antibiotics; growth performance; gut microbiota; weaned piglets; xylo-oligosaccharides; Microbiology
Abstract :
[en] Xylo-oligosaccharides (XOS) is a well-known kind of oligosaccharide and extensively applied as a prebiotic. The objective of this study was to investigate the effect of XOS supplementation substituting chlortetracycline (CTC) on growth, gut morphology, gut microbiota, and hindgut short chain fatty acid (SCFA) contents of weaning piglets. A total of 180 weaned piglets were randomly allocated to three treatments for 28 days, as follows: control group (basal diet, CON), basal diet with 500 mg/kg (XOS500) XOS, and positive control (basal diet with 100 mg/kg CTC). Compared with the CON group, the piglets in the XOS500 group improved body weight (BW) on days 28, average daily gain (ADG) and reduced feed: gain ratio during days 1-28 (P < 0.05). The XOS500 supplementation increased Villus height and Villus height: Crypt depth ratio in the ileum (P < 0.05). Villus Height: Crypt Depth of the ileum was also increased in the CTC treatment group (P < 0.05). Meanwhile, the XOS500 supplementation increased significantly the numbers of goblet cells in the crypt of the cecum. High-throughput 16S rRNA gene sequencing revealed distinct differences in microbial compositions between the ileum and cecum. XOS500 supplementation significantly increased the bacterial diversity. However, CTC treatment markedly reduced the microbial diversity (P < 0.05). Meanwhile, XOS500 supplementation in the diet significantly increased the abundance of Lactobacillus genus compared to the CON and CTC group in the ileum and cecum (P < 0.01), whereas the level of Clostridium_sensu_stricto_1, Escherichia-Shigella, and Terrisporobacter genus in the XOS500 group were markedly lower than the CON and CTC group (P < 0.05). In addition, dietary supplementation with XOS500 significantly increased the total short-chain fatty acids, propionate and butyrate concentrations and decreased the acetate concentration compared to the CON group in the cecum (P < 0.05). In summary, dietary supplemented with XOS500 could enhance specific beneficial microbiota abundance and decrease harmful microbiota abundance to maintain the structure of the intestinal morphology and improve growth performance of weaned piglets. Thus, XOS may potentially function as an alternative to in-feed antibiotics in weaned piglets in modern husbandry.
Disciplines :
Microbiology
Author, co-author :
Chen, Yuxia ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Xie, Yining; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China ; School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Lei; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Lin, Changguang; Institute of Animal Husbandry and Veterinary Medicine, Fujian Academy of Agriculture Sciences, Fuzhou, China
Xiao, Lin; Shandong Longlive Bio-Technology Co., Ltd., Yucheng, China
Chen, Liang; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Beckers, Yves ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition
Everaert, Nadia ; Université de Liège - ULiège > Département GxABT
Language :
English
Title :
Effects of Xylo-Oligosaccharides on Growth and Gut Microbiota as Potential Replacements for Antibiotic in Weaning Piglets.
This project was supported by the National Natural Science Foundation (31702119) and the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202006-02, ASTIPIAS07) in China.
Alizadeh A., Akbari P., Difilippo E., Schols H. A., Ulfman L. H., Schoterman M. H. C., et al. (2015). The piglet as a model for studying dietary components in infant diets: effects of galacto-oligosaccharides on intestinal functions. Brit. J. Nutr. 115 605–618. 10.1017/s0007114515004997 26653138
Callaway T. R., Edrington T. S., Anderson R. C., Harvey R. B., Genovese K. J., Kennedy C. N., et al. (2008). Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim. Health Res. Rev. 9 217–225. 10.1017/s1466252308001540 19102792
Carney E. F., (2015). Protective role of gut microbial SCFAs. Nat. Rev. Nephrol. 11 127–127. 10.1038/nrneph.2015.10 25643665
Cheng M. P., Domingo M.-C., Lévesque S., Yansouni C. P., (2016). A case report of a deep surgical site infection with Terrisporobacter glycolicus/T. Mayombei and review of the literature. BMC Infect. Dis. 16:529. 10.1186/s12879-016-1865-8 27686579
Choe D. W., Loh T. C., Foo H. L., Hair-Bejo M., Awis Q. S., (2012). Egg production, faecal pH and microbial population, small intestine morphology, and plasma and yolk cholesterol in laying hens given liquid metabolites produced byLactobacillus plantarumstrains. Brit. Poultry Sci. 53 106–115. 10.1080/00071668.2012.659653 22404811
Christensen E. G., Licht T. R., Leser T. D., Bahl M. I., (2014). Dietary Xylo-oligosaccharide stimulates intestinal bifidobacteria and lactobacilli but has limited effect on intestinal integrity in rats. BMC Res. Notes 19:660. 10.1186/1756-0500-7-660 25238818
Cromwell G. L., (2002). Why and how antibiotics are used in swine production. Anim. Biotechnol. 13 7–27. 10.1081/ABIO-120005767 12212945
De Maesschalck C., Eeckhaut V., Maertens L., De Lange L., Marchal L., Nezer C., et al. (2015). Effects of xylo-oligosaccharides on broiler chicken performance and microbiota. Appl. Environ. Microbiol. 81 5880–5888. 10.1128/AEM.01616-15 26092452
Den Besten G., Lange K., Havinga R., van Dijk T. H., Gerding A., van Eunen K., et al. (2013a). Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am. J. Physiol. Gastr. L 305 G900–G910. 10.1152/ajpgi.00265.2013 24136789
Den Besten G., van Eunen K., Groen A. K., Venema K., Reijngoud D. J., Bakker B. M., (2013b). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54 2325–2340. 10.1194/jlr.R036012 23821742
Deng Y., Guo X., Wang Y., He M., Ruan Z., (2015). Terrisporobacter petrolearius sp. nov., isolated from an oilfield petroleum reservoir. Int. J. Syst. Evol. Micr. 65:3522. 10.1099/ijsem.0.000450 26297478
Ding X., Li D., Bai S., Wang J., Zeng Q., Su Z., et al. (2017). Effect of dietary xylooligosaccharides on intestinal characteristics, gut microbiota, cecal short-chain fatty acids, and plasma immune parameters of laying hens. Poultry Sci. 97 874–881. 10.3382/ps/pex372 29294100
Dumonceaux T. J., Hill J. E., Hemmingsen S. M., Van Kessel A. G., (2006). Characterization of intestinal microbiota and response to dietary virginiamycin supplementation in the broiler chicken. Appl. Environ. Microbiol. 72 2815–2823. 10.1128/AEM.72.4.2815-2823.2006 16597987
Duncan S. H., Louis P., Thomson J. M., Flint H. J., (2009). The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 11 2112–2122. 10.1111/j.1462-2920.2009.01931.x 19397676
Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R., (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 2194–2200. 10.1093/bioinformatics/btr381 21700674
Erwin E., Marco G., Emery E., (1961). Volatile fatty acid analyses of blood and rumen fluid by gas chromatography. J. Dairy Sci. 44 1768–1771. 10.3168/jds.S0022-0302(61)89956-6
Espey M. G., (2013). Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota. Free Radic. Biol. Med. 55 130–140. 10.1016/j.freeradbiomed.2012.10.554 23127782
Gibson G. R., Hutkins R., Sanders M. E., Prescott S. L., Reimer R. A., Salminen S. J., et al. (2017). Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastro. Hepat. 14 491–502. 10.1038/nrgastro.2017.75 28611480
Gobinath D., Madhu A. N., Prashant G., Srinivasan K., Prapulla S. G., (2010). Beneficial effect of xylo-oligosaccharides and fructo-oligosaccharides in streptozotocin-induced diabetic rats. Brit. J. Nutr. 104:40. 10.1017/S0007114510000243 20187988
Gresse R., Chaucheyras-Durand F., Fleury M. A., Van de Wiele T., Forano E., Blanquet-Diot S., (2017). Gut Microbiota Dysbiosis in Postweaning Piglets: Understanding the Keys to Health. Trends Microbiol. 25 851–873. 10.1016/j.tim.2017.05.004 28602521
Groher A., Weuster-Botz D., (2016). Comparative reaction engineering analysis of different acetogenic bacteria for gas fermentation. J. Biotechnol. 228 82–94. 10.1016/j.jbiotec.2016.04.032 27107467
Herrero-Fresno A., Zachariasen C., Hansen M. H., Nielsen A., Hendriksen R. S., Nielsen S. S., et al. (2016). Apramycin treatment affects selection and spread of a multidrug-resistant Escherichia coli strain able to colonize the human gut in the intestinal microbiota of pigs. Vet. Res. 47:12. 10.1186/s13567-015-0291-z 26739225
Hu Q., Liu C., Zhang D., Wang R., Gao F., (2020). Effects of Low-Dose Antibiotics on Gut Immunity and Antibiotic Resistomes in Weaned Piglets. Front. Immunol. 11:903. 10.3389/fimmu.2020.00903 32655541
Huang W., Zhou L., Guo H., Xu Y., Xu Y., (2017). The role of short-chain fatty acids in kidney injury induced by gut-derived inflammatory response. Metabolism 68 20–30. 10.1016/j.metabol.2016.11.006 28183450
Kim H. B., Borewicz K., White B. A., Singer R. S., Sreevatsan S., Tu Z. J., et al. (2012). Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc. Natl. Acad. Sci. U S A. 109 15485–15490. 10.1073/pnas.1205147109 22955886
Klampfer L., Huang J., Sasazuki T., Shirasawa S., Augenlicht L., (2003). Inhibition of interferon gamma signaling by the short chain fatty acid butyrate. Mol. Cancer Res. 1 855–862. 10.1091/mbc.E02-12-0784 12972576
Knecht H., Neulinger S. C., Heinsen F. A., Knecht C., Schilhabel A., Schmitz R. A., et al. (2014). Effects of beta-lactam antibiotics and fluoroquinolones on human gut microbiota in relation to Clostridium difficile associated diarrhea. PLoS One 9:e89417. 10.1371/journal.pone.0089417 24586762
Kravtsov E. G., Yermolayev A. V., Anokhina I. V., Yashina N. V., Chesnokova V. L., Dalin M. V., (2008). Adhesion characteristics of lactobacillus is a criterion of the probiotic choice. Bull. Exp. Biol. Med. 145 232–234. 10.1007/s10517-008-0058-x 19023977
Layden B. T., Angueira A. R., Brodsky M., Durai V., Lowe W. L., Jr. (2013). Short chain fatty acids and their receptors: new metabolic targets. Transl. Res. 161 131–140. 10.1016/j.trsl.2012.10.007 23146568
Lecerf J.-M., Dépeint F., Clerc E., Dugenet Y., Niamba C. N., Rhazi L., et al. (2012). Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties. Brit. J. Nutr. 108 1847–1858. 10.1017/s0007114511007252 22264499
Li Y., Lu X., Wu H., Xia M., Hou Q., Hu W., et al. (2019). The effect of dietary supplementation of low crude protein on intestinal morphology in pigs. Res. Vet. Sci. 122 15–21. 10.1016/j.rvsc.2018.11.013 30447500
Lin J., (2011). Effect of antibiotic growth promoters on intestinal microbiota in food animals: a novel model for studying the relationship between gut microbiota and human obesity? Front. Microbiol. 2:53. 10.3389/fmicb.2011.00053 21833309
Liu J., Cao S., Liu J., Xie Y., Zhang H., (2018). Effect of probiotics and xylo-oligosaccharide supplementation on nutrient digestibility, intestinal health and noxious gas emission in weanling pigs. Asian Austr. J. Anim. Sci. 31 1660–1669. 10.5713/ajas.17.0908 29642680
Looft T., Allen H. K., Cantarel B. L., Levine U. Y., Bayles D. O., Alt D. P., et al. (2014). Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J. 8:1566. 10.1038/ismej.2014.12 24522263
Lukić I., Getselter D., Ziv O., Oron O., Reuveni E., Koren O., et al. (2019). Antidepressants affect gut microbiota and Ruminococcus flavefaciens is able to abolish their effects on depressive-like behavior. Transl. Psychiat. 9:133. 10.1038/s41398-019-0466-x 30967529
Mair C., Plitzner C., Domig K. J., Schedle K., Windisch W., (2010). Impact of inulin and a multispecies probiotic formulation on performance, microbial ecology and concomitant fermentation patterns in newly weaned piglets. J. Anim. Physiol. Anim. Nutr. 94 164–177e. 10.1111/j.1439-0396.2010.01000.x 20579190
Mikkelsen L. L., Jensen B. B., (2004). Effect of fructo-oligosaccharides and transgalacto-oligosaccharides on microbial populations and microbial activity in the gastrointestinal tract of piglets post-weaning. Anim. Feed Sci. Tech. 117 0–119. 10.1016/j.anifeedsci.2004.07.015
Mikkelsen L. L., Jakobsen M., Jensen B. B., (2003). Effects of dietary oligosaccharides on microbial diversity and fructo-oligosaccharide degrading bacteria in faeces of piglets post-weaning. Anim. Feed Sci. Tech. 109 133–150. 10.1016/S0377-8401(03)00172-X
Neuman H., Forsythe P., Uzan A., Avni O., Koren O., (2018). Antibiotics in early life: dysbiosis and the damage done. FEMS Microbiol. Rev. 42 489–499. 10.1093/femsre/fuy018 29945240
Pan L., Farouk M., Qin G., Zhao Y., Bao N., (2018). The Influences of Soybean Agglutinin and Functional Oligosaccharides on the Intestinal Tract of Monogastric Animals. Int. J. Mol. Sci. 19:19020554 10.3390/ijms19020554 29439523
Pfaffl M. W., (2001). A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29:e45. 10.1093/nar/29.9.e45 11328886
Pourabedin M., Guan L., Zhao X., (2015). Xylo-oligosaccharides and virginiamycin differentially modulate gut microbial composition in chickens. Microbiome 3:15. 10.1186/s40168-015-0079-4 25874109
Samanta A. K., Jayapal N., Jayaram C., Roy S., Kolte A. P., Senani S., et al. (2015). Xylooligosaccharides as prebiotics from agricultural by-products: Production and applications. Bioact. Carbohydr. Diet. Fibre 5 62–71. 10.1016/j.bcdf.2014.12.003
Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 7537–7541. 10.1128/AEM.01541-09 19801464
Shatos M. A., Ri′os J. D., Horikawa Y., Hodges R. R., Chang E. L., Bernardino C. R., et al. (2003). Isolation and Characterization of Cultured Human Conjunctival Goblet Cells. Investig. Ophthalmol. Vis. Sci. 44:550. 10.1167/iovs.02-0550 12766046
Silva J. P. B., Navegantes-Lima K. C., Oliveira A. L. B., Rodrigues D. V. S., Gaspar S. L. F., Monteiro V. V. S., et al. (2018). Protective Mechanisms of Butyrate on Inflammatory Bowel Disease. Curr. Pharm. Des. 24 4154–4166. 10.2174/1381612824666181001153605 30277149
Smith M. G., Jordan D., Chapman T. A., Chin J. C., Barton M. D., Do T. N., et al. (2010). Antimicrobial resistance and virulence gene profiles in multi-drug resistant enterotoxigenic Escherichia coli isolated from pigs with post-weaning diarrhoea. Vet. Microbiol. 145 299–307. 10.1016/j.vetmic.2010.04.004 20688440
Strobel S., Encarnação J., Becker N., Trenczek T., (2015). Histological and histochemical analysis of the gastrointestinal tract of the common pipistrelle bat (Pipistrellus pipistrellus). Eur. J. Histochem. 59:2477. 10.4081/ejh.2015.2477 26150154
Suo C., Yin Y., Wang X., Lou X., Song D., Wang X., et al. (2012). Effects of lactobacillus plantarum ZJ316 on pig growth and pork quality. BMC Vet. Res. 8:89. 10.1186/1746-6148-8-89 22731747
Toutain P. L., Ferran A. A., Bousquet-Melou A., Pelligand L., Lees P., (2016). Veterinary Medicine Needs New Green Antimicrobial Drugs. Front. Microbiol. 7:1196. 10.3389/fmicb.2016.01196 27536285
Wang R. X., Lee J. S., Campbell E. L., Colgan S. P., (2020). Microbiota-derived butyrate dynamically regulates intestinal homeostasis through regulation of actin-associated protein synaptopodin. PNAS 117 11648–11657. 10.1073/pnas.1917597117 32398370
Wang T., Teng K., Liu Y., Shi W., Zhang J., Dong E., et al. (2019). Lactobacillus plantarum PFM 105 Promotes Intestinal Development Through Modulation of Gut Microbiota in Weaning Piglets. Front. Microbiol. 10:90. 10.3389/fmicb.2019.00090 30804899
Wang W., Van Noten N., Degroote J., Romeo A., Vermeir P., Michiels J., (2019). Effect of zinc oxide sources and dosages on gut microbiota and integrity of weaned piglets. J. Anim. Physiol. Anim. Nutr. 103 231–241. 10.1111/jpn.12999 30298533
Wang Y., Xu C., Zhang R., Chen Y., Shen Y., Hu F., et al. (2020). Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: an epidemiological comparative study. Lancet Infect. Dis. 20 1161–1171. 10.1016/s1473-3099(20)30149-3
Wang Y., Xu L., Liu J., Zhu W., Mao S., (2017). A high grain diet dynamically shifted the composition of mucosa-associated microbiota and induced mucosal injuries in the colon of sheep. Front. Microbiol. 8:2080. 10.3389/fmicb.2017.02080 29123511
Wijtten P. J., van der Meulen J., Verstegen M. W., (2011). Intestinal barrier function and absorption in pigs after weaning: a review. Brit. J. Nutr. 105 967–981. 10.1017/S0007114510005660 21303573
Yang J., Summanen P., Henning S., Hsu M., Lam H., Huang J., et al. (2015). Xylooligosaccharide supplementation alters gut bacteria in both healthy and prediabetic adults: a pilot study. Front. Physiol. 6:216. 10.3389/fphys.2015.00216 26300782
Yi H. B., Yang Z. D., Xiong Y. X., Wen X. L., Wang Z. L., Yand X. F., et al. (2018). Effects of Lactobacillus reuteri LR1 on the growth performance, intestinal morphology, and intestinal barrier function in weaned pigs. J. Anim. Sci. 96 2342–2351. 10.1093/jas/sky129/4969323 29659876
Yin J., Li F., Kong X., Wen C., Guo Q., Zhang L., et al. (2019). Dietary xylo-oligosaccharide improves intestinal functions in weaned piglets. Food Funct. 10 2701–2709. 10.1039/c8fo02485e 31025998
Yuan L., Li W., Huo Q., Du C., Wang Z., Yi B., et al. (2018). Effects of xylo-oligosaccharide and flavomycin on the immune function of broiler chickens. PeerJ 6:e4435. 10.7717/peerj.4435 29527412
Zhang D., Ji H., Liu H., Wang S., Wang J., Wang Y., (2016). Changes in the diversity and composition of gut microbiota of weaned piglets after oral administration of Lactobacillus or an antibiotic. Appl. Microbiol. Biot. 100 10081–10093. 10.1007/s00253-016-7845-5 27757509
Zhang L., Wu W., Lee Y. K., Xie J., Zhang H., (2018). Spatial Heterogeneity and Co-occurrence of Mucosal and Luminal Microbiome across Swine Intestinal Tract. Front. Microbiol. 9:48. 10.3389/fmicb.2018.00048 29472900
Zhao P. Y., Jung J. H., Kim I. H., (2012). Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. J. Anim. Sci. 90:833. 10.2527/jas.2011-3921 21984718