Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T13:34:22.630Z Has data issue: false hasContentIssue false
  • English
  • Français

Antibiotic-induced alterations of the gut microbiota and microbial fermentation in protein parallel the changes in host nitrogen metabolism of growing pigs

Published online by Cambridge University Press:  29 June 2018

Y. Pi ,
K. Gao ,
Y. Peng ,
C. L. Mu  and
W. Y. Zhu
Y. Pi
Affiliation:
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China National Center for International Research on Animal Gut Nutrition, Nanjing Agricultural University, Nanjing, 210095, China
K. Gao
Affiliation:
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China National Center for International Research on Animal Gut Nutrition, Nanjing Agricultural University, Nanjing, 210095, China
Y. Peng
Affiliation:
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China National Center for International Research on Animal Gut Nutrition, Nanjing Agricultural University, Nanjing, 210095, China
C. L. Mu
Affiliation:
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China National Center for International Research on Animal Gut Nutrition, Nanjing Agricultural University, Nanjing, 210095, China
W. Y. Zhu*
Affiliation:
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China National Center for International Research on Animal Gut Nutrition, Nanjing Agricultural University, Nanjing, 210095, China
*
†E-mail: [email protected]
Get access

Abstract

Gut microbes, especially those in the large intestine, are actively involved in nutrient metabolism; however, their impact on host nitrogen (N) metabolism remains largely unknown. This study was designed to investigate the effects of feeding a cocktail of antibiotics (AGM) (ampicillin, gentamycin and metronidazole) on intestinal microbiota, N utilization efficiency, and amino acid (AA) digestibility in cannulated pigs, with the aim of exploring the impact of gut microbiota on host N metabolism. In total, 16 piglets were surgically fitted with a simple distal ileal T-cannula and a jugular venous catheter. The pigs were fed a basal diet without antibiotics (control; CON) or with antibiotics (antibiotic; ANTI), for 2 weeks. The results showed that feeding AGM did not affect weight gain or digestive enzyme activity. The antibiotics increased the concentration of urea N (P<0.05). However, they reduced N utilization, and the total tract apparent digestibility of isoleucine, methionine, valine, tyrosine and total AA (P<0.05). Furthermore, the antibiotics increased the terminal ileum apparent digestibility of CP, phenylalanine, valine, alanine, tyrosine and total AA (P<0.05). AGM markedly altered the composition of the microbiota in the ileum and feces, with a reduction in populations of Bifidobacterium, Lactobacillus and Ruminococcus, and an increase in the abundance of Escherichia coli (P<0.05). The antibiotics also significantly increased the concentration of cadaverine and ammonia, both in ileal digesta and feces (P<0.05), suggesting a marked impact on N metabolism in the intestine. The analyses indicated that the alteration of gut microbiota was correlated with the apparent digestibility of CP and AA in the intestine. These findings suggest that the AGM-induced alteration of gut microbiota may contribute to the change in intestinal N metabolism, and consequently, N excretion from the body. These results also suggest that antibiotics could have a significant effect on host N metabolism. The present study contributes to our understanding of the effects of antibiotics and provides a rational scientific basis for diet formulation during AGM use.

Keywords

antibiotics feedingintestinal microbiotamicrobial metabolitesnitrogen utilizationswine
Type
Research Article
Information
animal , Volume 13 , Issue 2 , February 2019 , pp. 262 - 272
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

These authors contributed equally to this work.

References

Association of Official Analytical Chemists (AOAC) 2003. Official methods of analysis, volume 17, 17th edition. AOAC, Arlington, VA, USA.Google Scholar
Blachier, F, Mariotti, F, Huneau, JF and Tome, D 2007. Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33, 547–562.Google Scholar
Caesar, R, Reigstad, CS, Backhed, HK, Reinhardt, C, Ketonen, M, Lunden, GO, Cani, PD and Backhed, F 2012. Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 61, 1701–1707.Google Scholar
Choi, JY, Kim, JS, Ingale, SL, Kim, KH, Shinde, PL, Kwon, IK and Chae, BJ 2011. Effect of potential multimicrobe probiotic product processed by high drying temperature and antibiotic on performance of weanling pigs. Journal of Animal Science 89, 1795–1804.Google Scholar
Cilieborg, MS, Boye, M, Molbak, L, Thymann, T and Sangild, PT 2011. Preterm birth and necrotizing enterocolitis alter gut colonization in pigs. Pediatric Research 69, 10–16.Google Scholar
Collington, GK, Parker, DS and Armstrong, DG 1990. The influence of inclusion of either an antibiotic or a probiotic in the diet on the development of digestive enzyme-activity in the pig. British Journal of Nutrition 64, 59–70.Google Scholar
Cromwell, GL 2002. Why and how antibiotics are used in swine production. Animal Biotechnology 13, 7–27.Google Scholar
Dai, ZL, Li, XL, Xi, PB, Zhang, J, Wu, GY and Zhu, WY 2012. Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 42, 1597–1608.Google Scholar
Dai, ZL, Wu, GY and Zhu, WY 2011. Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Frontiers in Bioscience-Landmark 16, 1768–1786.Google Scholar
Dai, ZL, Wu, ZL, Jia, SC and Wu, GY 2014. Analysis of amino acid composition in proteins of animal tissues and foods as pre-column o-phthaldialdehyde derivatives by HPLC with fluorescence detection. Journal of Chromatography B, Analytical Technologies in the Biomedical and Life Sciences 964, 116–127.Google Scholar
Dai, ZL, Zhang, J, Wu, GY and Zhu, WY 2010. Utilization of amino acids by bacteria from the pig small intestine. Amino Acids 39, 1201–1215.Google Scholar
Davila, AM, Blachier, F, Gotteland, M, Andriamihaja, M, Benetti, PH, Sanz, Y and Tome, D 2013. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacological Research 68, 95–107.Google Scholar
Ferrer, M, Martins dos Santos, VA, Ott, SJ and Moya, A 2014. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut Microbes 5, 64–70.Google Scholar
Gao, K, Pi, Y, Peng, Y, Mu, CL and Zhu, WY 2018. Time-course responses of ileal and fecal microbiota and metabolite profiles to antibiotics in cannulated pigs. Applied Microbiology and Biotechnology 102, 2289–2299.Google Scholar
Geypens, B, Claus, D, Evenepoel, P, Hiele, M, Maes, B, Peeters, M, Rutgeerts, P and Ghoos, Y 1997. Influence of dietary protein supplements on the formation of bacterial metabolites in the colon. Gut 41, 70–76.Google Scholar
Jensen, ML, Thymann, T, Cilieborg, MS, Lykke, M, Molbak, L, Jensen, BB, Schmidt, M, Kelly, D, Mulder, I, Burrin, DG and Sangild, PT 2014. Antibiotics modulate intestinal immunity and prevent necrotizing enterocolitis in preterm neonatal piglets. American Journal of Physiology Gastrointestinal and Liver Physiology 306, G59–G71.Google Scholar
Jonkers, D, Penders, J, Masclee, A and Pierik, M 2012. Probiotics in the management of inflammatory bowel disease: a systematic review of intervention studies in adult patients. Drugs 72, 803–823.Google Scholar
Macfarlane, GT, Allison, C, Gibson, SA and Cummings, JH 1988. Contribution of the microflora to proteolysis in the human large intestine. The Journal of Applied Bacteriology 64, 37–46.Google Scholar
Makkar, H, Sharma, O, Dawra, R and Negi, S 1982. Simple determination of microbial protein in rumen liquor. Journal of Dairy Science 65, 2170–2173.Google Scholar
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th edition. National Academy Press, Washington, DC, USA.Google Scholar
Mu, CL, Yang, YX, Yu, KF, Yu, M, Zhang, CJ, Su, Y and Zhu, WY 2017. Alteration of metabolomic markers of amino-acid metabolism in piglets with in-feed antibiotics. Amino Acids 49, 771–781.Google Scholar
Nicholson, JK, Holmes, E, Kinross, J, Burcelin, R, Gibson, G, Jia, W and Pettersson, S 2012. Host-gut microbiota metabolic interactions. Science 336, 1262–1267.Google Scholar
Nyachoti, CM, Omogbenigun, FO, Rademacher, M and Blank, G 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. Journal of Animal Science 84, 125–134.Google Scholar
Puiman, P, Stoll, B, Molbak, L, de Bruijn, A, Schierbeek, H, Boye, M, Boehm, G, Renes, I, van Goudoever, J and Burrin, D 2013. Modulation of the gut microbiota with antibiotic treatment suppresses whole body urea production in neonatal pigs. American Journal of Physiology Gastrointestinal and Liver Physiology 304, G300–G310.Google Scholar
Stein, HH, Shipley, CF and Easter, RA 1998. Technical note: a technique for inserting a T-cannula into the distal ileum of pregnant sows. Journal of Animal Science 76, 1433–1436.Google Scholar
Stoll, B, Henry, J, Reeds, PJ, Yu, H, Jahoor, F and Burrin, DG 1998. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. The Journal of Nutrition 128, 606–614.Google Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Willing, BP, Russell, SL and Finlay, BB 2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nature Reviews Microbiology 9, 233–243.Google Scholar
Wrong, OM, Vince, AJ and Waterlow, JC 1985. The contribution of endogenous urea to faecal ammonia in man, determined by 15N labelling of plasma urea. Clinical Science 68, 193–199.Google Scholar
Wu, GY 2009. Amino acids: metabolism, functions, and nutrition. Amino Acids 37, 1–17.Google Scholar
Yang, YX, Dai, ZL and Zhu, WY 2014. Important impacts of intestinal bacteria on utilization of dietary amino acids in pigs. Amino Acids 46, 2489–2501.Google Scholar
Yang, YX, Mu, CL, Zhang, JF and Zhu, WY 2014. Determination of biogenic amines in digesta by high performance liquid chromatography with precolumn dansylation. Analytical Letters 47, 1290–1298.Google Scholar
Yu, M, Mu, CL, Yang, YX, Zhang, CJ, Su, Y, Huang, Z, Yu, KF and Zhu, WY 2017. Increases in circulating amino acids with in-feed antibiotics correlated with gene expression of intestinal amino acid transporters in piglets. Amino Acids 49, 1587–1599.Google Scholar
Yu, M, Zhang, CJ, Yang, YX, Mu, CL, Su, Y, Yu, KF and Zhu, WY 2017. Long-term effects of early antibiotic intervention on blood parameters, apparent nutrient digestibility, and fecal microbial fermentation profile in pigs with different dietary protein levels. Journal of Animal Science and Biotechnology 8, 60.Google Scholar
Zhang, CJ, Yu, M, Yang, YX, Mu, CL, Su, Y and Zhu, WY 2016. Effect of early antibiotic administration on cecal bacterial communities and their metabolic profiles in pigs fed diets with different protein levels. Anaerobe 42, 188–196.Google Scholar
Supplementary material: File

Pi et al. supplementary material

Tables S1-S8 and Figure S1

Download Pi et al. supplementary material(File)
File 281 KB