Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T16:55:37.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Cow responses and evolution of the rumen bacterial and methanogen community following a complete rumen content transfer

Published online by Cambridge University Press:  27 December 2018

T. De Mulder Open the ORCID record for T. De Mulder [Opens in a new window] ,
L. Vandaele ,
N. Peiren ,
A. Haegeman ,
T. Ruttink ,
S. De Campeneere ,
T. Van De Wiele  and
K. Goossens
T. De Mulder
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
L. Vandaele
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
N. Peiren
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
A. Haegeman
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Science Unit, Caritasstraat 39, 9090, Melle, Belgium
T. Ruttink
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Science Unit, Caritasstraat 39, 9090, Melle, Belgium
S. De Campeneere
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
T. Van De Wiele
Affiliation:
Center for Microbial Ecology and Technology (CMET), Ghent University, Coupure Links 653, 9000 Ghent, Belgium
K. Goossens*
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
*
Author for correspondence: K. Goossens, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Understanding the rumen microbial ecosystem requires the identification of factors that influence the community structure, such as nutrition, physiological condition of the host and host–microbiome interactions. The objective of the current study was to describe the rumen microbial communities before, during and after a complete rumen content transfer. The rumen contents of one donor cow were removed completely and used as inoculum for the emptied rumen of the donor itself and three acceptor cows under identical physiological and nutritional conditions. Temporal changes in microbiome composition and rumen function were analysed for each of four cows over a period of 6 weeks. Shortly after transfer, the cows showed different responses to perturbation of their rumen content. Feed intake depression in the first 2 weeks after transfer resulted in short-term changes in milk production, methane emission, fatty acid composition and rumen bacterial community composition. These effects were more pronounced in two cows, whose microbiome composition showed reduced diversity. The fermentation metrics and microbiome diversity of the other two cows were not affected. Their rumen bacterial community initially resembled the composition of the donor but evolved to a new community profile that resembled neither the donor nor their original composition. Descriptive data presented in the current paper show that the rumen bacterial community composition can quickly recover from a reduction in microbiome diversity after a severe perturbation. In contrast to the bacteria, methanogenic communities were more stable over time and unaffected by stress or host effects.

Keywords

Bacteriamethanemethanogensrumenvolatile fatty acids
Type
Animal Research Paper
Information
The Journal of Agricultural Science , Volume 156 , Issue 8 , October 2018 , pp. 1047 - 1058
Copyright
Copyright © Cambridge University Press 2018 

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

AlZahal, O, Li, F, Guan, LL, Walker, ND and McBride, BW (2017) Factors influencing ruminal bacterial community diversity and composition and microbial fibrolytic enzyme abundance in lactating dairy cows with a focus on the role of active dry yeast. Journal of Dairy Science 100, 4377–4393.Google Scholar
Belanche, A, Doreau, M, Edwards, JE, Moorby, JM, Pinloche, E and Newbold, CJ (2012) Shifts in the rumen microbiota due to the type of carbohydrate and level of protein ingested by dairy cattle are associated with changes in rumen fermentation. Journal of Nutrition 142, 1684–1692.Google Scholar
Castro-Montoya, J, Peiren, N, Cone, JW, Zweifel, B, Fievez, V and De Campeneere, S (2015) In vivo and in vitro effects of a blend of essential oils on rumen methane mitigation. Livestock Science 180, 134–142.Google Scholar
De Boever, JL, Goossens, K, Peiren, N, Swanckaert, J, Ampe, B, Reheul, D, De Brabander, DL, De Campeneere, S and Vandaele, L (2017) The effect of maize silage type on the performances and methane emission of dairy cattle. Journal of Animal Physiology and Animal Nutrition 101, e246–e256.Google Scholar
De Campeneere, S and Peiren, N (2014) ILVO's ruminant respiration facility. In Pinares, C and Waghorn, G (eds), Technical Manual on Respiration Chamber Design. Wellington, New Zealand: Ministry of Agriculture and Forestry, pp. 43–58.Google Scholar
De Mulder, T, Goossens, K, Peiren, N, Vandaele, L, Haegeman, A, De Tender, C, Ruttink, T, Van de Wiele, T and De Campeneere, S (2017) Exploring the methanogen and bacterial communities of rumen environments: solid adherent, fluid and epimural. FEMS Microbiology Ecology 93, article no. fiw251, 1–12. doi: 10.1093/femsec/fiw251.Google Scholar
Getachew, G, Makkar, HPS and Becker, K (2001) Method of polyethylene glycol application to tannin-containing browses to improve microbial fermentation and efficiency of microbial protein synthesis from tannin-containing browses. Animal Feed Science and Technology 92, 51–57.Google Scholar
Gokarn, RR, Eiteman, MA, Martin, SA and Eriksson, KEL (1997) Production of succinate from glucose, cellobiose, and various cellulosic materials by the ruminal anaerobic bacteria Fibrobacter succinogenes and Ruminococcus flavefaciens. Applied Biochemistry and Biotechnology 68, 69–80.Google Scholar
Henderson, G, Cox, F, Ganesh, S, Jonker, A, Young, W, Global Rumen Census Collaborators and Janssen, PH (2015) Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports 5, Article No. 14567, 1–13. http://dx.doi.org/10.1038/srep14567.Google Scholar
Hook, SE, Northwood, KS, Wright, ADG and McBride, BW (2009) Long-term monensin supplementation does not significantly affect the quantity or diversity of methanogens in the rumen of the lactating dairy cow. Applied and Environmental Microbiology 75, 374–380.Google Scholar
Koskella, B and Meaden, S (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses 5, 806–823.Google Scholar
Madsen, J, Bjerg, B, Hvelplund, T, Weisbjerg, M and Lund, P (2010) Methane and carbon dioxide ratio in excreted air for quantification of the methane production from ruminants. Livestock Science 129, 223–227.Google Scholar
McMurdie, PJ and Holmes, S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217, https://doi.org/10.1371/journal.pone.0061217.Google Scholar
Morita, H, Shiratori, C, Murakami, M, Takami, H, Toh, H, Kato, Y, Nakajima, F, Takagi, M, Akita, H, Masaoka, T and Hattori, M (2008) Sharpea azabuensis gen. nov., sp. nov., a Gram-positive, strictly anaerobic bacterium isolated from the faeces of thoroughbred horses. International Journal of Systematic and Evolutionary Microbiology 58, 2682–2686.Google Scholar
Nagaraja, TG and Taylor, MB (1987) Susceptibility and resistance of ruminal bacteria to antimicrobial feed additives. Applied and Environmental Microbiology 53, 1620–1625.Google Scholar
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH and Wagner, H (2015). Package ‘Vegan’: Community Ecology Package. R package version 2.3-2. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://cran.r-project.org/package=veganGoogle Scholar
Ovreas, L, Forney, L, Daae, F and Torsvik, V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Applied and Environmental Microbiology 63, 3367–3373.Google Scholar
Prabhu, R, Altman, E and Eiteman, MA (2012) Lactate and acrylate metabolism by Megasphaera elsdenii under batch and steady-state conditions. Applied and Environmental Microbiology 78, 8564–8570.Google Scholar
Roehe, R, Dewhurst, RJ, Duthie, CA, Rooke, JA, McKain, N, Ross, DW, Hyslop, JJ, Waterhouse, A, Freeman, TC, Watson, M and Wallace, RJ (2016) Bovine host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance. PLoS Genetics 12, e1005846, https://doi.org/10.1371/journal.pgen.1005846.Google Scholar
Russell, JR and Hino, T (1985) Regulation of lactate production in Streptococcus bovis: a spiraling effect that contributes to rumen acidosis. Journal of Dairy Science 68, 1712–1721.Google Scholar
Shi, WB, Moon, CD, Leahy, SC, Kang, DW, Froula, J, Kittelmann, S, Fan, C, Deutsch, S, Gagic, D, Seedorf, H, Kelly, WJ, Atua, R, Sang, C, Soni, P, Li, D, Pinares-Patino, CS, McEwan, JC, Janssen, PH, Chen, F, Visel, A, Wang, Z, Attwood, GT and Rubin, EM (2014) Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Research 24, 1517–1525.Google Scholar
Tajima, K, Aminov, RI, Nagamine, T, Matsui, H, Nakamura, M and Benno, Y (2001) Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Applied and Environmental Microbiology 67, 2766–2774.Google Scholar
Tamminga, S, Van Straalen, WM, Subnel, APJ, Meijer, RGM, Steg, A, Wever, CJG and Blok, MC (1994) The Dutch protein evaluation system – the Dve/Oeb-system. Livestock Production Science 40, 139–155.Google Scholar
Varel, VH and Jung, HJ (1986) Influence of forage phenolics on ruminal fibrolytic bacteria and in vitro fiber degradation. Applied and Environmental Microbiology 52, 275–280.Google Scholar
Vilchez-Vargas, R, Geffers, R, Suárez-Diez, M, Conte, I, Waliczek, A, Kaser, VS, Kralova, M, Junca, H and Pieper, DH (2013) Analysis of the microbial gene landscape and transcriptome for aromatic pollutants and alkane degradation using a novel internally calibrated microarray system. Environmental Microbiology 15, 1016–1039.Google Scholar
Vlaming, JB, Lopez-Villalobos, N, Brookes, IM, Hoskin, SO and Clark, H (2008) Within- and between-animal variance in methane emissions in non-lactating dairy cows. Australian Journal of Experimental Agriculture 48, 124–127.Google Scholar
Weimer, PJ, Stevenson, DM, Mantovani, HC and Man, SLC (2010) Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. Journal of Dairy Science 93, 5902–5912.Google Scholar
Winter, C, Bouvier, T, Weinbauer, MG and Thingstad, TF (2010) Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner’ hypothesis revisited. Microbiology and Molecular Biology Reviews: MMBR 74, 42–57.Google Scholar
Woodward, SL, Waghorn, GC, Ulyatt, MJ and Lassey, KR (2001) Early indications that feeding Lotus will reduce methane emissions from ruminants. Proceedings of the New Zealand Society of Animal Production 61, 23–26.Google Scholar
Yu, Z and Morrison, M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. BioTechniques 36, 808–812.Google Scholar
Supplementary material: File

De Mulder et al. supplementary material

Figures S1-S2

Download De Mulder et al. supplementary material(File)
File 609.1 KB