Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Enhancing Butyrate Production, Ruminal Fermentation and Microbial Population through Supplementation with Clostridium saccharobutylicum

  • Miguel, Michelle A. (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University) ;
  • Lee, Sung Sill (Division of Applied Life Science (BK21 Program) and Institute of Agriculture and Life Sciences (IALS), Gyeongsang National University) ;
  • Mamuad, Lovelia L. (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University) ;
  • Choi, Yeon Jae (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University) ;
  • Jeong, Chang Dae (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University) ;
  • Son, Arang (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University) ;
  • Cho, Kwang Keun (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology) ;
  • Kim, Eun Tae (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Kim, Sang Bum (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Lee, Sang Suk (Department of Animal Science and Technology, College of Bio-industry Science, Sunchon National University)
  • Received : 2019.05.08
  • Accepted : 2019.06.06
  • Published : 2019.07.28
Download PDF
⟨ Previous Next ⟩

Abstract

Butyrate is known to play a significant role in energy metabolism and regulating genomic activities that influence rumen nutrition utilization and function. Thus, this study investigated the effects of an isolated butyrate-producing bacteria, Clostridium saccharobutylicum, in rumen butyrate production, fermentation parameters and microbial population in Holstein-Friesian cow. An isolated butyrate-producing bacterium from the ruminal fluid of a Holstein-Friesian cow was identified and characterized as Clostridium saccharobutylicum RNAL841125 using 16S rRNA gene sequencing and phylogenetic analyses. The bacterium was evaluated on its effects as supplement on in vitro rumen fermentation and microbial population. Supplementation with $10^6CFU/ml$ Clostridium saccharobutylicum increased (p < 0.05) microbial crude protein, butyrate and total volatile fatty acids concentration but had no significant effect on $NH_3-N$ at 24 h incubation. Butyrate and total VFA concentrations were higher (p < 0.05) in supplementation with $10^6CFU/ml$ Clostridium saccharobutylicum compared with control, with no differences observed for total gas production, $NH_3-N$ and propionate concentration. However, as the inclusion rate (CFU/ml) of C. saccharobutylicum was increased, reduction of rumen fermentation values was observed. Furthermore, butyrate-producing bacteria and Fibrobacter succinogenes population in the rumen increased in response with supplementation of C. saccharobutylicum, while no differences in the population in total bacteria, protozoa and fungi were observed among treatments. Overall, our study suggests that supplementation with $10^6CFU/ml$ C. saccharobutylicum has the potential to improve ruminal fermentation through increased concentrations of butyrate and total volatile fatty acid, and enhanced population of butyrate-producing bacteria and cellulolytic bacteria F. succinogenes.

Keywords

References

  1. Fellner V. 2002. Rumen microbes and nutrient management. Available from https://projects.ncsu.edu/project/swine_extension/swinereports/2004-2005/dairycattle/nutrition/fellner1.htm. Accessed Nov. 22, 2018.
  2. Chesson A, Forsberg CW. 1997. Polysaccharide degradation by rumen microorganism, pp. 329-381. In The Rumen Microbial Ecosystem. Dordrecht: Springer.
  3. Gournier-Chateau N, Larpent JP, Castellanos MI, Larpent JL. 1994. Probiotics in animal and human nutrition, pp. 192. Les probiotiques en Aliment. Anim. Hum. Paris. Technique et Documentation Lavoisier.
  4. Jouany JP, Morgavi DP. 2007. Use of “natural” products as alternatives to antibiotic feed additives in ruminant production. Animal 1: 1443-1466. https://doi.org/10.1017/S1751731107000742
  5. Guedes CM, Goncalves D, Rodrigues MAM, Dias-da-Silva A. 2008. Effects of a Saccharomyces cerevisiae yeast on ruminal fermentation and fibre degradation of maize silages in cows. Anim. Feed. Sci. Technol. 145: 27-40. https://doi.org/10.1016/j.anifeedsci.2007.06.037
  6. Wallace RJ, Colombatto D, Robinson PH. 2008. Enzymes, direct-fed microbials and plant extracts in ruminant nutrition. Anim. Feed. Sci. Technol. 145: 1-4. https://doi.org/10.1016/j.anifeedsci.2007.07.006
  7. Wallace RJ. 1994. Ruminal microbiology, biotechnology, and ruminant nutrition: progress and problems. J. Anim. Sci. 72: 2992-3003. https://doi.org/10.2527/1994.72112992x
  8. Bernardeau M, Vernoux JP. 2013. Overview of differences between microbial feed additives and probiotics for food regarding regulation, growth promotion effects and health properties and consequences for extrapolation of farm animal results to humans. Clin. Microbiol. Infect. 19: 321-330. https://doi.org/10.1111/1469-0691.12130
  9. Aluwong T, Kobo PI, Abdullahi A. 2013.Volatile fatty acids production in ruminants and the role of monocarboxylate transporters: a review. Afr. J. Biotechnol. 9: 6229-6232.
  10. Bugaut M. 1987. Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comp. Biochem. Physiol. B. 86: 439-472. https://doi.org/10.1016/0305-0491(87)90433-0
  11. Li X, Hojberg O, Canibe N, Jensen BB. 2016. Phylogenetic diversity of cultivable butyrate-producing bacteria from pig gut content and feces. J. Anim. Sci. 94: 377-381.
  12. Scheppach W. 1994. Effects of short chain fatty acids on gut morphology and function. Gut 35 Suppl 1: S35-S38. https://doi.org/10.1136/gut.35.1_Suppl.S35
  13. Kato SI, Sato K, Chida H, Roh SG, Ohwada S, Sato S, et al. 2011. Effects of Na-butyrate supplementation in milk formula on plasma concentrations of GH and insulin, and on rumen papilla development in calves. J. Endocrinol. 211: 241-248. https://doi.org/10.1530/JOE-11-0299
  14. Pierce, J., Marjen, M. and Goossens T. 2004. Butyrate: Feeding the gut and beyond for animal health. https://nutriad.com/2015/01/butyrate-feeding-the-gut-and-beyond-for-animal-health-2/. Accessed 20 Nov. 2018.
  15. Canani RB, Di Costanzo M, Leone L. 2012. The epigenetic effects of butyrate: Potential therapeutic implications for clinical practice. Clin. Epigenetics 4(1): 4. doi: 10.1186/1868-7083-4-4.
  16. Vital M, Penton CR, Wang Q, Young VB, Antonopoulos DA, Sogin ML, et al. 2013. A gene-targeted approach to investigate the intestinal butyrate-producing bacterial community. Microbiome 1: 8. https://doi.org/10.1186/2049-2618-1-8
  17. Levine UY, Looft T, Allen HK, Stanton TB. 2013. Butyrate-producing bacteria, including mucin degraders, from the swine intestinal tract. Appl. Environ. Microbiol. 79: 3879-3881. https://doi.org/10.1128/AEM.00589-13
  18. Mrazek J, Tepsic K, Avgustin G, Kopecny J. 2006. Diet-dependent shifts in ruminal butyrate-producing bacteria. Folia Microbiol. 51: 294-298. https://doi.org/10.1007/BF02931817
  19. Miyazaki K, Martin JC, Marinsek-Logar R, Flint HJ. 1997. Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B14. Anaerobe 3: 373-381. https://doi.org/10.1006/anae.1997.0125
  20. Singh S, Kundu SS. 2011. Comparative rumen microbial population in sheep fed Dicantium annulatum grass supplemented with Leucaena leucocephala and Hardwickia binata tree leaves. Livest. Res. Rural Dev. 23: 117-132.
  21. Lane DJ. 1991. 16S/23S rRNA sequencing, pp. 115-175. In Stackebrandt E, Goodfellow M (eds.). Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons, Chichester, United Kingdom.
  22. Madden T. 2003. The BLAST Sequence Analysis Tool. 2nd edition. NCBI Handbook[internet]. National Center for Biotechnology Information (USA).
  23. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evo.l Microbiol. 67: 1613-1617. https://doi.org/10.1099/ijsem.0.001755
  24. Richard C, Beaudouin E, Moneret-Vautrin DA, Kohler C, Nguyen-Grosjean VM, Jacquenet S. 2016. Severe anaphylaxis to propofol: first case of evidence of sensitization to soy oil. Eur. Ann. Allergy Clin. Immunol. 48: 103-106.
  25. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729. https://doi.org/10.1093/molbev/mst197
  26. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
  27. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120. https://doi.org/10.1007/BF01731581
  28. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution (NY) 39: 783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  29. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428. https://doi.org/10.1021/ac60147a030
  30. Asanuma N, Iwamoto M, Hino T. 1999. Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J. Dairy Sci. 82: 780-787. https://doi.org/10.3168/jds.S0022-0302(99)75296-3
  31. Chaney AL, Marbach EP. 1962. Modified reagents for determination of urea and ammonia. Clin. Chem. 8: 130-132. https://doi.org/10.1093/clinchem/8.2.130
  32. Castillo-Lopez E, Klopfenstein TJ, Fernando SC, Kononoff PJ. 2013. In vivo determination of rumen undegradable protein of dried distillers grains with solubles and evaluation of duodenal microbial crude protein flow. J. Anim. Sci. 91: 924-934. https://doi.org/10.2527/jas.2012-5323
  33. Keis S, Shaheen R, Jones DT. 2001. Emended descriptions of Clostridium acetobutylicum and Clostridium beijerinckii, and descriptions of Clostridium saccharoperbutylacetonicum sp. nov. and Clostridium saccharobutylicum sp. nov. Int. J. Syst. Evol. Microbiol. 51: 2095-2103. https://doi.org/10.1099/00207713-51-6-2095
  34. Bergman EN. 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70: 567-590. https://doi.org/10.1152/physrev.1990.70.2.567
  35. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK. 2008. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190: 843-850. https://doi.org/10.1128/JB.01417-07
  36. Li RW, Wu S, Baldwin VI RL, Li W, Li C. 2012. Perturbation dynamics of the rumen microbiota in response to exogenous butyrate. PLoS One 7: e29392. https://doi.org/10.1371/journal.pone.0029392
  37. Bedford A, Gong J. 2018. Implications of butyrate and its derivatives for gut health and animal production. Anim. Nutr. 4: 151-159. https://doi.org/10.1016/j.aninu.2017.08.010
  38. Kabara JJ, Swieczkowski DM, Conley AJ, Truant JP. 1972. Fatty acids and derivatives as antimicrobial agents. Antimicrob. Agents Chemother. 2: 23-28. https://doi.org/10.1128/AAC.2.1.23
  39. Thormar H, Hilmarsson H, Bergsson G. 2006. Stable concentrated emulsions of the 1-monoglyceride of capric acid (monocaprin) with microbicidal activities against the food-borne bacteria Campylobacter jejuni, Salmonella spp., and Escherichia coli. Appl. Environ. Microbiol. 72: 522-526. https://doi.org/10.1128/AEM.72.1.522-526.2006
  40. Keis S, Bennett CF, Ward VK, Jones DT. 1995. Taxonomy and phylogeny of industrial solvent-producing clostridia. Int. J. Syst. Bacteriol. 45: 693-705. https://doi.org/10.1099/00207713-45-4-693
  41. JohnsonN JL, Toth J, Santiwatanakul S, Chen JS. 1997. Cultures of "Clostridium acetobutylicum" from Various Collections Comprise Clostridium acetobutylicum, Clostridium beijerinckii, and Two Other Distinct Types Based on DNA-DNA Reassociation. Int. J. Syst. Bacteriol. 47: 420-424. https://doi.org/10.1099/00207713-47-2-420
  42. Meesukanun K, Satirapipathkul C. 2014. Production of acetone-butanol-ethanol from cassava rhizome hydrolysate by Clostridium saccharobutylicum BAA 117. Chem. Eng. Trans. 37: 421-426.
  43. Rymer C, Huntington JA, Williams BA, Givens DI. 2005. In vitro cumulative gas production techniques: history, methodological considerations and challenges. Anim. Feed Sci. Technol. 123: 9-30. https://doi.org/10.1016/j.anifeedsci.2005.04.055
  44. Metzler-Zebeli BU, Scherr C, Sallaku E, Drochner W, Zebeli Q. 2012. Evaluation of associative effects of total mixed ration for dairy cattle using in vitro gas production and different rumen inocula. J. Sci. Food Agric. 92: 2479-2485. https://doi.org/10.1002/jsfa.5656
  45. Doto S, Liu J. 2011. Effects of direct-fed microbials and their combinations with yeast culture on in vitro rumen fermentation characteristics. J. Anim. Feed Sci. 20: 259-271. https://doi.org/10.22358/jafs/66183/2011
  46. Cummings JH, Macfarlane GT. 1991. The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70: 443-459. https://doi.org/10.1111/j.1365-2672.1991.tb02739.x
  47. Louis P, Flint HJ. 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 294: 1-8. https://doi.org/10.1111/j.1574-6968.2009.01514.x
  48. Bryant MP. 1974. Nutritional features and ecology of predominant anaerobic bacteria of the intestinal tract. Am. J. Clin. Nutr. 27: 1313-1319. https://doi.org/10.1093/ajcn/27.11.1313
  49. Satter LD, Slyter LL.1974. Effect of ammonia concentration of rumen microbial protein production in vitro. Br. J. Nutr. 32: 199-208. https://doi.org/10.1079/BJN19740073
  50. Hristov AN, McAllister TA, Xu Z, Newbold CJ. 2002. Proteolytic activity in ruminal fluid from cattle fed two levels of barley grain: A comparison of three methods of determination. J. Sci. Food Agric. 82: 1886-1893. https://doi.org/10.1002/jsfa.1238
  51. Soriano AP, Mamuad LL, Kim SH, Choi YJ, Jeong CD, Bae GS, et al. 2014. Effect of Lactobacillus mucosae on in vitro rumen fermentation characteristics of dried brewers grain, methane production and bacterial diversity. Asian-Australasian J. Anim. Sci. 27: 1562-1570. https://doi.org/10.5713/ajas.2014.14517
  52. Mamuad L, Kim SH, Jeong CD, Choi YJ, Jeon CO, Lee SS. 2014. Effect of fumarate reducing bacteria on in vitro rumen fermentation, methane mitigation and microbial diversity. J. Microbiol. 52: 120-128. https://doi.org/10.1007/s12275-014-3518-1
  53. Kim SH, Mamuad LL, Kim DW, Kim SK, Lee SS. 2016. Fumarate reductase-producing enterococci reduce methane production in rumen fermentation in vitro. J. Microbiol. Biotechnol. 26: 558-566. https://doi.org/10.4014/jmb.1512.12008
  54. Ghorbani GR, Morgavi DP, Beauchemin KA, Leedle JAZ. 2002. Effects of bacterial direct-fed microbials on ruminal fermentation, blood variables, and the microbial populations of feedlot cattle. J. Anim. Sci. 80: 1977-1985. https://doi.org/10.2527/2002.8071977x
  55. Chiquette J, Allison MJ, Rasmussen M. 2012. Use of Prevotella bryantii 25A and a commercial probiotic during subacute acidosis challenge in midlactation dairy cows. J. Dairy Sci. 95: 5985-5995. https://doi.org/10.3168/jds.2012-5511
  56. Kowalski ZM, Gorka P, Flaga J, Barteczko A, Burakowska K, Oprządek J, et al. 2015. Effect of microencapsulated sodium butyrate in the close-up diet on performance of dairy cows in the early lactation period. J. Dairy Sci. 98: 3284-3291. https://doi.org/10.3168/jds.2014-8688
  57. Qadis AQ, Goya S, Ikuta K, Yatsu M, Kimura A, Nakanishi S, et al. 2014. Effects of a bacteria-based probiotic on ruminal pH, volatile fatty acids and bacterial flora of Holstein calves. J. Vet. Med. Sci. 76: 877-885. https://doi.org/10.1292/jvms.14-0028
  58. Timpka T, Eriksson H, Gursky EA, Strömgren M, Holm E, Ekberg J, et al. 2011. Requirements and design of the PROSPER protocol for implementation of information infrastructures supporting pandemic response: a nominal group study. PLoS One 6: e17941 https://doi.org/10.1371/journal.pone.0017941
  59. Block E. 2006. Rumen microbial protein production: Are we missing an opportunity to improve dietary and economic efficiencies in protein nutrition of the high producing dairy cow? In: High Plains Dairy Conference. Available from http//.www.highplainsdairy.org/2006/Block-pdf. Accessed Nov. 18, 2018.
  60. Castillo-Lopez E. 2012. Intestinal flow of microbial protein and rumen undegradable protein in cattle fed corn distillers grains and solubles, with emphasis during lactation. Vailable from https://digitalcommons.unl.edu/animalscidiss/60/. Accessed Nov. 21, 2018.
  61. Storm AC, Kristensen NB, Hanigan MD. 2012. A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows. J. Dairy Sci. 95: 2919-2934. https://doi.org/10.3168/jds.2011-4239
  62. Sakata T, Tamate H. 1978.Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. J. Dairy Sci. 61: 1109-1113. https://doi.org/10.3168/jds.S0022-0302(78)83694-7
  63. Graham C, Simmons NL. 2005. Functional organization of the bovine rumen epithelium. Am. J. Physiol. Integr. Comp. Physiol. 288: R173-181. https://doi.org/10.1152/ajpregu.00425.2004
  64. Mamuad LL, Kim SH, Choi YJ, Soriano AP, Cho KK, Lee K, et al. 2017. Increased propionate concentration in Lactobacillus mucosae-fermented wet brewers grains and during in vitro rumen fermentation. J. Appl. Microbiol. 123: 29-40. https://doi.org/10.1111/jam.13475
  65. Gorka P, Kowalski ZM, Pietrzak P, Kotunia A, Kiljanczyk R, Flaga J, et al. 2009. Effect of sodium butyrate supplementation in milk replacer and starter diet on rumen development in calves. J. Physiol. Pharmacol. 3 Suppl: 47-53.
  66. Patra RC, Lal SB, Swarup D. 1996. Biochemical profile of rumen liquor, blood and urine in experimental acidosis in sheep. Small Rumin. Res. 19: 177-180. https://doi.org/10.1016/0921-4488(95)00743-1
  67. Mao SY, Zhang G, Zhu WY. 2008. Effect of disodium fumarate on ruminal metabolism and rumen bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. Anim. Feed Sci. Technol. 140: 293-306. https://doi.org/10.1016/j.anifeedsci.2007.04.001
  68. Wang W, Chen L, Zhou R, Wang X, Song L, Huang S, et al. 2014. Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J. Clin. Microbiol. 52: 398-406. https://doi.org/10.1128/JCM.01500-13
  69. Flint HJ, Duncan SH, Scott KP, Louis P. 2007. Interactions and competition within the microbial community of the human colon: Links between diet and health. Environ. Microbiol. 9: 1101-1111. https://doi.org/10.1111/j.1462-2920.2007.01281.x
  70. Denman SE, McSweeney CS. 2006. Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol. Ecol. 58: 572-582. https://doi.org/10.1111/j.1574-6941.2006.00190.x
  71. Sylvester JT, Karnati SKR, Yu Z, Morrison M, Firkins JL. 2004. Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. J. Nutr. 134: 3378-3384. https://doi.org/10.1093/jn/134.12.3378
  72. Yu Y, Lee C, Kim J, Hwang S. 2005. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 89: 670-679. https://doi.org/10.1002/bit.20347
  73. Sylvester JT, Karnati SKR, Yu Z, Newbold CJ, Firkins JL. 2005. Evaluation of a real-time PCR assay quantifying the ruminal pool size and duodenal flow of protozoal nitrogen. J. Dairy Sci. 88: 2083-2095. https://doi.org/10.3168/jds.S0022-0302(05)72885-X

Cited by

  1. Effects of Thymol Supplementation on Goat Rumen Fermentation and Rumen Microbiota In Vitro vol.8, pp.8, 2019, https://doi.org/10.3390/microorganisms8081160
  2. Supplementing the Diet of Dairy Goats with Dried Orange Pulp throughout Lactation: I. Effect on Milk Performance, Nutrient Utilisation, Blood Parameters and Production Economics vol.11, pp.9, 2021, https://doi.org/10.3390/ani11092601
  3. Dietary fiber‐derived short‐chain fatty acids: A potential therapeutic target to alleviate obesity‐related nonalcoholic fatty liver disease vol.22, pp.11, 2019, https://doi.org/10.1111/obr.13316
  4. An efficient system for intestinal on-site butyrate production using novel microbiome-derived esterases vol.15, pp.1, 2019, https://doi.org/10.1186/s13036-021-00259-4