Browse > Article
http://dx.doi.org/10.5713/ajas.15.0078

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)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.28, no.9, 2015 , pp. 1362-1370 More about this Journal
Abstract
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.
Keywords
Dietary Crude Protein; Pig Slurry; Phenols; Indoles; Volatile Fatty Acids; Bacterial Community;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
11 Duncan, D. B. 1955. Multiple range and multiple F tests. Biometrics 11:1-42.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI
14 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.   DOI
15 Gaskins, H. R. 2001. Intestinal bacteria and their influence on swine growth. CRC Press, Boca Raton, FL, USA.
16 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.   DOI   ScienceOn
17 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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI
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.   DOI   ScienceOn
22 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.   DOI   ScienceOn
23 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.   DOI   ScienceOn
24 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.   DOI   ScienceOn
25 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.   DOI   ScienceOn
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 Ramakrishna, B. S. 2013. Role of the gut microbiota in human nutrition and metabolism. J. Gastroenterol. Hepatol. 28(S4):9-17.   DOI   ScienceOn
33 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.   DOI   ScienceOn
34 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.
35 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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI
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.   DOI   ScienceOn
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.   DOI   ScienceOn
49 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.   DOI   ScienceOn
50 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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI