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Effect of feeding raw potato starch on the composition dynamics of the piglet intestinal microbiome

  • Yi, Seung-Won (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • Lee, Han Gyu (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • So, Kyoung-Min (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • Kim, Eunju (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • Jung, Young-Hun (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • Kim, Minji (Animal Nutrition and Physiology Division, National Institute of Animal Science, Rural Development Administration) ;
  • Jeong, Jin Young (Animal Nutrition and Physiology Division, National Institute of Animal Science, Rural Development Administration) ;
  • Kim, Ki Hyun (Animal Welfare Research Team, National Institute of Animal Science, Rural Development Administration) ;
  • Oem, Jae-Ku (Laboratory of Veterinary Infectious Disease, College of Veterinary Medicine, Jeonbuk National University) ;
  • Hur, Tai-Young (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration) ;
  • Oh, Sang-Ik (Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration)
  • 투고 : 2022.01.28
  • 심사 : 2022.07.04
  • 발행 : 2022.11.01

초록

Objective: Raw potato starch (RPS) is resistant to digestion, escapes absorption, and is metabolized by intestinal microflora in the large intestine and acts as their energy source. In this study, we compared the effect of different concentrations of RPS on the intestinal bacterial community of weaned piglets. Methods: Male weaned piglets (25-days-old, 7.03±0.49 kg) were either fed a corn/soybean-based control diet (CON, n = 6) or two treatment diets supplemented with 5% RPS (RPS5, n = 4) or 10% RPS (RPS10, n = 4) for 20 days and their fecal samples were collected. The day 0 and 20 samples were analyzed using a 16S rRNA gene sequencing technology, followed by total genomic DNA extraction, library construction, and high-throughput sequencing. After statistical analysis, five phyla and 45 genera accounting for over 0.5% of the reads in any of the three groups were further analyzed. Furthermore, short-chain fatty acids (SCFAs) in the day 20 fecal samples were analyzed using gas chromatography. Results: Significant changes were not observed in the bacterial composition at the phylum level even after 20 d post feeding (dpf); however, the abundance of Intestinimonas and Barnesiella decreased in both RPS treatment groups compared to the CON group. Consumption of 5% RPS increased the abundance of Roseburia (p<0.05) and decreased the abundance of Clostridium (p<0.01) and Mediterraneibacter (p< 0.05). In contrast, consumption of 10% RPS increased the abundance of Olsenella (p<0.05) and decreased the abundance of Campylobacter (p<0.05), Kineothrix (p<0.05), Paraprevotella (p<0.05), and Vallitalea (p<0.05). Additionally, acetate (p<0.01), butyrate (p<0.05), valerate (p = 0.01), and total SCFAs (p = 0.01) were upregulated in the RPS5 treatment group Conclusion: Feeding 5% RPS altered bacterial community composition and promoted gut health in weaned piglets. Thus, resistant starch as a feed additive may prevent diarrhea in piglets during weaning.

키워드

과제정보

This study was supported by the 2021 RDA Fellowship Program of the National Institute of Animal Science, Rural Development Administration, and was carried out with the support of the "Cooperative Research Program for Agriculture Science and Technology Development (Project title: Development of gut microbiota for preventing intestinal diseases and its impact on host immunity in pigs, Project No. PJ01564401)", Rural Development Administration, Republic of Korea.

참고문헌

  1. Baumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature 2016;535: 85-93. https://doi.org/10.1038/nature18849
  2. Mach N, Berri M, Estelle J, et al. Early-life establishment of the swine gut microbiome and impact on host phenotypes. Environ Microbiol Rep 2015;7:554-69. https://doi.org/10.1111/1758-2229.12285
  3. Campbell JM, Crenshaw JD, Polo J. The biological stress of early weaned piglets. J Anim Sci Biotechnol 2013;4:19. https://doi.org/10.1186/2049-1891-4-19
  4. Gresse R, Chaucheyras-Durand F, Fleury MA, Van de Wiele T, Forano E, Blanquet-Diot S. Gut microbiota dysbiosis in postweaning piglets: Understanding the keys to health. Trends Microbiol 2017;25:851-73. https://doi.org/10.1016/j.tim.2017.05.004
  5. Moeser AJ, Pohl CS, Rajput M. Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Anim Nutr 2017;3:313-21. https://doi.org/10.1016/j.aninu.2017.06.003
  6. Hermann-Bank ML, Skovgaard K, Stockmarr A, et al. Characterization of the bacterial gut microbiota of piglets suffering from new neonatal porcine diarrhoea. BMC Vet Res 2015;11:139. https://doi.org/10.1186/s12917-015-0419-4
  7. Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ, Nyachoti CM. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr (Berl). 2013;97:207-37. https://doi.org/10.1111/j.1439-0396.2012.01284.x
  8. Aarestrup FM, Jensen VF, Emborg HD, Jacobsen E, Wegener HC. Changes in the use of antimicrobials and the effects on productivity of swine farms in Denmark. Am J Vet Res 2010;71:726-33. https://doi.org/10.2460/ajvr.71.7.726
  9. Zhao J, Bai Y, Tao S, et al. Fiber-rich foods affected gut bacterial community and short-chain fatty acids production in pig model. J Funct Foods 2019;57:266-74. https://doi.org/10.1016/j.jff.2019.04.009
  10. Champ MM. Physiological aspects of resistant starch and in vivo measurements. J AOAC Int 2004;87:749-55. https://doi.org/10.1093/jaoac/87.3.749
  11. Trachsel J, Briggs C, Gabler NK, Allen HK, Loving CL. Dietary resistant potato starch alters intestinal microbial communities and their metabolites, and markers of immune regulation and barrier function in swine. Front Immunol 2019;10:1381. https://doi.org/10.3389/fimmu.2019.01381
  12. Gerrits WJ, Bosch MW, van den Borne JJ. Quantifying resistant starch using novel, in vivo methodology and the energetic utilization of fermented starch in pigs. J Nutr 2012;142:238-44. https://doi.org/10.3945/jn.111.147496
  13. Regmi PR, Metzler-Zebeli BU, Ganzle MG, van Kempen TATG, Zijlstra RT. Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes Bifidobacteria in pigs. J Nutr 2011;141:1273-80. https://doi.org/10.3945/jn.111.140509
  14. Nielsen TS, Laerke HN, Theil PK, et al. Diets high in resistant starch and arabinoxylan modulate digestion processes and scfa pool size in the large intestine and faecal microbial composition in pigs. Br J Nutr 2014;112:1837-49. https://doi.org/10.1017/S000711451400302X
  15. Guo L, Zhang D, Fu S, et al. Metagenomic sequencing analysis of the effects of colistin sulfate on the pig gut microbiome. Front Vet Sci 2021;8:663820. https://doi.org/10.3389/fvets.2021.663820
  16. Fang L, Jiang X, Su Y, Zhu W. Long-term intake of raw potato starch decreases back fat thickness and dressing percentage but has no effect on the longissimus muscle quality of growing-finishing pigs. Livest Sci 2014;170:116-23. https://doi.org/10.1016/j.livsci.2014.10.004
  17. Bang SJ, Lee ES, Song EJ, et al. Effect of raw potato starch on the gut microbiome and metabolome in mice. Int J Biol Macromol 2019;133:37-43. https://doi.org/10.1016/j.ijbiomac.2019.04.085
  18. Hughes RL, Horn WH, Finnegan P, et al. Resistant starch type 2 from wheat reduces postprandial glycemic response with concurrent alterations in gut microbiota composition. Nutrients 2021;13:645. https://doi.org/10.3390/nu13020645
  19. Pauly C, Spring P, O'Doherty JV, Kragten SA, Bee G. Performances, meat quality and boar taint of castrates and entire male pigs fed a standard and a raw potato starch-enriched diet. Animal 2008;2:1707-15. https://doi.org/10.1017/S1751731108002826
  20. Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: A tool for visualizing high-throughput microbial community data. GigaScience 2013;2:16. https://doi.org/10.1186/2047-217X-2-16
  21. Zhang D, Liu H, Wang S, et al. Fecal microbiota and its correlation with fatty acids and free amino acids metabolism in piglets after a Lactobacillus strain oral administration. Front Micobiol 2019:10:785. https://doi.org/10.3389/fmicb.2019.00785
  22. Bindelle J, Leterme P, Buldgen A. Nutritional and environmental consequences of dietary fibre in pig nutrition: a review. Biotechnol Agron Soc Environ 2008;12:69-80.
  23. Sun Y, Su Y, Zhu W. Microbiome-metabolome responses in the cecum and colon of pig to a high resistant starch diet. Front Microbiol 2016;7:779. https://doi.org/10.3389/fmicb.2016.00779
  24. Hedemann MS, Bach Knudsen KEB. Resistant starch for weaning pigs: effect on concentration of short chain fatty acids in digesta and intestinal morphology. Livest Sci 2007; 108:175-7. https://doi.org/10.1016/j.livsci.2007.01.045
  25. Sun Y, Zhou L, Fang L, Su Y, Zhu W. Responses in colonic microbial community and gene expression of pigs to a longterm high resistant starch diet. Front Microbiol 2015;6:877. https://doi.org/10.3389/fmicb.2015.00877
  26. Zhou L, Fang L, Sun Y, Su Y, Zhu W. Effects of a diet high in resistant starch on fermentation end-products of protein and mucin secretion in the colons of pigs. Starch-Starke; 2017;69:1600032. https://doi.org/10.1002/star.201600032
  27. Ding X, Lan W, Liu G, Ni H, Gu JD. Exploring possible associations of the intestine bacterial microbiome with the preweaned weight gaining performance of piglets in intensive pig production. Sci Rep 2019;9:15534. https://doi.org/10.1038/s41598-019-52045-4
  28. 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; 177:242-51. https://doi.org/10.1016/j.vetmic.2015.03.014
  29. Han GG, Lee JY, Jin GD, et al. Evaluating the association between body weight and the intestinal microbiota of weaned piglets via 16S rRNA sequencing. Appl Microbiol Biotechnol 2017;101:5903-11. https://doi.org/10.1007/s00253-017-8304-7
  30. Kemp JA, Regis de Paiva B, Fragoso Dos Santos H, et al. The impact of enriched resistant starch type-2 cookies on the gut microbiome in hemodialysis patients: a randomized controlled trial. Mol Nutr Food Res 2021;65:2100374. https://doi.org/10.1002/mnfr.202100374
  31. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: The role of butyrate on colonic function. Aliment Pharmacol Ther 2008;27:104-19. https://doi.org/10.1111/j.1365-2036.2007.03562.x
  32. Kraatz M, Wallace RJ, Svensson L. Olsenella umbonata sp. nov., a microaerotolerant anaerobic lactic acid bacterium from the sheep rumen and pig jejunum, and emended descriptions of Olsenella, Olsenella uli and Olsenella profusa. Int J Syst Evol Microbiol 2011;61:795-803. https://doi.org/10.1099/ijs.0.022954-0
  33. Li X, Jensen RL, Hojberg O, Canibe N, Jensen BB. Olsenella scatoligenes sp. Nov., a 3-methylindole-(skatole) and 4-methylphenol-(p-cresol) producing bacterium isolated from pig faeces. Int J Syst Evol Microbiol 2015;65:1227-33. https://doi.org/10.1099/ijs.0.000083
  34. Long SF, Xu YT, Pan L, et al. Mixed organic acids as antibiotic substitutes improve performance, serum immunity, intestinal morphology and microbiota for weaned piglets. Anim Feed Sci Technol 2018;235:23-32. https://doi.org/10.1016/j.anifeedsci.2017.08.018
  35. Hasan S, Saha S, Junnikkala S, Orro T, Peltoniemi O, Oliviero C. Late gestation diet supplementation of resin acid-enriched composition increases sow colostrum immunoglobulin G content, piglet colostrum intake and improve sow gut microbiota. Animal 2018;13:1599-606. https://doi.org/10.1017/S1751731118003518
  36. Ruzauskas M, Bartkiene E, Stankevicius A, et al. The influence of essential oils on gut microbial profiles in pigs. Animals (Basel) 2020;10:1734. https://doi.org/10.3390/ani10101734
  37. Wylensek D, Hitch TCA, Riedel T, et al. A collection of bacterial isolates from pig intestines revealed functional and taxonomic diversity. Nat Commun 2020;11:6389. https://doi.org/10.1038/s41467-020-19929-w
  38. Morotomi M, Nagai F, Sakon H, Tanaka R. Dialister succinatiphilus sp. Nov. and Barnesiella intestinihominis sp. Nov., isolated from human faeces. Int J Syst Evol Microbiol 2008; 58:2716-20. https://doi.org/10.1099/ijs.0.2008/000810-0
  39. Bui TPN, Ritari J, Boeren S, Plugge CM, de Vos WM. Production of butyrate from lysine and the amadori product fructoselysine by a human gut commensal. Nat Commun 2015;6:10062. https://doi.org/10.1038/ncomms10062
  40. Kumar H, Jang YN, Kim K, Park J, Jung MW, Park JE. Compositional and functional characteristics of swine slurry microbes through 16S rRNA metagenomic sequencing approach. Animals 2020;10:1372. https://doi.org/10.3390/ani10081372
  41. Torres-Pitarch A, Gardiner GE, Cormican P, et al. Effect of cereal soaking and carbohydrase supplementation on growth, nutrient digestibility and intestinal microbiota in liquid-fed grow-finishing pigs. Sci Rep 2020;10:1023. https://doi.org/10.1038/s41598-020-57668-6
  42. Casas GA, Blavi L, Cross TWL, Lee AH, Swanson KS, Stein HH. Inclusion of the direct-fed microbial Clostridium butyricum in diets for weanling pigs increases growth performance and tends to increase villus height and crypt depth, but does not change intestinal microbial abundance. J Anim Sci 2020;98:skz372. https://doi.org/10.1093/jas/skz372
  43. Hu X, Lin B, Luo M, Zheng X, Zhang H. The isolation, identification, physiological property of pig-isolate Clostridium butyricum ly33 using lactic acid and its effects on intestinal function of weaned piglets. Ital J Anim Sci 2019;18:910-21. https://doi.org/10.1080/1828051X.2019.1603089
  44. Liu P, Zhao J, Wang W, et al. Dietary corn bran altered the diversity of microbial communities and cytokine production in weaned pigs. Front Microbiol 2018;9:2090. https://doi.org/10.3389/fmicb.2018.02090
  45. Zhang J, Chen X, Liu P, et al. Dietary Clostridium butyricum induces a phased shift in fecal microbiota structure and increases the acetic acid-producing bacteria in a weaned piglet model. J Agric Food Chem 2018;66:5157-66. https://doi.org/10.1021/acs.jafc.8b01253
  46. Jin M, Kalainy S, Baskota N, et al. Faecal microbiota from patients with cirrhosis has a low capacity to ferment nondigestible carbohydrates into short-chain fatty acids. Liver Int 2019;39:1437-47. https://doi.org/10.1111/liv.14106
  47. Togo AH, Diop A, Bittar F, et al. Description of Mediterraneibacter massiliensis, gen. nov., sp. nov., a new genus isolated from the gut microbiota of an obese patient and reclassification of Ruminococcus faecis, Ruminococcus lactaris, Ruminococcus torques, Ruminococcus gnavus and Clostridium glycyrrhizinilyticum as Mediterraneibacter faecis comb. nov., Mediterraneibacter lactaris comb. nov., Mediterraneibacter torques comb. nov., Mediterraneibacter gnavus comb. nov. and Mediterraneibacter glycyrrhizinilyticus comb. nov. Antonie van Leeuwenhoek 2018;111:2107-28. https://doi.org/10.1007/s10482-018-1104-y
  48. Levesque S, Lemay F, Bekal S, Frost EH, Michaud S. First reported case of Campylobacter lanienae enteritis in a human. JMM Case Rep 2016;3:e005045. https://doi.org/10.1099/jmmcr.0.005045
  49. Burrough E, Terhorst S, Sahin O, Zhang Q. Prevalence of campylobacter spp. Relative to other enteric pathogens in grow-finish pigs with diarrhea. Anaerobe 2013;22:111-4. https://doi.org/10.1016/j.anaerobe.2013.06.004
  50. Ben Aissa FB, Postec A, Erauso G, et al. Vallitalea pronyensis sp. Nov., isolated from a marine alkaline hydrothermal chimney. Int J Syst Evol Microbiol 2014;64:1160-5. https://doi.org/10.1099/ijs.0.055756-0
  51. Haas KN, Blanchard JL. Kineothrix alysoides, gen. Nov., sp. nov., a saccharolytic butyrate-producer within the family Lachnospiraceae. Int J Syst Evol Microbiol 2017;67:402-10. https://doi.org/10.1099/ijsem.0.001643
  52. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Moller K. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 2002;68:673-90. https://doi.org/10.1128/AEM.68.2.673-690.2002
  53. Morotomi M, Nagai F, Sakon H, Tanaka R. Paraprevotella clara gen. Nov., sp. Nov. and Paraprevotella xylaniphila sp. Nov., members of the family 'Prevotellaceae' isolated from human faeces. Int J Syst Evol Microbiol 2009;59:1895-900. https://doi.org/10.1099/ijs.0.008169-0
  54. Schouw A, Leiknes Eide TL, Stokke R, Pedersen RB, Steen IH, Bodtker G. Abyssivirga alkaniphila gen. Nov., sp. Nov., an alkane-degrading, anaerobic bacterium from a deep-sea hydrothermal vent system, and emended descriptions of Natranaerovirga pectinivora and Natranaerovirga hydrolytica. Int J Syst Evol Microbiol 2016;66:1724-34. https://doi.org/10.1099/ijsem.0.000934
  55. Climent E, Martinez-Blanch JF, Llobregat L, et al. Changes in gut microbiota correlates with response to treatment with probiotics in patients with atopic dermatitis. A post hoc analysis of a clinical trial. Microorganisms 2021;9:854. https://doi.org/10.3390/microorganisms9040854
  56. Poco Jr SE, Nakazawa F, Sato M, Hoshino E. Eubacterium minutum sp. Nov., isolated from human periodontal pockets. Int J Syst Bacteriol 1996;46:31-4. https://doi.org/10.1099/00207713-46-1-31