1887

Graphical Abstract

Graphical abstract

Microbiota of healthy dogs demonstrate significant changes in specific bacterial groups in response to supplementation with resistant starch (but not psyllium or methylcellulose) in this randomized cross-over trial.

Abstract

Even though dietary fibres are often used as prebiotic supplements in dogs, the effect of individual types of fibres on canine microbiota composition is unknown. The objective of this study was to assess changes in faecal microbiota richness, diversity and taxonomic abundance with three different fibre supplements in dogs. These were psyllium husk, resistant starch from banana flour and methylcellulose. They were administered to 17 healthy dogs in a cross-over trial after transition to the same complete feed. Faecal scores and clinical activity indices were recorded, and faecal samples were collected before and at the end of supplementation, as well as 2 weeks after each supplement (washout). Illumina NovaSeq paired-end 16S rRNA gene sequencing was performed on all samples. After quality control and chimera removal, alpha diversity indices were calculated with QIIME. Differences in specific taxa between groups were identified using Metastats. Methylcellulose significantly increased faecal scores but had no effect on microbiota. Psyllium resulted in minor changes in the abundance of specific taxa, but with questionable biological significance. Resistant starch reduced microbiota richness and resulted in the most abundant changes in taxa, mostly a reduction in short-chain fatty acid-producing genera of the phylum , with an increase in genera within the , , and . In conclusion, while psyllium and methylcellulose led to few changes in the microbiota composition, the taxonomic changes seen with resistant starch may indicate a less favourable composition. Based on this, the type of resistant starch used here cannot be recommended as a prebiotic in dogs.

Funding
This study was supported by the:
  • Comparative Gastroenterology Society (Award n/a)
    • Principle Award Recipient: SilkeSalavati Schmitz
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/D/30002276)
    • Principle Award Recipient: LauraGlendinning
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/RL/230001C)
    • Principle Award Recipient: LauraGlendinning
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article is published under the Publish and Read agreement
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000774.v4
2024-05-14
2024-05-20
Loading full text...

Full text loading...

/deliver/fulltext/acmi/6/5/acmi000774.v4.html?itemId=/content/journal/acmi/10.1099/acmi.0.000774.v4&mimeType=html&fmt=ahah

References

  1. Makki K, Deehan EC, Walter J, Bäckhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 2018; 23:705–715 [View Article] [PubMed]
    [Google Scholar]
  2. Loke YL, Chew MT, Ngeow YF, Lim WWD, Peh SC. Colon carcinogenesis: the interplay between diet and gut microbiota. Front Cell Infect Microbiol 2020; 10:603086 [View Article] [PubMed]
    [Google Scholar]
  3. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 2017; 14:491–502 [View Article] [PubMed]
    [Google Scholar]
  4. Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol 2020; 17:687–701 [View Article] [PubMed]
    [Google Scholar]
  5. Stephen AM, Champ MM-J, Cloran SJ, Fleith M, van Lieshout L et al. Dietary fibre in Europe: current state of knowledge on definitions, sources, recommendations, intakes and relationships to health. Nutr Res Rev 2017; 30:149–190 [View Article] [PubMed]
    [Google Scholar]
  6. Martínez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS One 2010; 5:e15046 [View Article] [PubMed]
    [Google Scholar]
  7. Chassard C, Delmas E, Robert C, Bernalier-Donadille A. The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens. FEMS Microbiol Ecol 2010; 74:205–213 [View Article] [PubMed]
    [Google Scholar]
  8. Gamage HKAH, Tetu SG, Chong RWW, Bucio-Noble D, Rosewarne CP et al. Fiber supplements derived from sugarcane stem, wheat dextrin and psyllium husk have different in vitro effects on the human gut microbiota. Front Microbiol 2018; 9:1618 [View Article] [PubMed]
    [Google Scholar]
  9. Cox LM, Cho I, Young SA, Anderson WHK, Waters BJ et al. The nonfermentable dietary fiber hydroxypropyl methylcellulose modulates intestinal microbiota. FASEB J 2013; 27:692–702 [View Article] [PubMed]
    [Google Scholar]
  10. Coelho LP, Kultima JR, Costea PI, Fournier C, Pan Y et al. Similarity of the dog and human gut microbiomes in gene content and response to diet. Microbiome 2018; 6:72 [View Article] [PubMed]
    [Google Scholar]
  11. Hernandez J, Rhimi S, Kriaa A, Mariaule V, Boudaya H et al. Domestic environment and gut microbiota: lessons from pet dogs. Microorganisms 2022; 10:949 [View Article] [PubMed]
    [Google Scholar]
  12. Reese AT, Chadaideh KS, Diggins CE, Schell LD, Beckel M et al. Effects of domestication on the gut microbiota parallel those of human industrialization. Elife 2021; 10:e60197 [View Article] [PubMed]
    [Google Scholar]
  13. Cerquetella M, Spaterna A, Laus F, Tesei B, Rossi G et al. Inflammatory bowel disease in the dog: differences and similarities with humans. World J Gastroenterol 2010; 16:1050–1056 [View Article] [PubMed]
    [Google Scholar]
  14. Fritsch DA, Wernimont SM, Jackson MI, MacLeay JM, Gross KL. A prospective multicenter study of the efficacy of a fiber-supplemented dietary intervention in dogs with chronic large bowel diarrhea. BMC Vet Res 2022; 18:244 [View Article] [PubMed]
    [Google Scholar]
  15. Lappin MR, Zug A, Hovenga C, Gagne J, Cross E. Efficacy of feeding a diet containing a high concentration of mixed fiber sources for management of acute large bowel diarrhea in dogs in shelters. J Vet Intern Med 2022; 36:488–492 [View Article] [PubMed]
    [Google Scholar]
  16. Mackei M, Talabér R, Müller L, Sterczer Á, Fébel H et al. Altered intestinal production of volatile fatty acids in dogs triggered by Lactulose and Psyllium treatment. Vet Sci 2022; 9:206 [View Article] [PubMed]
    [Google Scholar]
  17. Bretin A, Zou J, San Yeoh B, Ngo VL, Winer S et al. Psyllium fiber protects against colitis via activation of bile acid sensor farnesoid X receptor. Cell Mol Gastroenterol Hepatol 2023; 15:1421–1442 [View Article] [PubMed]
    [Google Scholar]
  18. Guard BC, Honneffer JB, Jergens AE, Jonika MM, Toresson L et al. Longitudinal assessment of microbial dysbiosis, fecal unconjugated bile acid concentrations, and disease activity in dogs with steroid-responsive chronic inflammatory enteropathy. J Vet Intern Med 2019; 33:1295–1305 [View Article] [PubMed]
    [Google Scholar]
  19. Jergens AE, Schreiner CA, Frank DE, Niyo Y, Ahrens FE et al. A scoring index for disease activity in canine inflammatory bowel disease. J Vet Intern Med 2003; 17:291–297 [View Article] [PubMed]
    [Google Scholar]
  20. Washabau RJ, Hall JA. Canine and Feline Gastroenterology. In Washabau RJ, Day MJ. eds Canine and Feline Gastroenterology, 1st. edn Louis, Missouri, USA: Saunders Elsevier; 2013 pp 1–937
    [Google Scholar]
  21. Glendinning L, Wright S, Pollock J, Tennant P, Collie D et al. Variability of the sheep lung microbiota. Appl Environ Microbiol 2016; 82:3225–3238 [View Article] [PubMed]
    [Google Scholar]
  22. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011; 27:2957–2963 [View Article] [PubMed]
    [Google Scholar]
  23. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 2013; 10:57–59 [View Article] [PubMed]
    [Google Scholar]
  24. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335–336 [View Article] [PubMed]
    [Google Scholar]
  25. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011; 27:2194–2200 [View Article] [PubMed]
    [Google Scholar]
  26. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–D596 [View Article] [PubMed]
    [Google Scholar]
  27. White JR, Nagarajan N, Pop M. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 2009; 5:e1000352 [View Article] [PubMed]
    [Google Scholar]
  28. AlShawaqfeh MK, Wajid B, Minamoto Y, Markel M, Lidbury JA et al. A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy. FEMS Microbiol Ecol 2017; 93:136 [View Article] [PubMed]
    [Google Scholar]
  29. Martínez-López LM, Pepper A, Pilla R, Woodward AP, Suchodolski JS et al. Effect of sequentially fed high protein, hydrolyzed protein, and high fiber diets on the fecal microbiota of healthy dogs: a cross-over study. Anim Microbiome 2021; 3:42 [View Article] [PubMed]
    [Google Scholar]
  30. Bermudez Sanchez S, Pilla R, Sarawichitr B, Gramenzi A, Marsilio F et al. Fecal microbiota in client-owned obese dogs changes after weight loss with a high-fiber-high-protein diet. PeerJ 2020; 8:e9706 [View Article] [PubMed]
    [Google Scholar]
  31. Jewell DE, Jackson MI, Cochrane C-Y, Badri DV. Feeding fiber-bound polyphenol ingredients at different levels modulates colonic postbiotics to improve gut health in dogs. Animals 2022; 12:627 [View Article] [PubMed]
    [Google Scholar]
  32. Palmqvist H, Ringmark S, Höglund K, Pelve E, Lundh T et al. Effects of rye inclusion in dog food on fecal microbiota and short-chain fatty acids. BMC Vet Res 2023; 19:70 [View Article] [PubMed]
    [Google Scholar]
  33. Finet S, He F, Clark LV, de Godoy MRC. Functional properties of miscanthus fiber and prebiotic blends in extruded canine diets. J Anim Sci 2022; 100:skac078 [View Article] [PubMed]
    [Google Scholar]
  34. Song H, Lee J, Yi S, Kim W-H, Kim Y et al. Red ginseng dietary fiber shows prebiotic potential by modulating gut microbiota in dogs. Microbiol Spectr 2023; 11:e0094923 [View Article] [PubMed]
    [Google Scholar]
  35. Rudinsky AJ, Parker VJ, Winston J, Cooper E, Mathie T et al. Randomized controlled trial demonstrates nutritional management is superior to metronidazole for treatment of acute colitis in dogs. J Am Vet Med Assoc 2022; 260:S23–S32 [View Article] [PubMed]
    [Google Scholar]
  36. Alves JC, Santos A, Jorge P, Pitães A. The use of soluble fibre for the management of chronic idiopathic large-bowel diarrhoea in police working dogs. BMC Vet Res 2021; 17:100 [View Article] [PubMed]
    [Google Scholar]
  37. Hamilton JW, Wagner J, Burdick BB, Bass P. Clinical evaluation of methylcellulose as a bulk laxative. Dig Dis Sci 1988; 33:993–998 [View Article] [PubMed]
    [Google Scholar]
  38. Bowman JP. The genus Psychrobacter. Prokaryotes 2006920–930 [View Article]
    [Google Scholar]
  39. Korneev KV, Kondakova AN, Arbatsky NP, Novototskaya-Vlasova KA, Rivkina EM et al. Distinct biological activity of lipopolysaccharides with different lipid A acylation status from mutant strains of Yersinia pestis and some members of genus Psychrobacter. Biochemistry 2014; 79:1333–1338 [View Article] [PubMed]
    [Google Scholar]
  40. Kou Y, Xu X, Zhu Z, Dai L, Tan Y. Microbe-set enrichment analysis facilitates functional interpretation of microbiome profiling data. Sci Rep 2020; 10:21466 [View Article] [PubMed]
    [Google Scholar]
  41. Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR et al. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 2020; 38:685–688 [View Article] [PubMed]
    [Google Scholar]
  42. Beloshapka AN, Cross TWL, Swanson KS. Graded dietary resistant starch concentrations on apparent total tract macronutrient digestibility and fecal fermentative end products and microbial populations of healthy adult dogs. J Anim Sci 2021; 99:1–11 [View Article] [PubMed]
    [Google Scholar]
  43. Muñoz M, Guerrero-Araya E, Cortés-Tapia C, Plaza-Garrido A, Lawley TD et al. Comprehensive genome analyses of Sellimonas intestinalis, a potential biomarker of homeostasis gut recovery. Microb Genom 2020; 6:mgen000476 [View Article] [PubMed]
    [Google Scholar]
  44. Stege PB, Hordijk J, Sandholt AKS, Zomer AL, Viveen MC et al. Gut colonization by ESBL-producing Escherichia coli in dogs is associated with a distinct microbiome and resistome composition. Microbiol Spectr 2023; 11:e0006323 [View Article] [PubMed]
    [Google Scholar]
  45. Wang J-L, Han X, Li J-X, Shi R, Liu L-L et al. Differential analysis of intestinal microbiota and metabolites in mice with dextran sulfate sodium-induced colitis. World J Gastroenterol 2022; 28:6109–6130 [View Article] [PubMed]
    [Google Scholar]
  46. Mukherjee A, Lordan C, Ross RP, Cotter PD. Gut microbes from the phylogenetically diverse genus Eubacterium and their various contributions to gut health. Gut Microbes 2020; 12:1802866 [View Article] [PubMed]
    [Google Scholar]
  47. Gaukroger CH, Stewart CJ, Edwards SA, Walshaw J, Adams IP et al. Changes in faecal microbiota profiles associated with performance and birthweight of piglets. Front Microbiol 2020; 11:917 [View Article] [PubMed]
    [Google Scholar]
  48. Pessoa J, Belew GD, Barroso C, Egas C, Jones JG. The gut microbiome responds progressively to fat and/or sugar-rich diets and is differentially modified by dietary fat and sugar. Nutrients 2023; 15:2097 [View Article] [PubMed]
    [Google Scholar]
  49. Tavella T, Rampelli S, Guidarelli G, Bazzocchi A, Gasperini C et al. Elevated gut microbiome abundance of Christensenellaceae, Porphyromonadaceae and Rikenellaceae is associated with reduced visceral adipose tissue and healthier metabolic profile in Italian elderly. Gut Microbes 2021; 13:1–19 [View Article] [PubMed]
    [Google Scholar]
  50. Yang T, Ahmari N, Schmidt JT, Redler T, Arocha R et al. Shifts in the gut microbiota composition due to depleted bone marrow beta adrenergic signaling are associated with suppressed inflammatory transcriptional networks in the mouse colon. Front Physiol 2017; 8:220 [View Article] [PubMed]
    [Google Scholar]
  51. Suchodolski JS, Xenoulis PG, Paddock CG, Steiner JM, Jergens AE. Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet Microbiol 2010; 142:394–400 [View Article] [PubMed]
    [Google Scholar]
  52. Oba PM, Carroll MQ, Alexander C, Valentine H, Somrak AJ et al. Microbiota populations in supragingival plaque, subgingival plaque, and saliva habitats of adult dogs. Anim Microbiome 2021; 3:38 [View Article] [PubMed]
    [Google Scholar]
  53. Brereton NJB, Gonzalez E, Desjardins D, Labrecque M, Pitre FE. Co-cropping with three phytoremediation crops influences rhizosphere microbiome community in contaminated soil. Sci Total Environ 2020; 711:135067 [View Article] [PubMed]
    [Google Scholar]
  54. Ayangbenro AS, Babalola OO. Reclamation of arid and semi-arid soils: the role of plant growth-promoting archaea and bacteria. Cur Plant Biol 2021; 25:100173 [View Article]
    [Google Scholar]
  55. Gryaznova M, Dvoretskaya Y, Burakova I, Syromyatnikov M, Popov E et al. Dynamics of changes in the gut microbiota of healthy mice fed with lactic acid bacteria and bifidobacteria. Microorganisms 2022; 10:1020 [View Article] [PubMed]
    [Google Scholar]
  56. Chen Y-R, Jing Q-L, Chen F-L, Zheng H, Chen L-D et al. Desulfovibrio is not always associated with adverse health effects in the guangdong gut microbiome project. PeerJ 2021; 9:e12033 [View Article] [PubMed]
    [Google Scholar]
  57. Le PH, Chiu CT, Yeh PJ, Pan YB, Chiu CH. Clostridium innocuum infection in hospitalised patients with inflammatory bowel disease. J Infect 2022; 84:337–342 [View Article] [PubMed]
    [Google Scholar]
  58. Remely M, Hippe B, Zanner J, Aumueller E, Brath H et al. Gut microbiota of obese, type 2 diabetic individuals is enriched in Faecalibacterium prausnitzii, Akkermansia muciniphila and Peptostreptococcus anaerobius after weight loss. Endocr Metab Immune Disord Drug Targets 2016; 16:99–106 [View Article] [PubMed]
    [Google Scholar]
  59. Hendrickson EL, Bor B, Kerns KA, Lamont EI, Chang Y et al. Transcriptome of epibiont Saccharibacteria Nanosynbacter lyticus strain TM7x during the establishment of symbiosis. J Bacteriol 2022; 204:e0011222 [View Article] [PubMed]
    [Google Scholar]
  60. Zhou X, Wang J-T, Zhang Z-F, Li W, Chen W et al. Microbiota in the rhizosphere and seed of rice From China, with reference to their transmission and biogeography. Front Microbiol 2020; 11:995 [View Article] [PubMed]
    [Google Scholar]
  61. Cordovez V, Schop S, Hordijk K, Dupré de Boulois H, Coppens F et al. Priming of plant growth promotion by volatiles of root-associated Microbacterium spp. Appl Environ Microbiol 2018; 84:e01865-18 [View Article] [PubMed]
    [Google Scholar]
  62. Oliynyk M, Samborskyy M, Lester JB, Mironenko T, Scott N et al. Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat Biotechnol 2007; 25:447–453 [View Article] [PubMed]
    [Google Scholar]
  63. Amabebe E, Anumba DOC. Female gut and genital tract microbiota-induced crosstalk and differential effects of short-chain fatty acids on immune sequelae. Front Immunol 2020; 11:2184 [View Article] [PubMed]
    [Google Scholar]
  64. Pollock J, Glendinning L, Wisedchanwet T, Watson M. The madness of microbiome: attempting to find consensus “Best Practice” for 16S microbiome studies. Appl Environ Microbiol 2018; 84:e02627-17 [View Article] [PubMed]
    [Google Scholar]
  65. Roume H, Mondot S, Saliou A, Le Fresne-Languille S, Doré J. Multicenter evaluation of gut microbiome profiling by next-generation sequencing reveals major biases in partial-length metabarcoding approach. Sci Rep 2023; 13:22593 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000774.v4
Loading
/content/journal/acmi/10.1099/acmi.0.000774.v4
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error