Effects of Phloroglucinol on In Vitro Methanogenesis, Rumen Fermentation, and Microbial Population Density
Abstract
This study investigated the effect of phloroglucinol (1,3,5-trihydroxybenzene) supplementation alone on methane production, rumen fermentation profiles, and microbial population structure of mixed in vitro cultures. Treatments included a control group containing a substrate with no supplement, and substrates supplemented with 2, 4, 6, 8, or 10 mmol/L of phloroglucinol. The results revealed that phloroglucinol was able to decrease methane production in a dose-dependent manner. The highest decrease was observed with 8 and 10 mmol/L supplementations. The relative quantity of methanogen was not affected by phloroglucinol, whereas genus Coprococcus was increased with increasing concentrations of phloroglucinol (p<0.05). Total gas production, dry matter digestibility (DMD), and NH3-N were significantly lowered by phloroglucinol (p<0.001). Total short-chain fatty acid (SCFA) concentration was not affected by phloroglucinol. Acetate proportion increased with the addition of phloroglucinol at the expense of propionate (p<0.001). This might indicate the redirection of [H] from methane to acetate, and might be related to methane inhibition.. Our study concluded that supplementation of phloroglucinol alone could decrease methane production by inhibiting nutrient digestibility in the rumen and by possible redirection of rumen fermentation to acetate production. Genus Coprococcus could be an important actor for phloroglucinol metabolism in the rumen.
References
Ban-Tokuda, T., S. Maekawa, T. Miwa, S. Ohkawara, & H. Matsui. 2017. Changes in faecal bacteria during fattening in finishing swine. Anaerobes 47:188-193. https://doi.org/10.1016/j.anaerobe.2017.06.006
Broucek, J. 2018. Options to methane production abatement in ruminants: A review. J. Anim. Plant Sci. 28:348-364.
Da Silva, H. E., A. Teterina, E. M. Cornelli, A. Taibi, B. M. Arendt, S. E. Fischer, W. Lou, & J. P. Allard. 2018. Nonalcoholic fatty liver disease is associated with dysibiosis independent of body mass indes and insulin resistance. Sci. Rep. 8(1466): 1-12. https://doi.org/10.1038/s41598-018-19753-9
Dobreva, M. A., R. A. Frazier, I. Mueller-Harvey, L. A. Clifton, A. Gea, & R. J. Green. 2011. Binding of pentagalloyl glucose to two globular proteins occurs via multiple surface sites. Biomacromolecules 12:710-715. https://doi.org/10.1021/bm101341s
Hierholtzer, A., L. Chatellard, M. Kierans, J. C. Akunna, & P. J. Collier. 2012. The impact and mode of action of phenolic compounds extracted from brown seaweed on mixed anaerobic microbial cultures. J. Appl. Microbiol., 114:964-973. https://doi.org/10.1111/jam.12114
Jayanegara, A. 2010. Ruminal methane production on simple phenolic acids addition in in vitro gas production method. Med. Pet. 32:53-62.
Jayanegara, A., & E. Palupi. 2010. Condensed tannin effects on nitrogen digestion in ruminants: a meta-analysis from in vitro and in vivo studies. Med. Pet. 33:176-181. https://doi.org/10.5398/medpet.2010.33.3.176
Jayanegara, A., G. Goel, H. P. S. Makkar, & K. Becker. 2015. Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Anim. Feed Sci. Tech. 209:60-68. https://doi.org/10.1016/j.anifeedsci.2015.08.002
Johnson, K. A., & D. E. Johnson. 1995. Methane emissions from cattle. J. Anim. Sci, 73:2483-2492. https://doi.org/10.2527/1995.7382483x
Kisworo, A. N., A. Agus, Kustantinah, & B. Suwingyo. 2017. Physicochemical characteristics, in vitro fermentation indicators, gas production kinetics, and degradability of solid herbal waste as alternative feed source for ruminants. Med. Pet. 40:101-110. https://doi.org/10.5398/medpet.2017.40.2.101
Klop, G., B. Hatew, A. Bannink, & J. Dijkstra. 2016. Feeding nitrate and docosahexaenoic acid affects enteric methane production and milk fatty acid composition in lactating dairy cows. J. Dairy Sci. 99:1161-1172. https://doi.org/10.3168/jds.2015-10214
Knapp, J. R., G. L. Laur, P. A. Vadas, W. P. Weiss, & J. M. Tricarico. 2014. Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions. J. Dairy Sci. 97:3231-3261. https://doi.org/10.3168/jds.2013-7234
Krumholz, L. R., & M. P. Bryant. 1986. Eubacterium oxidoreducens sp. nov. requiring H2 or formate to degrade gallate, pyrogallol, phloroglucinol and quercetin. Arch. Microbiol. 144:8-14. https://doi.org/10.1007/BF00454948
Lan, W. & C. Yang. 2019. Ruminal methane production: Associated microorganisms and the potential of applying hydrogen-utilizing bacteria for mitigation. Sci. Total Environ. 654:1270-1283. https://doi.org/10.1016/j.scitotenv.2018.11.180
Li, Z., N. Liu, Y. Cao, C. Jin, F. Li, C. Cai, & J. Yao. 2018. Effects of fumaric acid supplementation on methane production and rumen fermentation in goats fed diets varying in forage and concentrate particle size. J. Anim. Sci. Biotechnol. 9:21. https://doi.org/10.1186/s40104-018-0235-3
Lund, P., R. Dahl, H. J. Yang, A. L. F. Hellwing, B. B. Cao, & M. R. Weisbjerg. 2014. The acute effect of addition of nitrate on in vitro and in vivo methane emission in dairy cows. Anim. Prod. Sci. 54:1432-1435. https://doi.org/10.1071/AN14339
Lwin, K. O., M. Kondo, T. Ban-Tokuda, R. M. Lapitan, A. N. Del-Barrio, T. Fujihara, & H. Matsui. 2012. Ruminal fermentation and microbial ecology of buffaloes and cattle fed the same diet. Anim. Sci. J. 83:767-776. https://doi.org/10.1111/j.1740-0929.2012.01031.x
Martin, C., D. Morgavi, & M. Doreau. 2010. Methane mitigation in ruminants: From microbe to the farm scale.Animal 4:351-365. https://doi.org/10.1017/S1751731109990620
Martinez-Fernandez, G., S. E. Denman, J. Cheung, & C. S. McSweeney. 2017. Phloroglucinol degradation in the rumen promotes the capture of excess hydrogen generated from methanogenesis inhibition. Front. Microbiol. 8:1871. https://doi.org/10.3389/fmicb.2017.01871
Matsui, H., H. Wakabayashi, N. Fukushima, K. Ito, A. Nishikawa, R. Yoshimi, Y. Ogawa, S. Yoneda, T. Ban-Tokuda, & M. Wakita. 2013. Effect of raw rice bran supplementation on rumen methanogen population density and in vitro rumen fermentation. Grassl. Sci. 59:129-134. https://doi.org/10.1111/grs.12023
McSweeney, C. S., B. Palmer, D. M. McNeill, & D. O. Krause. 2001. Microbial interactions with tannins: nutritional consequences for ruminants. Anim. Feed Sci. Technol. 91:83-93. https://doi.org/10.1016/S0377-8401(01)00232-2
Mullins, C. R., L. K. Mamedova, A. J. Carpenter, Y. Ying, M. S. Allen, I. Yoon, & B. J. Bradford. 2013. Analysis of rumen microbial populations in lactating dairy cattle fed diets varying in carbohydrate profiles and Saccharomyces cerevisiae fermentation product. J. Dairy Sci. 96:5872-5881. https://doi.org/10.3168/jds.2013-6775
Myhre, G., D. Shindell, F. -M. Bréon, W. Collins, J. Fuglestvedt, J. Huang, D. Koch, J. -F. Lamarque, D. Lee, B. Mendoza, T. Nakajima, A. Robock, G. Stephens, T. Takemura, & H. Zhang. 2013. Anthropogenic and Natural Radiative Forcing. In: Stocker, T. F., D. Qin, G. -K. Plattner, M. Tignor, S. K. Allen, J. Doschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (Eds.). Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge. pp. 659-740.
Patel, T. R., K. G. Jure, & G. A. Jones. 1981. Catabolism of phloroglucinol by the rumen anaerobe Coprococcus. Appl. Environ. Microb. 42:1010-1017.
Patra, A. K., & Z. Yu. 2012. Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Appl. Environ. Microbiol. 78:4271-4280. https://doi.org/10.1128/AEM.00309-12
Sarwono, K. A., M. Kondo, T. Ban-Tokuda, A. Jayanegara, & H. Matsui. 2019. Effects of phloroglucinol and the forage:concentrate ratio on methanogenesis, in vitro rumen fermentation, and microbial population density. Adv. Anim. Vet. Sci. 7:164-171. https://doi.org/10.17582/journal.aavs/2019/7.3.164.171
Schmittgen, T. D., & K. J. Livak. 2008. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3:1101-1108.
Smith, P., H. Clark, H. Dong, E. A. Elsiddig, H. Haberl, R. Harper, J. House, M. Jafari, O. Masera, C. Mbow, N. H. Ravindranath, C. W. Rice, C. Roble Do Abad, A. Romanovskaya, F. Sperling, & F. Tubiello. 2014. Chapter 11 - Agriculture, forestry and other land use (AFOLU). Climate Change 2014: Mitigation of Climate Change. IPCC Working Group III Contribution to AR5. Cambridge University Press, Cambridge.
Song, M. K., X. Z. Li, Y. K. Oh, C. K. Lee, & Y. Hyun. 2011. Control of methane emission in ruminants and industrial application of biogas from livestock manure in korea. Asian-Aust. J. Anim. Sci. 24:130-136. https://doi.org/10.5713/ajas.2011.r.02
Tsai, C. G. & G. A. Jones. 1975. Isolation and identification of rumen bacteria capable of anaerobic phloroglucinol degradation. Can. J. Microbiol. 21:794-801. https://doi.org/10.1139/m75-117
Tsai, C. G., D. M. Gates, W. M. Ingledew, & G. A. Jones. 1976. Products of anaerobic phloroglucinol degradation by Coprococcus sp. Pe15. Can. J. Microbiol. 22:159-64. https://doi.org/10.1139/m76-022
Uddin, M. K., M. Kondo, J. Kita, H. Matsui, S. Karita, M. Goto. 2010. Effect of supplementation of soy sauce cake and vinegar brewer’s cake with total mixed ration silage-based diet on nutrient utilization by Holstein steers. J. Food Agric. Environ. 8:282-287.
Ungerfeld, E. M. 2015. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis. Front. Microbiol. 6:37. https://doi.org/10.3389/fmicb.2015.00538
Zijderveld, van S.M., B. Fonken, J. Dijkstra, W.J. Gerrits, H.B. Perdok, W. Fokkink, & J.R. Newbold. 2011. Effects of a combination of feed additives on methane production, diet digestibility, and animal performance in lactating dairy cows. J. Dairy Sci. 94:1445-1454. https://doi.org/10.3168/jds.2010-3635
Authors
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Authors submitting manuscripts should understand and agree that copyright of manuscripts of the article shall be assigned/transferred to Tropical Animal Science Journal. The statement to release the copyright to Tropical Animal Science Journal is stated in Form A. This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License (CC BY-SA) where Authors and Readers can copy and redistribute the material in any medium or format, as well as remix, transform, and build upon the material for any purpose, but they must give appropriate credit (cite to the article or content), provide a link to the license, and indicate if changes were made. If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original.
Article Details
