.
- The dietary transition from fibre-based to high-starch led to an increase in the abundance of Candidatus Saccharibacteria and Firmicutes phyla and a decrease in Fibrobactres abundance.
- The abundance of Streptococcus genera also increased, however, the increase was inconsistent among individual animals.
- Bacterial diversity reduced during the dietary transition in Streptococcus ‘responders’.
- The dietary change also influenced faecal pH and Volatile Fatty Acid (VFA) concentrations, although there was significant inter-individual variation.
Implications
- The study provided insights into changes in the digestive bacteria of ponies transitioning from a fibre-based to high-starch diet. While age did not bear a significant effect, the diet transition did bring certain alterations in the faecal bacteriome.
- The considerable variation in digestive responses among individuals suggests the potential presence of functional differences in the bacterial populations present in the hindgut of the ponies, emphasizing the tailored approach needed for individual diet changes.
Cite This Article
APA
Morrison PK, Newbold CJ, Jones E, Worgan HJ, Grove-White DH, Dugdale AH, Barfoot C, Harris PA, Argo CM.
(2020).
Effect of age and the individual on the gastrointestinal bacteriome of ponies fed a high-starch diet.
PLoS One, 15(5), e0232689.
https://doi.org/10.1371/journal.pone.0232689 Publication
Researcher Affiliations
- Scotland's Rural College, Aberdeen, Scotland, United Kingdom.
- Scotland's Rural College, Edinburgh, Scotland, United Kingdom.
- Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Wales, United Kingdom.
- Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Wales, United Kingdom.
- Faculty of Health and Life Sciences, University of Liverpool, Neston, Wirral, England, United Kingdom.
- ChesterGates Veterinary Specialists CVS (UK) Ltd., Chester, England, United Kingdom.
- MARS Horsecare UK Ltd, Buckinghamshire, England, United Kingdom.
- WALTHAM Petcare Science Institute, Waltham-on-the-Wolds, Leicestershire, England, United Kingdom.
- Scotland's Rural College, Aberdeen, Scotland, United Kingdom.
MeSH Terms
- Aging
- Animal Feed / analysis
- Animals
- Dietary Carbohydrates / analysis
- Dietary Carbohydrates / metabolism
- Dietary Fiber / analysis
- Dietary Fiber / metabolism
- Feces / microbiology
- Gastrointestinal Microbiome
- Glucose / metabolism
- Horses / physiology
- Insulin / metabolism
- Starch / analysis
- Starch / metabolism
Conflict of Interest Statement
Co-authors PH and CB are employed by the funding organization, WALTHAM (https://www.waltham.com/). Co-author AD is employed by ChesterGates Veterinary Specialists CVS Ltd. This does not alter our adherence to PLOS ONE policies on sharing data and materials. All other authors declare that they have no competing interests.
References
This article includes 52 references
- Janis C. THE EVOLUTIONARY STRATEGY OF THE EQUIDAE AND THE ORIGINS OF RUMEN AND CECAL DIGESTION.. Evolution 1976 Dec;30(4):757-774.
- Mihlbachler MC, Rivals F, Solounias N, Semprebon GM. Dietary change and evolution of horses in North America.. Science 2011 Mar 4;331(6021):1178-81.
- 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.
- 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.
- 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.
- Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
- Julliand V, Grimm P. The Impact of Diet on the Hindgut Microbiome. J Equine Vet Sci. 2017;52: 23u201328. 10.1016/j.jevs.2017.03.002
- De Fombelle A, Julliand V, Drogoul C, Jacotot E. Feeding and microbial disorders in horses: 1-Effects of an abrupt incorporation of two levels of barley in a hay diet on microbial profile and activities. J Equine Vet Sci. 2001;21: 439u2013445.
- 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.
- 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.
- Julliand V, de Fombelle A, Drogoul C, Jacotot E. Feeding and microbial disorders in horses: Part 3u2014Effects of three hay: grain ratios on microbial profile and activities. J Equine Vet Sci. 2001;21 10.1016/s0737-0806(01)70159-1
- Harlow BE, Donley TM, Lawrence LM, Flythe MD. Effect of starch source (corn, oats or wheat) and concentration on fermentation by equine faecal microbiota in vitro.. J Appl Microbiol 2015 Nov;119(5):1234-44.
- Julliand V, De Fombelle A, Varloud M. Starch digestion in horses: The impact of feed processing. Livest Sci. 2006;100: 44u201352. 10.1016/j.livprodsci.2005.11.001
- Philippeau C, Sadet-Bourgeteau S, Varloud M, Julliand V. Impact of barley form on equine total tract fibre digestibility and colonic microbiota.. Animal 2015 Dec;9(12):1943-8.
- Meyer H, Radicke S, Kienzle E, Wilke S, Kleffken D, Illenseer M. Investigations on preileal digestion of starch from grain, potato and manioc in horses.. Zentralbl Veterinarmed A 1995 Aug;42(6):371-81.
- Woodmansey EJ, McMurdo ME, Macfarlane GT, Macfarlane S. Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects.. Appl Environ Microbiol 2004 Oct;70(10):6113-22.
- Geor RJ, Harris P. Dietary management of obesity and insulin resistance: countering risk for laminitis.. Vet Clin North Am Equine Pract 2009 Apr;25(1):51-65, vi.
- Ireland JL, Clegg PD, McGowan CM, McKane SA, Pinchbeck GL. A cross-sectional study of geriatric horses in the United Kingdom. Part 1: Demographics and management practices.. Equine Vet J 2011 Jan;43(1):30-6.
- Mc Gowan TW, Pinchbeck GP, Mc Gowan CM. Evaluation of basal plasma u03b1-melanocyte-stimulating hormone and adrenocorticotrophic hormone concentrations for the diagnosis of pituitary pars intermedia dysfunction from a population of aged horses.. Equine Vet J 2013 Jan;45(1):66-73.
- 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.
- 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.
- Kohnke J. Feeding and Nutrition: The making of a champion. Birubi Pacific, Pymble; 1992.
- Dugdale AH, Curtis GC, Milne E, Harris PA, Argo CM. Assessment of body fat in the pony: part II. Validation of the deuterium oxide dilution technique for the measurement of body fat.. Equine Vet J 2011 Sep;43(5):562-70.
- Argo CM, Curtis GC, Grove-White D, Dugdale AH, Barfoot CF, Harris PA. Weight loss resistance: a further consideration for the nutritional management of obese Equidae.. Vet J 2012 Nov;194(2):179-88.
- Yu Z, Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples.. Biotechniques 2004 May;36(5):808-12.
- de la Fuente G, Belanche A, Girwood SE, Pinloche E, Wilkinson T, Newbold CJ. Pros and cons of ion-torrent next generation sequencing versus terminal restriction fragment length polymorphism T-RFLP for studying the rumen bacterial community.. PLoS One 2014;9(7):e101435.
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.. Appl Environ Microbiol 2009 Dec;75(23):7537-41.
- Edgar RC, Flyvbjerg H. Error filtering, pair assembly and error correction for next-generation sequencing reads.. Bioinformatics 2015 Nov 1;31(21):3476-82.
- Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.. Appl Environ Microbiol 2007 Aug;73(16):5261-7.
- Stewart CS, Duncan SH. The Effect of Avoparcin on Cellulolytic Bacteria of the Ovine Rumen. Microbiology. 1985;131: 427u2013435. 10.1099/00221287-131-3-427
- Gihring TM, Green SJ, Schadt CW. Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes.. Environ Microbiol 2012 Feb;14(2):285-90.
- Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser. 1995;57: 289u2013300.
- Frank N, Geor RJ, Bailey SR, Durham AE, Johnson PJ. Equine metabolic syndrome.. J Vet Intern Med 2010 May-Jun;24(3):467-75.
- Jaccard P. Nouvelles recherches sur la distribution florale. Bull Soc Vaud Des Sci Nat. 44: 223u2013270.
- Vital M, Harkema JR, Rizzo M, Tiedje J, Brandenberger C. Alterations of the Murine Gut Microbiome with Age and Allergic Airway Disease.. J Immunol Res 2015;2015:892568.
- Mitnitski AB, Graham JE, Mogilner AJ, Rockwood K. Frailty, fitness and late-life mortality in relation to chronological and biological age.. BMC Geriatr 2002 Feb 27;2:1.
- Maffei VJ, Kim S, Blanchard E 4th, Luo M, Jazwinski SM, Taylor CM, Welsh DA. Biological Aging and the Human Gut Microbiota.. J Gerontol A Biol Sci Med Sci 2017 Oct 12;72(11):1474-1482.
- Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease.. Br J Nutr 2012 Apr;107(7):989-95.
- Kristoffersen C, Jensen RB, Avershina E, Austbu00f8 D, Tauson AH, Rudi K. Diet-Dependent Modular Dynamic Interactions of the Equine Cecal Microbiota.. Microbes Environ 2016 Dec 23;31(4):378-386.
- Warzecha CM, Coverdale JA, Janecka JE, Leatherwood JL, Pinchak WE, Wickersham TA, McCann JC. Influence of short-term dietary starch inclusion on the equine cecal microbiome.. J Anim Sci 2017 Nov;95(11):5077-5090.
- 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.
- Petri RM, Schwaiger T, Penner GB, Beauchemin KA, Forster RJ, McKinnon JJ, McAllister TA. Characterization of the core rumen microbiome in cattle during transition from forage to concentrate as well as during and after an acidotic challenge.. PLoS One 2013;8(12):e83424.
- Khafipour E, Li S, Plaizier JC, Krause DO. Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis.. Appl Environ Microbiol 2009 Nov;75(22):7115-24.
- Li F, Guan LL. Metatranscriptomic Profiling Reveals Linkages between the Active Rumen Microbiome and Feed Efficiency in Beef Cattle.. Appl Environ Microbiol 2017 May 1;83(9).
- Huws SA, Creevey CJ, Oyama LB, Mizrahi I, Denman SE, Popova M, Muu00f1oz-Tamayo R, Forano E, Waters SM, Hess M, Tapio I, Smidt H, Krizsan SJ, Yu00e1u00f1ez-Ruiz DR, Belanche A, Guan L, Gruninger RJ, McAllister TA, Newbold CJ, Roehe R, Dewhurst RJ, Snelling TJ, Watson M, Suen G, Hart EH, Kingston-Smith AH, Scollan ND, do Prado RM, Pilau EJ, Mantovani HC, Attwood GT, Edwards JE, McEwan NR, Morrisson S, Mayorga OL, Elliott C, Morgavi DP. Addressing Global Ruminant Agricultural Challenges Through Understanding the Rumen Microbiome: Past, Present, and Future.. Front Microbiol 2018;9:2161.
- Philippeau C, Varloud M, Julliand V. Mobile bag starch prececal disappearance and postprandial glycemic response of four forms of barley in horses.. J Anim Sci 2014 May;92(5):2087-93.
- Murray J-AMD, Longland A, Moore-Colyer M, Dunnett C, Longland A. The effect of feeding a low- or high-starch diet on equine faecal parameters. Livest Sci. 2014;159: 67u201370. 10.1016/j.livsci.2013.10.017
- Heiman ML, Greenway FL. A healthy gastrointestinal microbiome is dependent on dietary diversity.. Mol Metab 2016 May;5(5):317-320.
- Julliand V, Grimm P. The Impact of Diet on the Hindgut Microbiome. J Equine Vet Sci. 2017;52: 23u201328. 10.1016/j.jevs.2017.03.002
- Destrez A, Grimm P, Julliand V. Dietary-induced modulation of the hindgut microbiota is related to behavioral responses during stressful events in horses.. Physiol Behav 2019 Apr 1;202:94-100.
- 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.
- 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.