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Quantitative evaluation of ruminal methane and carbon dioxide formation from formate through C-13 stable isotope analysis in a batch culture system

Published online by Cambridge University Press:  12 April 2018

Z. X. He ,
J. Y. Qiao ,
Q. X. Yan ,
Z. L. Tan  and
M Wang
Z. X. He
Affiliation:
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, P.R. China National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan 410125, P.R. China Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Hunan 410125, P.R. China Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
J. Y. Qiao
Affiliation:
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, P.R. China Institute of Commercial Crop, Shanxi Academy of Agricultural Sciences, Fenyang, Shanxi 032200, P.R. China
Q. X. Yan
Affiliation:
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
Z. L. Tan
Affiliation:
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, P.R. China National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan 410125, P.R. China Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Hunan 410125, P.R. China Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
M Wang*
Affiliation:
Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Hunan 410125, P.R. China National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan 410125, P.R. China Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Hunan 410125, P.R. China Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
*
†E-mail: wing_mail@hotmail.com
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Abstract

Methane produced from formate is one of the important methanogensis pathways in the rumen. However, quantitative information of CH4 production from formate has been rarely reported. The aim of this study was to characterize the conversion rate (CR) of formic acid into CH4 and CO2 by rumen microorganisms. Ground lucerne hay was incubated with buffered ruminal fluid for 6, 12, 24 and 48 h. Before the incubation, 13C-labeled H13COOH was also supplied into the incubation bottle at a dose of 0, 1.5, 2.2 or 2.9 mg/g of DM substrate. There were no interactions (P>0.05) between dose and incubation time for all variables evaluated. When expressed as an absolute amount (ml in gas sample) or a relative CR (%), both 13CH4 and 13CO2 production quadratically increased (P<0.01) with the addition of H13COOH. The total 13C (13CH4 and 13CO2) CR was also quadratically increased (P<0.01) when H13COOH was added. Moreover, formate addition linearly decreased (P<0.031) the concentrations of NH3-N, total and individual volatile fatty acids (acetate, propionate and butyrate), and quadratically decreased (P<0.014) the populations of protozoa, total methanogens, Methanosphaera stadtmanae, Methanobrevibacter ruminantium M1, Methanobrevibacter smithii and Methanosarcina barkeri. In summary, formate affects ruminal fermentation and methanogenesis, as well as the rumen microbiome, in particular microorganisms which are directly or indirectly involved in ruminal methanogenesis. This study provides quantitative verification for the rapid dissimilation of formate into CH4 and CO2 by rumen microorganisms.

Keywords

fermentationformatemethanogenesismethanogensrumen
Type
Research Article
Information
animal , Volume 13 , Issue 1 , January 2019 , pp. 90 - 97
Copyright
© The Animal Consortium 2018 

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Footnotes

a

This author contributed equally to this work as co-first author.

References

Annison, E 1954. Studies on the volatile fatty acids of sheep blood with special reference to formic acid. Biochemical Journal 58, 670–680.Google Scholar
Association of Official Analytical Chemists (AOAC) 1995. Official methods of analyses, 16th edition. AOAC, Arlington, VA, USA.Google Scholar
Bento, CBP, Azevedo, AC, Gomes, DI, Batista, ED, Rufino, LMA, Detmann, E and Mantovani, HC 2016. Effect of protein supplementation on ruminal parameters and microbial community fingerprint of Nellore steers fed tropical forages. Animal 10, 44–54.Google Scholar
Carroll, E and Hungate, R 1955. Formate dissimilation and methane production in bovine rumen contents. Archives of Biochemistry and Biophysics 56, 525–536.Google Scholar
Ellis, JE, Williams, AG and Lloyd, D 1990. Formate and glucose stimulation of methane and hydrogen production in rumen liquor. Current Microbiology 20, 251–254.Google Scholar
Grant, R and Mertens, D 1992. Influence of buffer pH and raw corn starch addition on in vitro fiber digestion kinetics. Journal of Dairy Science 75, 2762–2768.Google Scholar
Gray, F, Pilgrim, A, Rodda, H and Weller, R 1952. Fermentation in the rumen of the sheep. Journal of Experimental Biology 29, 57–65.Google Scholar
He, Z, Ding, S, Xu, L, Beauchemin, KA and Yang, W 2013. Using exogenous enzymes to increase the rumen degradability of wheat dried distillers grains with solubles. Archives of Animal Nutrition 67, 381–392.Google Scholar
He, Z, Yang, L, Yang, W, Beauchemin, K, Tang, S, Huang, J, Zhou, C, Han, X, Wang, M and Kang, J 2015. Efficacy of exogenous xylanases for improving in vitro fermentation of forages. The Journal of Agricultural Science 153, 538–553.Google Scholar
Hegarty, R 1999. Reducing rumen methane emissions through elimination of rumen protozoa. Crop and Pasture Science 50, 1321–1328.Google Scholar
Hegarty, R, Bird, S, Vanselow, B and Woodgate, R 2008. Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs. British Journal of Nutrition 100, 1220–1227.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
Janssen, PH and Kirs, M 2008. Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 3619–3625.Google Scholar
Kara, K, Aktuğ, E, Çağri, A, Güçlü, BK and Baytok, E 2015. Effect of formic acid on in vitro ruminal fermentation and methane emission. Turkish Journal of Agriculture-Food Science and Technology 3, 856–860. (Abstract English).Google Scholar
Kara, K, Özkaya, S, Erbaş, S and Baytok, E 2018. Effect of dietary formic acid on the in vitro ruminal fermentation parameters of barley-based concentrated mix feed of beef cattle. Journal of Applied Animal Research 46, 178–183.Google Scholar
Lewis, D 1951. The metabolism of nitrate and nitrite in the sheep. 2. Hydrogen donators in nitrate reduction by rumen micro-organisms in vitro . Biochemical Journal 49, 149–153.Google Scholar
Martinez-Fernandez, G, Denman, SE, Cheung, J and McSweeney, CS 2017. Phloroglucinol degradation in the rumen promotes the capture of excess hydrogen generated from methanogenesis inhibition. Frontiers in Microbiology 8, 1871.Google Scholar
Martinez-Fernandez, G, Denman, SE, Yang, C, Cheung, J, Mitsumori, M and McSweeney, CS 2016. Methane inhibition alters the microbial community, hydrogen flow, and fermentation response in the rumen of cattle. Frontiers in Microbiology 7, 1122.Google Scholar
Olijhoek, DW, Hellwing, ALF, Brask, M, Weisbjerg, MR, Højberg, O, Larsen, MK, Dijkstra, J, Erlandsen, EJ and Lund, P 2016. Effect of dietary nitrate level on enteric methane production, hydrogen emission, rumen fermentation, and nutrient digestibility in dairy cows. Journal of Dairy Science 99, 6191–6205.Google Scholar
Owens, FN and Basalan, M 2016. Ruminal fermentation. In Rumenology (ed. D Millen, MDB Arrigoni and RDL Pacheco), pp. 63–102. Springer International Publishing Switzerland, Cham, Switzerland.Google Scholar
Poulsen, M, Schwab, C, Jensen, BB, Engberg, RM, Spang, A, Canibe, N, Højberg, O, Milinovich, G, Fragner, L and Schleper, C 2013. Methylotrophic methanogenic thermoplasmata implicated in reduced methane emissions from bovine rumen. Nature Communications 4, 1428.Google Scholar
Qiao, J, Tan, Z, Guan, L, Tang, S, Zhou, C, Han, X, Wang, M, Kang, J and He, Z 2015. Effects of hydrogen in headspace and bicarbonate in media on rumen fermentation, methane production and methanogenic population using in vitro gas production techniques. Animal Feed Science and Technology 206, 19–28.Google Scholar
Sparling, R and Daniels, L 1986. Source of carbon and hydrogen in methane produced from formate by Methanococcus thermolithotrophicus . Journal of Bacteriology 168, 1402–1407.Google Scholar
Sylvester, JT, Karnati, SK, Yu, Z, Morrison, M and Firkins, JL 2004. Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. The Journal of Nutrition 134, 3378–3384.Google Scholar
Tapio, I, Snelling, TJ, Strozzi, F and Wallace, RJ 2017. The ruminal microbiome associated with methane emissions from ruminant livestock. Journal of Animal Science and Biotechnology 8, 7.Google Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Vercoe, J and Blaxter, K 1965. The metabolism of formic acid in sheep. British Journal of Nutrition 19, 523–530.Google Scholar
Wallace, RJ, Rooke, JA, McKain, N, Duthie, CA, Hyslop, JJ, Ross, DW, Waterhouse, A, Watson, M and Roehe, R 2015. The rumen microbial metagenome associated with high methane production in cattle. BMC Genomics 16, 839.Google Scholar
Wang, M, Janssen, PH, Sun, XZ, Muetzel, S, Tavendale, M, Tan, ZL and Pacheco, D 2013. A mathematical model to describe in vitro kinetics of H2 gas accumulation. Animal Feed Science and Technology 184, 1–16.Google Scholar
Wang, M, Sun, XZ, Janssen, PH, Tang, SX and Tan, ZL 2014. Responses of methane production and fermentation pathways to the increased dissolved hydrogen concentration generated by eight substrates in in vitro ruminal cultures. Animal Feed Science and Technology 194, 1–11.Google Scholar
Weatherburn, MW 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39, 971–974.Google Scholar
Yu, Z and Morrison, M 2004. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36, 808–813.Google Scholar
Zhang, HF and Zhang, ZY 1998. Animal nutrition parameters and feeding standard (in Chinese), 2nd edition. China Agriculture Press, Beijing, China.Google Scholar
Zmora, P, Cieslak, A, Jedrejek, D, Stochmal, A, Pers-Kamczyc, E, Oleszek, W, Nowak, A, Szczechowiak, J, Lechniak, D and Szumacher-Strabel, M 2012. Preliminary in vitro study on the effect of xanthohumol on rumen methanogenesis. Archives of Animal Nutrition 66, 66–71.Google Scholar