Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Metabolomic and morphologic surveillance reveals the impact of lactic acid-treated barley on in vitro ruminal fermentation

  • K E Tian (The United Graduate School of Agricultural Science, Gifu University) ;
  • Dicky Aldian (The United Graduate School of Agricultural Science, Gifu University) ;
  • Masato Yayota (The United Graduate School of Agricultural Science, Gifu University)
  • Received : 2023.12.27
  • Accepted : 2024.05.01
  • Published : 2024.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Lactic acid (LA) treatment of cereals is known to improve ruminant performance. However, changes in cereal nutrient levels and variations in rumen fermentation remain unclear. Methods: This study was designed to compare the effects of 5% LA treatment on the trophic and morphological characteristics of barley and to discover the differences in rumen fermentation characteristics and metabolomes between LA-treated and untreated barley. Results: Compared with those of untreated barley (BA), the dry matter (DM), crude protein (CP), ash and water-soluble carbohydrate contents of barley plants treated with 5% LA for 48 h (BALA) decreased, but the resistant starch (RS) and non-fiber carbohydrate contents increased. Moreover, the amount of proteinaceous matrix in BA decreased in response to LA treatment. During in vitro fermentation, BALA had a greater pH but lower dry matter disappearance and ammonia, methane, and short-chain fatty acid levels than BA. The differential metabolites between BA and BALA were clustered into metabolic pathways such as purine metabolism, lysine degradation, and linoleic acid metabolism. Observable differences in ultrastructure between BALA and BA were noted during fermentation. Conclusion: Lactic treatment altered barley nutrient content, including DM, CP, RS, ash, water-soluble carbohydrates and non-fiber carbohydrates, and affected barley ultrastructure. These variations led to significant and incubation time-dependent changes in the in vitro fermentation characteristics and metabolome.

Keywords

Acknowledgement

The authors would like to thank Prof Iwasawa Atsushi at the Faculty of Applied Biological Science, Gifu University, for his assistance during the laboratory experiment and Ms Takatera Kinuyo at Life Science Research Centre, Gifu University, for her kind assistance during the SEM analysis.

References

  1. Khafipour E, Krause DO, Plaizier JC. A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. J Dairy Sci 2009;92:1060-70. https://doi.org/10.3168/jds.2008-1389
  2. Zebeli Q, Mansmann D, Steingass H, Ametaj BN. Balancing diets for physically effective fibre and ruminally degradable starch: A key to lower the risk of sub-acute rumen acidosis and improve productivity of dairy cattle. Livest Sci 2010;127:1-10. https://doi.org/10.1016/j.livsci.2009.09.003
  3. Nikkhah A. Barley grain for ruminants: a global treasure or tragedy. J Anim Sci Biotechnol 2012;3:22. https://doi.org/10.1186/2049-1891-3-22
  4. Yang Y, Dong G, Wang Z, Liu J, Chen J, Zhang Z. Treatment of corn with lactic acid or hydrochloric acid modulates the rumen and plasma metabolic profiles as well as inflammatory responses in beef steers. BMC Vet Res 2018;14:408. https://doi.org/10.1186/s12917-018-1734-3
  5. Dailey OD, Dowd MK, Mayorga JC. Influence of lactic acid on the solubilization of protein during corn steeping. J Agric Food Chem 2000;48:1352-7. https://doi.org/10.1021/jf990866s
  6. Iqbal S, Zebeli Q, Mazzolari A, et al. Feeding barley grain steeped in lactic acid modulates rumen fermentation patterns and increases milk fat content in dairy cows. J Dairy Sci 2009;92:6023-32. https://doi.org/10.3168/jds.2009-2380
  7. Iqbal S, Terrill SJ, Zebeli Q, et al. Treating barley grain with lactic acid and heat prevented sub-acute ruminal acidosis and increased milk fat content in dairy cows. Anim Feed Sci Technol 2012;172:141-9. https://doi.org/10.1016/j.anifeedsci.2011.12.024
  8. Deckardt K, Metzler-Zebeli BU, Zebeli Q. Processing barley grain with lactic acid and tannic acid ameliorates rumen microbial fermentation and degradation of dietary fibre in vitro. J Sci Food Agric 2016;96:223-31. https://doi.org/10.1002/jsfa.7085
  9. Votterl JC, Zebeli Q, Hennig-Pauka I, Metzler-Zebeli BU. Soaking in lactic acid lowers the phytate-phosphorus content and increases the resistant starch in wheat and corn grains. Anim Feed Sci Technol 2019;252:115-25. https://doi.org/10.1016/j.anifeedsci.2019.04.013
  10. Beauchemin KA, McGinn SM. Methane emissions from feedlot cattle fed barley or corn diets1. J Anim Sci 2005;83:653-61. https://doi.org/10.2527/2005.833653x
  11. McCleary BV, Monaghan DA. Measurement of resistant starch. J AOAC Int 2002;85:665-75. https://doi.org/10.1093/jaoac/85.3.665
  12. Martinez TF, McAllister TA, Wang Y, Reuter T. Effects of tannic acid and quebracho tannins on in vitro ruminal fermentation of wheat and corn grain. J Sci Food Agric 2006;86:1244-56. https://doi.org/10.1002/jsfa.2485
  13. National Research Council (NRC). Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids. Washington, DC, USA: National Academic Press; 2007.
  14. Tian K, Liu J, Sun Y, et al. Effects of dietary supplementation of inulin on rumen fermentation and bacterial microbiota, inflammatory response and growth performance in finishing beef steers fed high or low-concentrate diet. Anim Feed Sci Technol 2019;258:114299. https://doi.org/10.1016/j.anifeedsci.2019.114299
  15. Horwitz W; AOAC International. Official methods of analysis of AOAC International. 18th ed. Gaithersburg, MD, USA: AOAC International; 2005.
  16. Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 1991;74:3583-97. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
  17. Koehler LH. Differentiation of carbohydrates by anthrone reaction rate and color intensity. Anal Chem 1952;24:1576-9. https://doi.org/10.1021/ac60070a014
  18. Aldian D, Harisa LD, Mitsuishi H, Tian K, Iwasawa A, Yayota M. Diverse forage improves lipid metabolism and antioxidant capacity in goats, as revealed by metabolomics. Animal 2023;17:100981. https://doi.org/10.1016/j.animal.2023.100981
  19. Moss AR, Jouany JP, Newbold J. Methane production by ruminants: its contribution to global warming. Ann Zootech 2000;49:231-53. https://doi.org/10.1051/animres:2000119
  20. Pang Z, Zhou G, Ewald J, et al. Using MetaboAnalyst 5.0 for LC-HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics data. Nat Protoc 2022;17:1735-61. https://doi.org/10.1038/s41596-022-00710-w
  21. Mickdam E, Khiaosa-ard R, Metzler-Zebeli BU, et al. Modulation of ruminal fermentation profile and microbial abundance in cows fed diets treated with lactic acid, without or with inorganic phosphorus supplementation. Anim Feed Sci Technol 2017;230:1-12. https://doi.org/10.1016/j.anifeedsci.2017.05.017
  22. Zhu JH, Haase NU, Kempf W. Investigations on the laboratory scale separation of mung bean starch. Starch-Starke 1990;42:1-4. https://doi.org/10.1002/star.19900420102
  23. Dailey OD. Effect of lactic acid on protein solubilization and starch yield in corn wet-mill steeping: a study of hybrid effects. Cereal Chem 2002;79:257-60. https://doi.org/10.1094/CCHEM.2002.79.2.257
  24. Vandenbergh PA. Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol Rev 1993;12:221-37. https://doi.org/10.1111/j.1574-6976.1993.tb00020.x
  25. Skrede G, Herstad O, Sahlstrom S, Holck A, Slinde E, Skrede A. Effects of lactic acid fermentation on wheat and barley carbohydrate composition and production performance in the chicken. Anim Feed Sci Technol 2003;105:135-48. https://doi.org/10.1016/S0377-8401(03)00055-5
  26. Humer E, Zebeli Q. Grains in ruminant feeding and potentials to enhance their nutritive and health value by chemical processing. Anim Feed Sci Technol 2017;226:133-51. https://doi.org/10.1016/j.anifeedsci.2017.02.005
  27. Sajilata MG, Singhal RS, Kulkarni PR. Resistant starch-a review. Compr Rev Food Sci Food Saf 2006;5:1-17. https://doi.org/10.1111/j.1541-4337.2006.tb00076.x
  28. Harder H, Khol-Parisini A, Zebeli Q. Modulation of resistant starch and nutrient composition of barley grain using organic acids and thermal cycling treatments. Starch-Starke 2015;67:654-62. https://doi.org/10.1002/star.201500040
  29. Iqbal S, Zebeli Q, Mazzolari A, Dunn SM, Ametaj BN. Feeding rolled barley grain steeped in lactic acid modulated energy status and innate immunity in dairy cows. J Dairy Sci 2010;93:5147-56. https://doi.org/10.3168/jds.2010-3118
  30. Serna-Saldivar SO, Mezo-Villanueva M. Effect of a cell-wall-degrading enzyme complex on starch recovery and steeping requirements of sorghum and maize. Cereal Chem 2003;80:148-53. https://doi.org/10.1094/CCHEM.2003.80.2.148
  31. Tian KE, Luo G, Aldian D, Yayota M. Treatment of corn with lactic acid delayed in vitro ruminal degradation without compromising fermentation: a biological and morphological monitoring study. Front Vet Sci 2024;11:1336800. https://doi.org/10.3389/fvets.2024.1336800
  32. Hellebois T, Gaiani C, Planchon S, Renaut J, Soukoulis C. Impact of heat treatment on the acid induced gelation of brewers' spent grain protein isolate. Food Hydrocoll 2021;113:106531. https://doi.org/10.1016/j.foodhyd.2020.106531
  33. Pereira AM, de Lurdes Nunes Enes Dapkevicius M, Borba AES. Alternative pathways for hydrogen sink originated from the ruminal fermentation of carbohydrates: which microorganisms are involved in lowering methane emission? Anim Microbiome 2022;4:5. https://doi.org/10.1186/s42523-021-00153-w
  34. Harder H, Khol-Parisini A, Metzler-Zebeli BU, Klevenhusen F, Zebeli Q. Treatment of grain with organic acids at 2 different dietary phosphorus levels modulates ruminal microbial community structure and fermentation patterns in vitro. J Dairy Sci 2015;98:8107-20. https://doi.org/10.3168/jds.2015-9913
  35. Newbold CJ, de la Fuente G, Belanche A, Ramos-Morales E, McEwan NR. The role of ciliate protozoa in the rumen. Front Microbiol 2015;6:1313. https://doi.org/10.3389/fmicb.2015.01313
  36. Petrova P, Petrov K. Lactic acid fermentation of cereals and pseudocereals: ancient nutritional biotechnologies with modern applications. Nutrients 2020;12:1118. https://doi.org/10.3390/nu12041118
  37. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc 2003;62:67-72. https://doi.org/10.1079/PNS2002207
  38. Tie S, Zhang L, Li B, et al. Effect of dual targeting procyanidins nanoparticles on metabolomics of lipopolysaccharide-stimulated inflammatory macrophages. Food Sci Hum Wellness 2023;12:2252-62. https://doi.org/10.1016/j.fshw.2023.03.045
  39. Chen XB, Gomes MJ. Estimation of microbial protein supply to sheep and cattle based on urinary excretion of purine derivatives: an overview of the technical details. Aberdeen, UK: International Feed Resources Unit, Rowett Research Institute; 1992.
  40. Broquist HP. Lysine-pipecolic acid metabolic relationships in microbes and mammals. Annu Rev Nutr 1991;11:435-48. https://doi.org/10.1146/annurev.nu.11.070191.002251
  41. Wood JD, Richardson RI, Nute GR, et al. Effects of fatty acids on meat quality: a review. Meat Sci 2004;66:21-32. https://doi.org/10.1016/S0309-1740(03)00022-6
  42. Liu H, Chen Y, Ming D, et al. Integrative analysis of indirect calorimetry and metabolomics profiling reveals alterations in energy metabolism between fed and fasted pigs. J Anim Sci Biotechnol 2018;9:41. https://doi.org/10.1186/s40104-018-0257-x