Asian-Australasian Journal of Animal Sciences

  • 제28권9호
  • /
  • Pages.1362-1370
  • /
  • 2015
  • /
  • 1011-2367(pISSN)
  • /
  • 1976-5517(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
권호 표지
DOI QR코드

DOI QR Code

Effect of Dietary Protein Levels on Composition of Odorous Compounds and Bacterial Ecology in Pig Manure

  • Cho, Sungback (National Institute of Animal Science, Rural Development Administration) ;
  • Hwang, Okhwa (National Institute of Animal Science, Rural Development Administration) ;
  • Park, Sungkwon (Department of Food Science and Technology, Sejong University)
  • 투고 : 2015.01.29
  • 심사 : 2015.04.03
  • 발행 : 2015.09.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

This study was performed to investigate the effect of different levels of dietary crude protein (CP) on composition of odorous compounds and bacterial communities in pig manure. A total of 48 male pigs (average initial body weight 45 kg) fed diets containing three levels of dietary CP (20%, 17.5%, and 15%) and their slurry samples were collected from the pits under the floor every week for one month. Changes in composition of odorous compounds and bacterial communities were analyzed by gas chromatography and 454 FLX titanium pyrosequencing systems, respectively. Levels of phenols, indoles, short chain fatty acid and branched chain fatty acid were lowest (p<0.05) in CP 15% group among three CP levels. Relative abundance of Bacteroidetes phylum and bacterial genera including Leuconostoc, Bacillus, Atopostipes, Peptonphilus, Ruminococcaceae_uc, Bacteroides, and Pseudomonas was lower (p<0.05) in CP 15% than in CP 20% group. There was a positive correlation (p<0.05) between odorous compounds and bacterial genera: phenol, indole, iso-butyric acid, and iso-valeric acid with Atopostipes, p-cresol and skatole with Bacteroides, acetic acid and butyric acid with AM982595_g of Porphyromonadaceae family, and propionic acid with Tissierella. Taken together, administration of 15% CP showed less production of odorous compounds than 20% CP group and this result might be associated with the changes in bacterial communities especially whose roles in protein metabolism.

키워드

참고문헌

  1. Aarnink, A. J. A. 1997. Ammonia emission from houses for growing pigs as affected by pen design, indoor climate and behaviour. Droevendaalsesteeg PB Wageningen, Netherlands.
  2. Alam, M. J., C. D. Jeong, L. L. Mamuad, H. G. Sung, D. W. Kim, S. B. Cho, K. Lee, C. O. Jeon, and S. S. Lee. 2012. Bacterial community dynamics during swine in vitro fermentation using starch as a substrate with different feed additives for odor reduction. Asian Australas. J. Anim. Sci. 25:690-700. https://doi.org/10.5713/ajas.2011.11451
  3. Chen, G. J. and J. B. Russell. 1988. Fermentation of peptides and amino acids by a monensin-sensitive ruminal Peptostreptococcus. Appl. Environ. Microbiol. 54:2742-2749.
  4. Chun, J., K. Y. Kim, J.-H. Lee, and Y. Choi. 2010. The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol. 10:101. https://doi.org/10.1186/1471-2180-10-101
  5. Chung, K. T., G. M. Anderson, and G. E. Fulk. 1975. Formation of indoleacetic acid by intestinal anaerobes. J. Bacteriol. 124:573-575.
  6. Cook, K. L., M. J. Rothrock, J. H. Loughrin, and K. C. Doerner. 2007. Characterization of skatole-producing microbial populations in enriched swine lagoon slurry. FEMS Microbiol. Ecol. 60:329-340. https://doi.org/10.1111/j.1574-6941.2007.00299.x
  7. Cotta, M. A., T. R. Whitehead, M. D. Collins, and P. A. Lawson. 2004. Atopostipes suicloacale gen. nov., sp. nov., isolated from an underground swine manure storage pit. Anaerobe 10:191-195. https://doi.org/10.1016/j.anaerobe.2004.04.001
  8. David, L. A., C. F. Maurice, R. N. Carmody, D. B. Gootenberg, J. E. Button, B. E. Wolfe, A. V. Ling, A. S. Devlin, Y. Varma, and M. A. Fischbach et al. 2013. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559-563. https://doi.org/10.1038/nature12820
  9. Davila, A.-M., F. Blachier, M. Gotteland, M. Andriamihaja, P.-H. Benetti, Y. Sanz, and D. Tome. 2013. Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host. Pharmacol. Res. 68:95-107. https://doi.org/10.1016/j.phrs.2012.11.005
  10. Dourmad, J.-Y. and C. Jondreville. 2007. Impact of nutrition on nitrogen, phosphorus, Cu and Zn in pig manure, and on emissions of ammonia and odours. Livest. Sci. 112:192-198. https://doi.org/10.1016/j.livsci.2007.09.002
  11. Duncan, D. B. 1955. Multiple range and multiple F tests. Biometrics 11:1-42. https://doi.org/10.2307/3001478
  12. Edgar, R. C., B. J. Haas, J. C. Clemente, C. Quince, and R. Knight. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 27:2194-2200. https://doi.org/10.1093/bioinformatics/btr381
  13. Edwards, J. E., N. R. McEwan, A. J. Travis, and R. J. Wallace. 2004. 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie Van Leeuwenhoek 86:263-281. https://doi.org/10.1023/B:ANTO.0000047942.69033.24
  14. Gaskins, H. R. 2001. Intestinal bacteria and their influence on swine growth. CRC Press, Boca Raton, FL, USA.
  15. Gill, S. R., M. Pop, R. T. DeBoy, P. B. Eckburg, P. J. Turnbaugh, B. S. Samuel, J. I. Gordon, D. A. Relman, C. M. Fraser-Liggett, and K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355-1359. https://doi.org/10.1126/science.1124234
  16. Hamady, M., J. J. Walker, J. K. Harris, N. J. Gold, and R. Knight. 2008. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5:235-237. https://doi.org/10.1038/nmeth.1184
  17. Harms, C., A. Schleicher, M. D. Collins, and J. R. Andreesen. 1998. Tissierella creatinophila sp. nov., a Gram-positive, anaerobic, non-spore-forming, creatinine-fermenting organism. Int. J. Syst. Bacteriol. 48:983-993. https://doi.org/10.1099/00207713-48-3-983
  18. Hernandez, F., S. Martinez, C. Lopez, M. D. Megias, M. Lopez, and J. Madrid. 2011. Effect of dietary crude protein levels in a commercial range, on the nitrogen balance, ammonia emission and pollutant characteristics of slurry in fattening pigs. Animal. 5:1290-1298. https://doi.org/10.1017/S1751731111000115
  19. Hobbs, P. J., B. F. Pain, R. M. Kay, and P. A. Lee. 1996. Reduction of odorous compounds in fresh pig slurry by dietary control of crude protein. J. Sci. Food Agric. 71:508-514. https://doi.org/10.1002/(SICI)1097-0010(199608)71:4<508::AID-JSFA610>3.0.CO;2-0
  20. Jensen, B. B. and H. Jorgensen. 1994. Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl. Environ. Microbiol. 60:1897-1904.
  21. Keseler, I. M., A. Mackie, M. Peralta-Gil, A. Santos-Zavaleta, S. Gama-Castro, C. Bonavides-Martinez, C. Fulcher, A. M. Huerta, A. Kothari, and M. Krummenacker et al. 2013. EcoCyc: Fusing model organism databases with systems biology. Nucl. Acids Res. 41(D1):D605-D612. https://doi.org/10.1093/nar/gks1027
  22. Kim, O.-S., Y.-J. Cho, K. Lee, S.-H. Yoon, M. Kim, H. Na, S.-C. Park, Y. S. Jeon, J.-H. Lee, H. Yi, S. Won, and J. Chun. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62(Pt 3):716-721. https://doi.org/10.1099/ijs.0.038075-0
  23. Lamendella, R., J. W. Santo Domingo, S. Ghosh, J. Martinson, and D. B. Oerther. 2011. Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol. 11:103. https://doi.org/10.1186/1471-2180-11-103
  24. Le, P. D., A. J. A. Aarnink, A. W. Jongbloed, C. M. C. Peet-Schwering, N. W. M. Ogink, and M. W. A. Verstegen. 2007. Effects of dietary crude protein level on odour from pig manure. Animal 1:734-744. https://doi.org/10.1017/S1751731107710303
  25. Le, P. D., A. J. A. Aarnink, N. W. M. Ogink, P. M. Becker, and M. W. A. Verstegen. 2005. Odour from animal production facilities: its relationship to diet. Nutr. Res. Rev. 18:3-30. https://doi.org/10.1079/NRR200592
  26. Macfarlane, S. M. G. T. and G. T. Macfarlane. 1995. Proteolysis and amino acid fermentation. CRC Press, Boca Raton, FL, USA.
  27. MAFRA. 2010. Ministry of agriculture, food and rural affairs annual report 2010. Ministry of Agriculture Food and Rural Affairs, Sejong, Korea.
  28. MAFRA. 2013. Ministry of agriculture, food and rural affairs annual report 2013. Ministry of Agriculture Food and Rural Affairs, Sejong, Korea.
  29. MEV. 2011. Law on livestock excretions management and usage. Ministry of Environment, Sejong, Korea.
  30. MEV. 2012. Law on offensive odor control. Ministry of Environment, Sejong, Korea.
  31. NIAS. 2012. Korean feeding standard, swine. National Institute of Animal Science, Wanju, Korea.
  32. Norrapoke, T., M. Wanapat, and S. Wanapat. 2012. Effects of protein level and mangosteen peel pellets (Mago-pel) in concentrate diets on rumen fermentation and milk production in lactating dairy crossbreds. Asian Australas. J. Anim. Sci. 25: 971-979. https://doi.org/10.5713/ajas.2012.12053
  33. Otto, E. R., M. Yokoyama, S. Hengemuehle, R. D. Von Bermuth, T. Van Kempen, and N. L. Trottier. 2003a. Ammonia, volatile fatty acids, phenolics, and odor offensiveness in manure from growing pigs fed diets reduced in protein concentration. J. Anim. Sci. 81:1754-1763.
  34. Parker, D. B., J. Gilley, B. Woodbury, K.-H. Kim, G. Galvin, S. L. Bartelt-Hunt, X. Li and D. D. Snow. 2013. Odorous VOC emission following land application of swine manure slurry. Atmos. Environ. 66:91-100. https://doi.org/10.1016/j.atmosenv.2012.01.001
  35. Ramakrishna, B. S. 2013. Role of the gut microbiota in human nutrition and metabolism. J. Gastroenterol. Hepatol. 28(S4):9-17. https://doi.org/10.1111/jgh.12294
  36. Riepe, S. P., J. Goldstein, and D. H. Alpers. 1980. Effect of secreted Bacteroides proteases on human intestinal brush border hydrolases. J. Clin. Invest. 66:314-322. https://doi.org/10.1172/JCI109859
  37. Rist, V. T. S., E. Weiss, M. Eklund, and R. Mosenthin. 2013. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: A review. Animal 7:1067-1078. https://doi.org/10.1017/S1751731113000062
  38. Sorensen, P. and J. A. Fernandez. 2003. Dietary effects on the composition of pig slurry and on the plant utilization of pig slurry nitrogen. J. Agric. Sci. 140:343-355. https://doi.org/10.1017/S0021859603003113
  39. Sakamoto, M., A. Takagaki, K. Matsumoto, Y. Kato, K. Goto, and Y. Benno. 2009. Butyricimonas synergistica gen. nov., sp. nov. and Butyricimonas virosa sp. nov., butyric acid-producing bacteria in the family 'Porphyromonadaceae' isolated from rat faeces. Int. J. Syst. Evol. Microbiol. 59:1748-1753. https://doi.org/10.1099/ijs.0.007674-0
  40. SAS. 2002. SAS/STAT Software, Version 9.1. SAS Institute Inc., Cary, NC, USA.
  41. Schiffman, S. S., J. L. Bennett, and J. H. Raymer. 2001. Quantification of odors and odorants from swine operations in North Carolina. Agric. Forest Meteorol. 108:213-240. https://doi.org/10.1016/S0168-1923(01)00239-8
  42. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley, D. H. Parks, and C. J. Robinson et al. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. https://doi.org/10.1128/AEM.01541-09
  43. Scott, K. P., S. W. Gratz, P. O. Sheridan, H. J. Flint, and S. H. Duncan. 2013. The influence of diet on the gut microbiota. Pharmacol. Res. 69:52-60. https://doi.org/10.1016/j.phrs.2012.10.020
  44. Smith, E. A. and G. T. Macfarlane. 1998. Enumeration of amino acid fermenting bacteria in the human large intestine: effects of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiol. Ecol. 25:355-368. https://doi.org/10.1111/j.1574-6941.1998.tb00487.x
  45. Starrenburg, M. J. C. and J. Hugenholtz. 1991. Citrate fermentation by Lactococcus and Leuconostoc spp. Appl. Environ. Microbiol. 57:3535-3540.
  46. Sutton, A. L., K. B. Kephart, M. W. Verstegen, T. T. Canh, and P. J. Hobbs. 1999. Potential for reduction of odorous compounds in swine manure through diet modification. J. Anim. Sci. 77:430-439.
  47. Trabue, S. L., J. C. Anhalt, and J. A. Zahn. 2006. Bias of tedlar bags in the measurement of agricultural odorants. J. Environ. Qual. 35:1668-1677. https://doi.org/10.2134/jeq2005.0370
  48. Trabue, S. L., K. Scoggin, F. Mitloehner, H. Li, R. Burns, and H. Xin. 2008a. Field sampling method for quantifying volatile sulfur compounds from animal feeding operations. Atmos. Environ. 42:3332-3341. https://doi.org/10.1016/j.atmosenv.2007.03.016
  49. Trabue, S. L., K. D. Scoggin, H. Li, R. Burns, and H. Xin. 2008b. Field sampling method for quantifying odorants in humid environments. Environ. Sci. Technol. 42:3745-3750. https://doi.org/10.1021/es7031407
  50. Van der Meulen, R., N. Camu, T. Van Vooren, C. Heymans, and L. De Vuyst. 2008. In vitro kinetic analysis of carbohydrate and aromatic amino acid metabolism of different members of the human colon. Int. J. Food Microbiol. 124:27-33. https://doi.org/10.1016/j.ijfoodmicro.2008.02.013
  51. Wadud, S. J. 2011. Understanding the microbial ecology of chicken litter in the context of odour production. Ph.D. Thesis. The university of new south wales, Sydney, Australia.
  52. Zhu, J. 2000. A review of microbiology in swine manure odor control. Agric. Ecosyst. Environ. 78:93-106. https://doi.org/10.1016/S0167-8809(99)00116-4
  53. Ziemer, C. J. 2013. Broad diversity and newly cultured bacterial isolates from enrichment of pig feces on complex polysaccharides. Microb. Ecol. 66:448-461. https://doi.org/10.1007/s00248-013-0185-4
  54. Ziemer, C. J., B. J. Kerr, S. L. Trabue, H. Stein, D. A. Stahl, and S. K. Davidson. 2009. Dietary protein and cellulose effects on chemical and microbial characteristics of swine feces and stored manure. J. Environ. Qual. 38:2138-2146. https://doi.org/10.2134/jeq2008.0039
  55. Ziganshin, A. M., T. Schmidt, F. Scholwin, O. N. Il'inskaya, H. Harms, and S. Kleinsteuber. 2011. Bacteria and archaea involved in anaerobic digestion of distillers grains with solubles. Appl. Microbiol. Biotechnol. 89:2039-2052. https://doi.org/10.1007/s00253-010-2981-9

피인용 문헌

  1. Nutritional effects on odour emissions in broiler production vol.73, pp.02, 2017, https://doi.org/10.1017/S0043933917000046
  2. Nutrition and feed approach according to pig physiology vol.43, pp.5, 2015, https://doi.org/10.7744/kjoas.20160078
  3. The Mode of Action of Chicory Roots on Skatole Production in Entire Male Pigs Is neither via Reducing the Population of Skatole-Producing Bacteria nor via Increased Butyrate Production in the Hindgut vol.85, pp.6, 2015, https://doi.org/10.1128/aem.02327-18
  4. Changes in the Ileal, but Not Fecal, Microbiome in Response to Increased Dietary Protein Level and Enterotoxigenic Escherichia coli Exposure in Pigs vol.85, pp.19, 2015, https://doi.org/10.1128/aem.01252-19
  5. Influence of Sargassum horneri Mitigating Odorous Gas Emissions from Swine Manure Storage Facilities vol.12, pp.18, 2015, https://doi.org/10.3390/su12187587
  6. Hepatoprotective Effect of Cereal Vinegar Sediment in Acute Liver Injury Mice and Its Influence on Gut Microbiota vol.8, pp.None, 2015, https://doi.org/10.3389/fnut.2021.798273
  7. Dietary turmeric (Curcuma longa L.) supplementation improves growth performance, short-chain fatty acid production, and modulates bacterial composition of weaned piglets vol.63, pp.3, 2015, https://doi.org/10.5187/jast.2021.e55
  8. Dietary protein sources and their effects on faecal odour and the composition of volatile organic compounds in faeces of French Bulldogs vol.105, pp.suppl, 2015, https://doi.org/10.1111/jpn.13605