Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-19T15:40:52.680Z Has data issue: false hasContentIssue false

Effect of dietary fiber on the methanogen community in the hindgut of Lantang gilts

Published online by Cambridge University Press:  07 April 2016

Z. Cao
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China
J. B. Liang
Affiliation:
Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400 Serdang, Malaysia
X. D. Liao*
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China
A. D. G. Wright
Affiliation:
School of Animal and Comparative Biomedical Sciences, College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ 85721, USA
Y. B. Wu
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510642, China
B. Yu
Affiliation:
Agro-Animal Husbandry Co., Ltd., Shenzhen, Guangdong 518023, China
*
Get access

Abstract

The primary objective of this study was to investigate the effect of dietary fiber on methanogenic diversity and community composition in the hindgut of indigenous Chinese Lantang gilts to explain the unexpected findings reported earlier that Lantang gilts fed low-fiber diet (LFD) produced more methane than those fed high-fiber diet (HFD). In total, 12 Lantang gilts (58.7±0.37 kg) were randomly divided into two dietary groups (six replicates (pigs) per group) and fed either LFD (NDF=201.46 g/kg) or HFD (NDF=329.70 g/kg). Wheat bran was the main source of fiber for the LFD, whereas ground rice hull (mixture of rice hull and rice bran) was used for the HFD. Results showed that the methanogens in the hindgut of Lantang gilts belonged to four known species (Methanobrevibacter ruminantium, Methanobrevibacter wolinii, Methanosphaera stadtmanae and Methanobrevibacter smithii), with about 89% of the methanogens belonging to the genus Methanobrevibacter. The 16S ribosomal RNA (rRNA) gene copies of Methanobrevibacter were more than three times higher (P<0.05) for gilts fed LFD (3.31×109 copies/g dry matter (DM)) than gilts fed HFD (1.02×109 copies/g DM). No difference (P>0.05) was observed in 16S rRNA gene copies of Fibrobacter succinogenes between the two dietary groups, and 18S rRNA gene copies of anaerobic fungi in gilts fed LFD were lower than (P<0.05) those fed HFD. To better explain the effect of different fiber source on the methanogen community, a follow-up in vitro fermentation using a factorial design comprised of two inocula (prepared from hindgut content of gilts fed two diets differing in their dietary fiber)×four substrates (LFD, HFD, wheat bran, ground rice hull) was conducted. Results of the in vitro fermentation confirmed that the predominant methanogens belonged to the genus of Methanobrevibacter, and about 23% methanogens was found to be distantly related (90%) to Thermogymnomonas acidicola. In vitro fermentation also seems to suggest that fiber source did change the methanogens community. Although the density of Methanobrevibacter species was positively correlated with CH4 production in both in vivo (P<0.01, r=0.737) and in vitro trials (P<0.05, r=0.854), which could partly explain the higher methane production from gilts fed LFD compared with those in the HFD group. Further investigation is needed to explain how the rice hull affected the methanogens and inhibited CH4 emission from gilts fed HFD.

Type
Research Article
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bindelle, J, Buldgen, A, Boudry, A and Leterme, P 2007. Effect of inoculum and pepsin pancreatin hydrolysis on fiber fermentation measured by the gas production technique in pigs. Animal Feed Science and Technology 132, 111122.Google Scholar
Cao, Y, Takahashi, T, Horiguchi, K, Yoshida, N and Cai, YM 2010. Methane emissions from sheep fed fermented or non-fermented total mixed ration containing whole-crop rice and rice bran. Animal Feed Science and Technology 157, 7278.Google Scholar
Cao, Z, Gong, YL, Liao, XD, Liang, JB, Yu, B and Wu, YB 2013. Effect of dietary fiber on methane production in Chinese Lantang gilts. Livestock Science 157, 191199.Google Scholar
Cao, Z, Liao, XD, Liang, JB, Wu, YB and Yu, B 2012. Diversity of methanogens community in hindgut of grower and finisher pigs. African Journal of Biotechnology 2, 49494955.Google Scholar
Chaucheyras-Durand, F, Masséglia, S, Fonty, G and Forano, E 2010. Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs. Applied and Environmental Microbiology 24, 79317937.Google Scholar
Denman, SE and McSweeney, CS 2006. Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiology Ecology 58, 572582.CrossRefGoogle ScholarPubMed
Goberna, M, Gadermaier, M, García, C, Wett, B and Insam, H 2010. Adaptation of methanogenic communities to the co-fermentation of cattle excreta and olive mill wastes at 37°C and 55°C. Applied and Environmental Microbiology 19, 65646571.Google Scholar
Jayanegara, A, Leiber, F and Kreuzer, M 2012. Meta-455 analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and Animal Nutrition 96, 365375.Google Scholar
Jennifer, UA, David, UF, Wang, SY and Ellender, RD 2007. Development of a swine-specific fecal pollution marker based on host differences in methanogen mcrA genes. Applied and Environmental Microbiology 73, 52095217.Google Scholar
Jensen, BB 1996. Methanogenesis in monogastric animals. Environmental Monitoring and Assessment 42, 99112.Google Scholar
Jørgensen, H 2011. Methane emission from pigs. Faculty of Agricultural Sciences, Aarhus University. https://pure.au.dk/portal/files/43896229/764414_Foelgebrev_DJF_rapport, 11 February 2011, Aarhus DK.Google Scholar
Lee, HJ, Lee, SC, Kim, JD, Oh, YG, Kim, BK, Kim, CW and Kim, KJ 2003. Methane production potential of feed ingredients as measured by in vitro gas test. Asian-Australasian Journal of Animal Sciences 16, 11431150.Google Scholar
Liu, C, Zhu, ZP, Liu, YF, Guo, TJ and Dong, HM 2011. Diversity and abundance of the rumen and fecal methanogens in Altay sheep native to Xinjiang and the influence of diversity on methane emissions. Archives Microbiology 194, 353361.Google Scholar
Liu, H, Vaddella, V and Zhou, D 2011. Effect of chestnut tannins and coconut oil on growth performance, methane emission, ruminal fermentation, and microbial populations in sheep. Journal of Dairy Science 94, 60696077.CrossRefGoogle ScholarPubMed
López, Y, García, A, Karimi, K, Taherzadeh, MJ and Martín, C 2010. Chemical characterization and dilute-acid hydrolysis of rice hulls from an artisan mill. Bioresources 5, 22682277.Google Scholar
Luo, YH, Su, Y, Wright, ADG, Zhang, LL, Smidt, H and Zhu, WY 2012. Lean breed Landrace pigs harbor fecal methanogens at higher diversity and density than obese breed Erhualian pigs. Archaea, 19. http://dx.doi.org/10.1155/2012/605289 CrossRefGoogle ScholarPubMed
Mao, SY, Yang, CF and Zhu, WY 2011. Phylogenetic analysis of methanogens in the pig feces. Current Microbiology 62, 13861389.Google Scholar
Matsui, H, Wakabayashi, H, Fukushima, N, Ito, K, Nishikawa, A, Yoshimi, R, Ogawa, Y, Yoneda, S, Ban-Tokuda, T and Wakita, M 2013. Effect of raw rice bran supplementation on rumen methanogen population density and in vitro rumen fermentation. Grassland Science 59, 129134.Google Scholar
Menke, KH and Steingass, H 1988. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal Research and Development 28, 755.Google Scholar
Miller, TL 1991. Biogenic sources of methane. In Microbial production and consumption of greenhouse gases, methane, nitrogen oxide and halomethanes (ed. Roger JE and Whitman WB), pp. 175188. American Society for Microbiology, Washington, DC, USA.Google Scholar
Miller, TL, Wolin, MJ and Kusel, EA 1986. Isolation and characterization of methanogens from animal feces. Systematic and Applied Microbiology 8, 234238.Google Scholar
Moss, AR, Jouany, JP and Newbold, J 2000. Methane production by ruminants: its contribution to global warming. Annales de Zootechnie 49, 231253.Google Scholar
Pei, CX, Mao, SY, Cheng, YF and Zhu, WY 2010. Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle. Animal 4, 2029.Google Scholar
Samuel, BS and Gordon, JI 2006. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proceedings of the National Academy of Sciences of the United States of America 103, 1001110016.CrossRefGoogle ScholarPubMed
Shi, PJ, Meng, K, Zhou, ZG, Wang, YR, Diao, QY and Yao, B 2008. The host species affects the microbial community in the goat rumen. Letters in Applied Microbiology 46, 132135.Google Scholar
Shinoda, M, Singu, H, Kushibiki, S and Ueda, Y 2007. Methane emission from Japanese Black cows fed hay or whole crop rice [Oryza sativa] silage at a maintenance intake level and the effect of concentrate feeding on emission. Bulletin of the National Agricultural Research Center for Tohoku Region, Japan. 108 pp.Google Scholar
Stackebrandt, E and Goebel, BM 1994. Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. International Journal of Systematic Bacteriology 44, 846849.Google Scholar
Steinberg, LM and Regan, JM 2009. McrA-targeted real-time quantitative PCR method to examine methanogen communities. Applied Environmental Microbiology 75, 44354442.Google Scholar
Su, Y, Smidt, H and Zhu, WY 2014. Comparison of fecal methanogenic archaeal community between Erhualian and Landrace pigs using denaturing gradient gel electrophoresis and real-time PCR analysis. Journal of Integrative Agriculture 13, 13401348.Google Scholar
Tan, HY, Abdulah, CC, Liang, N, Huang, XD and Ho, YW 2011. Effect of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro. Animal Feed Science and Technology 169, 185193.CrossRefGoogle Scholar
Varel, VH 1987. Activity of fiber-degrading microorganisms in the pig large intestine. Journal of Animal Science 65, 488496.Google Scholar
Varel, VH and Yen, JT 1997. Microbial perspective on fiber utilization by swine. Journal of Animal Science 75, 27152722.Google Scholar
Varel, VJ and Pond, WG 1985. Enumeration and activity of cellulolytic bacteria from gestating swine fed various levels of dietary fiber. Applied Environmental Microbiology 49, 858862.Google Scholar
Wang, H 2008. Study on enzymatic extraction of rice bran protein and inhibition its browning. Master thesis, Northeast Agricultural University, Harbin, China, pp. 35–46.Google Scholar
Whitehead, TR, Spence, CC and Michael, A 2013. Inhibition of hydrogen sulfide, methane, and total gas production and sulfate-reducing bacteria in in vitro swine manure by tannins, with focus on condensed Quebracho tannins. Applied Microbiology and Biotechnology 97, 84038409.Google Scholar
Whitford, MF, Teather, RM and Forster, RJ 2001. Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiology 1, 157.Google Scholar
Williams, BA, Bosch, MW, Boer, H, Verstegen, MWA and Tamminga, S 2005. An in vitro batch culture method to assess potential fermentability of feed ingredients for monogastric diets. Animal Feed Science and Technology 123–124, 445462.Google Scholar
Wright, ADG and Pimm, C 2003. Improved strategy for presumptive identification of methanogens using 16S riboprinting. Journal of Microbiological Methods 55, 337349.Google Scholar
Wright, ADG, Toovey, AF and Pimm, CL 2006. Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveals more uncultured novel archaea. Anaerobe 12, 134139.Google Scholar
Wright, ADG, Williams, AJ, Winder, B, Christophersen, CT, Rodgers, SL and Smith, KD 2004. Molecular diversity of rumen methanogens from sheep in Western Australia. Applied Environmental Microbiology 70, 12631270.Google Scholar
Yu, Z, García-González, R, Schanbacher, FL and Morrison, M 2008. Evaluations of different hypervariable regions of archaeal 16S rRNA genes in profiling of methanogens by Archaea-specific PCR and denaturing gradient gel electrophoresis. Applied Environmental Microbiology 74, 889893.Google Scholar