DOI QR코드

DOI QR Code

Effects of short-term fasting on in vivo rumen microbiota and in vitro rumen fermentation characteristics

  • Kim, Jong Nam (Deparment of Animal Biosystem Sciences, Chungnam National University) ;
  • Song, Jaeyong (Department of Animal Science, Kyungpook National University) ;
  • Kim, Eun Joong (Department of Animal Science, Kyungpook National University) ;
  • Chang, Jongsoo (Department of Agricultural Science, Korea National Open University) ;
  • Kim, Chang-Hyun (Department of Animal Life and Environmental science, Hankyung National University) ;
  • Seo, Seongwon (Department of Animal Science and Technology, Chung-Ang University) ;
  • Chang, Moon Baek (Department of Animal Science and Technology, Chung-Ang University) ;
  • Bae, Gui-Seck (Department of Animal Science and Technology, Chung-Ang University)
  • Received : 2018.07.01
  • Accepted : 2018.09.10
  • Published : 2019.06.01

Abstract

Objective: Fasting may lead to changes in the microbiota and activity in the rumen. In the present study, the effects of fasting on rumen microbiota and the impact of fasting on in vitro rumen fermentation were evaluated using molecular culture-independent methods. Methods: Three ruminally cannulated Holstein steers were fed rice straw and concentrates. The ruminal fluids were obtained from the same steers 2 h after the morning feeding (control) and 24 h after fasting (fasting). The ruminal fluid was filtrated through four layers of muslin, collected for a culture-independent microbial analysis, and used to determine the in vitro rumen fermentation characteristics. Total DNA was extracted from both control and fasting ruminal fluids. The rumen microbiota was assessed using denaturing gradient gel electrophoresis (DGGE) and quantitative polymerase chain reaction. Microbial activity was evaluated in control and fasting steers at various intervals using in vitro batch culture with rice straw and concentrate at a ratio of 60:40. Results: Fasting for 24 h slightly affected the microbiota structure in the rumen as determined by DGGE. Additionally, several microorganisms, including Anaerovibrio lipolytica, Eubacterium ruminantium, Prevotella albensis, Prevotella ruminicola, and Ruminobacter amylophilus, decreased in number after fasting. In addition, using the ruminal fluid as the inoculum after 24 h of fasting, the fermentation characteristics differed from those obtained using non-fasted ruminal fluid. Compared with the control, the fasting showed higher total gas production, ammonia, and microbial protein production (p<0.05). No significant differences, however, was observed in pH and dry matter digestibility. Conclusion: When in vitro techniques are used to evaluate feed, the use of the ruminal fluid from fasted animals should be used with caution.

Keywords

References

  1. Johnson RR. Techniques and procedures for in vitro and in vivo rumen studies. J Anim Sci 1966;25:855-75. https://doi.org/10.2527/jas1966.253855x
  2. Kim DH, Amanullah SM, Lee HJ, et al. Effects of different cutting height on nutritional quality of whole crop barley silage and feed value on Hanwoo heifers. Asian-Australas J Anim Sci 2016; 29:1265-72. https://doi.org/10.5713/ajas.16.0099
  3. Mould FL, Kliem KE, Morgan R, Mauricio RM. In vitro microbial inoculum: a review of its function and properties. Anim Feed Sci Technol 2005;123-124, Part 1:31-50. https://doi.org/10.1016/j.anifeedsci.2005.04.028
  4. Payne JS, Hamersley AR, Milligan JC, Huntington JA. The effect of rumen fluid collection time on its fermentative capacity and the stability of rumen conditions in sheep fed a constant diet. In: Proceedings of the British Society of Animal Science, UK: British Society of Animal Science; 2002. p. 165.
  5. Jeon S, Sohn K-N, Seo S. Evaluation of feed value of a by-product of pickled radish for ruminants: analyses of nutrient composition, storage stability, and in vitro ruminal fermentation. J Anim Sci Technol 2016;58:34. https://doi.org/10.1186/s40781-016-0117-1
  6. Menke KH, Steingass H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim Res Dev 1988;28:7-55.
  7. McAllister TA, Bae HD, Jones GA, Cheng KJ. Microbial attachment and feed digestion in the rumen. J Anim Sci 1994;72: 3004-18. https://doi.org/10.2527/1994.72113004x
  8. Chaudhry AS, Mohamed RAI. Fresh or frozen rumen contents from slaughtered cattle to estimate in vitro degradation of two contrasting feeds. Czech J Anim Sci 2012;57:265-73. https://doi.org/10.17221/5961-CJAS
  9. Rius AG, Kittelmann S, Macdonald KA, et al. Nitrogen metabolism and rumen microbial enumeration in lactating cows with divergent residual feed intake fed high-digestibility pasture. J Dairy Sci 2012;95:5024-34. https://doi.org/10.3168/jds.2012-5392
  10. Ben Omar N, Ampe F. Microbial community dynamics during production of the Mexican fermented maize dough pozol. Appl Environ Microbiol 2000;66:3664-73. https://doi.org/10.1128/AEM.66.9.3664-3673.2000
  11. Yu Z, Morrison M. Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 2004;70:4800-6. https://doi.org/10.1128/AEM.70.8.4800-4806.2004
  12. Lopez I, Ruiz-Larrea F, Cocolin L, et al. Design and evaluation of PCR primers for analysis of bacterial populations in wine by denaturing gradient gel electrophoresis. Appl Environ Microbiol 2003;69:6801-7. https://doi.org/10.1128/AEM.69.11.6801-6807.2003
  13. Fernando SC, Purvis II HT, Najar FZ, et al. Rumen microbial population dynamics during adaptation to a high-grain diet. Appl Environ Microbiol 2010;76:7482-90. https://doi.org/10.1128/AEM.00388-10
  14. Karnati SK, Yu Z, Sylvester JT, et al. Technical note: Specific PCR amplification of protozoal 18S rDNA sequences from DNA extracted from ruminal samples of cows. J Anim Sci 2003;81:812-5. https://doi.org/10.2527/2003.813812x
  15. Koike S, Kobayashi Y. Development and use of competitive PCR assays for the rumen cellulolytic bacteria: Fibrobacter succinogenes, Ruminococcus albus and Ruminococcus flavefaciens. FEMS Microbiol Lett 2001;204:361-6. https://doi.org/10.1111/j.1574-6968.2001.tb10911.x
  16. Shin EC, Choi BR, Lim WJ, et al. Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 2004;10:313-9. https://doi.org/10.1016/j.anaerobe.2004.08.002
  17. AOAC. Official methods of analysis (16th Ed.). Washington, DC, USA: Association of Official Analytical Chemists; 1995.
  18. Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstartch polysaccharides in relation to animal nutrition. J Dairy Sci 1991;74:3583-97. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
  19. McDougall EI. Studies on ruminant saliva. 1. The composition and output of sheep's saliva. Biochem J 1948;43:99-109. https://doi.org/10.1042/bj0430099
  20. Miller TL, Wolin MJ. A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 1974;27:985-7. https://doi.org/10.1128/AEM.27.5.985-987.1974
  21. Chaney AL, Marbach EP. Modified reagents for determination of urea and ammonia. Clin Chem 1962;8:130-2. https://doi.org/10.1093/clinchem/8.2.130
  22. Erwin ES, Marco GJ, Emery EM. Volatile fatty acid analyses of blood and rumen fluid by gas chromatography. J Dairy Sci 1961;44:1768-71. https://doi.org/10.3168/jds.S0022-0302(61)89956-6
  23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193: 265-75. https://doi.org/10.1016/S0021-9258(19)52451-6
  24. SAS. SAS Procedures Guide, Version 8. Cary, NC, USA: SAS Institute Inc.; 1999.
  25. Carberry CA, Kenny DA, Han S, McCabe MS, Waters SM. Effect of phenotypic residual feed intake and dietary forage content on the rumen microbial community of beef cattle. Appl Environ Microbiol 2012;78:4949-58. https://doi.org/10.1128/AEM.07759-11
  26. Kohl KD, Amaya J, Passement CA, Dearing MD, McCue MD. Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts. FEMS Microbiol Ecol 2014;90:883-94. https://doi.org/10.1111/1574-6941.12442
  27. McCue MD. An introduction to fasting, starvation, and food limitation. In: McCue MD, editor. Comparative physiology of fasting, starvation, and food limitation. 1 ed: Berlin Heidelberg, Germany: Springer-Verlag; 2012. p. 1-5.
  28. Maccarana L, Cattani M, Tagliapietra F, et al. Methodological factors affecting gas and methane production during in vitro rumen fermentation evaluated by meta-analysis approach. J Anim Sci Biotechnol 2016;7:35. https://doi.org/10.1186/s40104-016-0094-8
  29. Lee SJ, Shin NH, Jeong JS, et al. Effects of Gelidium amansii extracts on in vitro ruminal fermentation characteristics, methanogenesis, and microbial populations. Asian-Australas J Anim Sci 2018;31:71-9. https://doi.org/10.5713/ajas.17.0619

Cited by

  1. Effect of Dietary Crude Protein on Animal Performance, Blood Biochemistry Profile, Ruminal Fermentation Parameters and Carcass and Meat Quality of Heavy Fattening Assaf Lambs vol.10, pp.11, 2020, https://doi.org/10.3390/ani10112177
  2. Determination of maintenance energy requirement and responses of dry ewes to dietary inclusion of lucerne versus concentrate meal vol.15, pp.5, 2019, https://doi.org/10.1016/j.animal.2021.100200
  3. Gut microbiota modulation as a possible mediating mechanism for fasting-induced alleviation of metabolic complications: a systematic review vol.18, pp.1, 2019, https://doi.org/10.1186/s12986-021-00635-3
  4. Exploring the Ruminal Microbial Community Associated with Fat Deposition in Lambs vol.11, pp.12, 2019, https://doi.org/10.3390/ani11123584
  5. Experimental crossover study on the effects of withholding feed for 24 h on the equine faecal bacterial microbiota in healthy mares vol.17, 2021, https://doi.org/10.1186/s12917-020-02706-8