Investigating the efficacy of purified tannin extracts from underutilized temperate forages in reducing enteric methane emissions in vitro.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
31 May 2024
Historique:
received: 27 12 2023
accepted: 29 05 2024
medline: 1 6 2024
pubmed: 1 6 2024
entrez: 31 5 2024
Statut: epublish

Résumé

The study investigated how the concentration and composition of purified tannin extracts, at various inclusion rates, affect the ruminal in vitro fermentation parameters. Tannin extracts were isolated from four different forage species: birdsfoot trefoil (Lotus corniculatus), sulla (Hedysarum coronarium), big trefoil (Lotus pedunculatus), and salad burnet (Sanguisorba minor). Plants extracts were purified by Sephadex LH-20 gel chromatography and analyzed by UPLC-ESI-MS/MS. The results showed a large variation among the extracts from different species in terms of tannin composition and structural features. The extracts from salad burnet were dominated by hydrolysable tannins, comprising mainly ellagitannins. The extracts derived from sulla and big trefoil contained predominantly proanthocyanidins (PA), primarily composed of prodelphinidins with high mean degree of polymerisation (mDP). Birdsfoot trefoil extracts comprised procyanidin-rich PAs with low mDP. To determine whether the combined presence of tannins and flavonoid together lead to synergistic or antagonistic effects, the tannin extracts were incubated both with or without rutin at concentrations of 10, 20, and 30 g/kg DM, using a base substrate of perennial ryegrass (Lolium perenne, control). In general, all the tannin extracts decreased methane (CH

Identifiants

pubmed: 38822060
doi: 10.1038/s41598-024-63434-9
pii: 10.1038/s41598-024-63434-9
doi:

Substances chimiques

Tannins 0
Methane OP0UW79H66
Plant Extracts 0
Proanthocyanidins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

12578

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : MA 8199/1-1

Informations de copyright

© 2024. The Author(s).

Références

Gerber, P. J. et al. Tackling Climate Change Through Livestock: A Global Assessment of Emissions and Mitigation Opportunities (Food and Agriculture Organization of the United Nations (FAO), Rome, 2013).
Eugène, M., Klumpp, K. & Sauvant, D. Methane mitigating options with forages fed to ruminants. Grass Forage Sci. 76, 196–204. https://doi.org/10.1111/gfs.12540 (2021).
doi: 10.1111/gfs.12540
Reisinger, A. et al. How necessary and feasible are reductions of methane emissions from livestock to support stringent temperature goals?. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 379, 20200452. https://doi.org/10.1098/rsta.2020.0452 (2021).
doi: 10.1098/rsta.2020.0452
Tubiello, F., Conchedda, G. & Obli-Laryea, G. Emissions from agriculture and forest land Global, regional and country trends 1990–2019 (2021).
Min, B. R. et al. Dietary mitigation of enteric methane emissions from ruminants: A review of plant tannin mitigation options. Anim. Nutr. 6, 231–236. https://doi.org/10.1016/j.aninu.2020.05.002 (2020).
doi: 10.1016/j.aninu.2020.05.002 pubmed: 33005757 pmcid: 7503797
Beauchemin, K. A., Ungerfeld, E. M., Eckard, R. J. & Wang, M. Review: Fifty years of research on rumen methanogenesis: lessons learned and future challenges for mitigation. Animal 14, s2–s16. https://doi.org/10.1017/S1751731119003100 (2020).
doi: 10.1017/S1751731119003100 pubmed: 32024560
van Gastelen, S., Dijkstra, J. & Bannink, A. Are dietary strategies to mitigate enteric methane emission equally effective across dairy cattle, beef cattle, and sheep?. J. Dairy Sci. 102, 6109–6130. https://doi.org/10.3168/jds.2018-15785 (2019).
doi: 10.3168/jds.2018-15785 pubmed: 31079901
Roldan, M. B. et al. Condensed tannins in white clover (Trifolium repens) foliar tissues expressing the transcription factor TaMYB14–1 Bind to forage protein and reduce ammonia and methane emissions in vitro. Front. Plant Sci. https://doi.org/10.3389/fpls.2021.777354 (2022).
doi: 10.3389/fpls.2021.777354 pubmed: 36186081 pmcid: 9523541
Aboagye, I. A. & Beauchemin, K. A. Potential of molecular weight and structure of tannins to reduce methane emissions from ruminants: A review. Animals 9, 856. https://doi.org/10.3390/ani9110856 (2019).
doi: 10.3390/ani9110856 pubmed: 31652766 pmcid: 6912696
Mueller-Harvey, I. et al. Benefits of condensed tannins in forage legumes fed to ruminants: Importance of structure, concentration and diet compsition. Crop Sci. 59, 861–885. https://doi.org/10.2135/cropsci2017.06.0369 (2017).
doi: 10.2135/cropsci2017.06.0369
Lagrange, S. P., MacAdam, J. W. & Villalba, J. J. The use of temperate tannin containing forage legumes to improve sustainability in forage-livestock production. Agronomy 11, 2264. https://doi.org/10.3390/agronomy11112264 (2021).
doi: 10.3390/agronomy11112264
MacAdam, J. W. & Villalba, J. J. Beneficial effects of temperate forage legumes that contain condensed tannins. Agriculture 5, 1–17. https://doi.org/10.3390/agriculture5030475 (2015).
doi: 10.3390/agriculture5030475
Naumann, H. D., Tedeschi, L. O., Zeller, W. E. & Huntley, N. F. The role of condensed tannins in ruminant animal production: advances, limitations and future directions. Rev. Bras. de Zootec. 46, 929–949. https://doi.org/10.1590/s1806-92902017001200009 (2017).
doi: 10.1590/s1806-92902017001200009
Mueller-Harvey, I. Unravelling the conundrum of tannins in animal nutrition and health. J. Sci. Food Agric. 86, 2010–2037. https://doi.org/10.1002/jsfa.2577 (2006).
doi: 10.1002/jsfa.2577
Waghorn, G. Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production-Progress and challenges. Anim. Feed Sci. Technol. 147, 116–139. https://doi.org/10.1016/j.anifeedsci.2007.09.013 (2008).
doi: 10.1016/j.anifeedsci.2007.09.013
Rira, M. et al. Potential of tannin-rich plants for modulating ruminal microbes and ruminal fermentation in sheep. J. Anim. Sci. 93, 334–347. https://doi.org/10.2527/jas.2014-7961 (2015).
doi: 10.2527/jas.2014-7961 pubmed: 25568379
Min, B. R. & Solaiman, S. Comparative aspects of plant tannins on digestive physiology, nutrition and microbial community changes in sheep and goats: A review. J. Anim. Physiol. Anim. Nutr. 102, 1181–1193. https://doi.org/10.1111/jpn.12938 (2018).
doi: 10.1111/jpn.12938
Stewart, E. K. et al. Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle1. J. Anim. Sci. 97, 3286–3299. https://doi.org/10.1093/jas/skz206 (2019).
doi: 10.1093/jas/skz206 pubmed: 31242504 pmcid: 6667269
Battelli, M. et al. Condensed tannins fed to dairy goats: effects on digestibility, milk production, blood parameters, methane emission, and energy and nitrogen balances. J. Dairy Sci. https://doi.org/10.3168/jds.2023-24076 (2024).
doi: 10.3168/jds.2023-24076 pubmed: 38246549
Zeller, W. E. Activity, purification, and analysis of condensed tannins: Current state of affairs and future endeavors. Crop Sci. 59, 886–904. https://doi.org/10.2135/cropsci2018.05.0323 (2019).
doi: 10.2135/cropsci2018.05.0323
Naumann, H. et al. Relationships between structures of condensed tannins from texas legumes and methane production during in vitro rumen digestion. Molecules 23, 2123. https://doi.org/10.3390/molecules23092123 (2018).
doi: 10.3390/molecules23092123 pubmed: 30142930 pmcid: 6225215
Flachowsky, G. & Lebzien, P. Effects of phytogenic substances on rumen fermentation and methane emissions: A proposal for a research process. Feed Sci. Technol. 176, 70–77. https://doi.org/10.1016/j.anifeedsci.2012.07.009 (2012).
doi: 10.1016/j.anifeedsci.2012.07.009
Verma, S., Taube, F. & Malisch, C. S. Examining the variables leading to apparent incongruity between antimethanogenic potential of tannins and their observed effects in ruminants—a review. Sustainability 13, 2743. https://doi.org/10.3390/su13052743 (2021).
doi: 10.3390/su13052743
Ropiak, H. M. et al. Structure–activity relationship of condensed tannins and synergism with trans-cinnamaldehyde against Caenorhabditis elegans. J. Agric. Food Chem. 64, 8795–8805. https://doi.org/10.1021/acs.jafc.6b03842 (2016).
doi: 10.1021/acs.jafc.6b03842 pubmed: 27796095
Jonker, A. & Yu, P. The occurrence, biosynthesis, and molecular structure of proanthocyanidins and their effects on legume forage protein precipitation, digestion and absorption in the ruminant digestive tract. Int J Mol Sci 18, 1105. https://doi.org/10.3390/ijms18051105 (2017).
doi: 10.3390/ijms18051105 pubmed: 28531145 pmcid: 5455013
Salminen, J.-P. & Karonen, M. Chemical ecology of tannins and other phenolics: We need a change in approach. Funct. Ecol. 25, 325–338. https://doi.org/10.1111/j.1365-2435.2010.01826.x (2011).
doi: 10.1111/j.1365-2435.2010.01826.x
Baert, N., Pellikaan, W. F., Karonen, M. & Salminen, J.-P. A study of the structure-activity relationship of oligomeric ellagitannins on ruminal fermentation in vitro. J. Dairy Sci. 99, 8041–8052. https://doi.org/10.3168/jds.2016-11069 (2016).
doi: 10.3168/jds.2016-11069 pubmed: 27522412
Olagaray, K. & Bradford, B. Plant flavonoids to improve productivity of ruminants—a review. Anim. Feed Sci. Technol. 251, 21–36. https://doi.org/10.1016/j.anifeedsci.2019.02.004 (2019).
doi: 10.1016/j.anifeedsci.2019.02.004
Kim, E. T. et al. Effects of flavonoid-rich plant extracts on in vitro ruminal methanogenesis, microbial populations and fermentation characteristics. Asian Australas. J. Anim. Sci. 28, 530–537. https://doi.org/10.5713/ajas.14.0692 (2015).
doi: 10.5713/ajas.14.0692 pubmed: 25656200 pmcid: 4341102
Brown, R. H. et al. Facile purification of milligram to gram quantities of condensed tannins according to mean degree of polymerization and flavan-3-ol subunit composition. J. Agric. Food Chem. 65, 8072–8082. https://doi.org/10.1021/acs.jafc.7b03489 (2017).
doi: 10.1021/acs.jafc.7b03489 pubmed: 28813594
Leppä, M. M., Karonen, M., Tähtinen, P., Engström, M. T. & Salminen, J.-P. Isolation of chemically well-defined semipreparative liquid chromatography fractions from complex mixtures of proanthocyanidin oligomers and polymers. J. Chromatogr. A 1576, 67–79. https://doi.org/10.1016/j.chroma.2018.09.034 (2018).
doi: 10.1016/j.chroma.2018.09.034 pubmed: 30314685
Menke, H. H. & Steingass, H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 28, 7–55 (1988).
Verma, S., Salminen, J.-P., Taube, F. & Malisch, C. S. Large Inter- and intraspecies variability of polyphenols and proanthocyanidins in eight temperate forage species indicates potential for their exploitation as nutraceuticals. J. Agric. Food Chem. https://doi.org/10.1021/acs.jafc.1c03898 (2021).
doi: 10.1021/acs.jafc.1c03898 pubmed: 34662108
Verma, S. et al. Linking metabolites in eight bioactive forage species to their in vitro methane reduction potential across several cultivars and harvests. 12, 10454. https://doi.org/10.1038/s41598-022-14424-2 (2022).
Loza, C. et al. Methane emission and milk production from jersey cows grazing perennial ryegrass-white clover and multispecies forage mixtures. Agriculture 11, 175. https://doi.org/10.3390/agriculture11020175 (2021).
doi: 10.3390/agriculture11020175
Min, B.-R., Lee, S., Jung, H., Miller, D. N. & Chen, R. Enteric methane emissions and animal performance in dairy and beef cattle production: strategies, opportunities, and impact of reducing emissions. Animals 12, 948 (2022).
doi: 10.3390/ani12080948 pubmed: 35454195 pmcid: 9030782
Battelli, M., Nielsen, M. O. & Nørskov, N. P. Dose- and substrate-dependent reduction of enteric methane and ammonia by natural additives in vitro. Front. Vet. Sci. https://doi.org/10.3389/fvets.2023.1302346 (2023).
doi: 10.3389/fvets.2023.1302346 pubmed: 38026671 pmcid: 10657808
Berça, A. S., Tedeschi, L. O., da Silva Cardoso, A. & Reis, R. A. Meta-analysis of the relationship between dietary condensed tannins and methane emissions by cattle. Anim. Feed Sci. Technol. 298, 115564. https://doi.org/10.1016/j.anifeedsci.2022.115564 (2023).
doi: 10.1016/j.anifeedsci.2022.115564
Saminathan, M., Sieo, C. C., Abdullah, N., Wong, C. M. V. L. & Ho, Y. W. Effects of condensed tannin fractions of different molecular weights from a Leucaena leucocephala hybrid on in vitro methane production and rumen fermentation. J. Food Agric. 95, 2742–2749. https://doi.org/10.1002/jsfa.7016 (2015).
doi: 10.1002/jsfa.7016
Hatew, B. et al. Impact of variation in structure of condensed tannins from sainfoin (Onobrychis viciifolia) on in vitro ruminal methane production and fermentation characteristics. J. Anim. (Berl) 100, 348–360. https://doi.org/10.1111/jpn.12336 (2016).
doi: 10.1111/jpn.12336
Huyen, N. T. et al. Structural features of condensed tannins affect in vitro ruminal methane production and fermentation characteristics. J. Agric. Sci. 154, 1474–1487. https://doi.org/10.1017/S0021859616000393 (2016).
doi: 10.1017/S0021859616000393
Lüscher, A., Mueller-Harvey, I., Soussana, J. F., Rees, R. M. & Peyraud, J. L. Potential of legume-based grassland–livestock systems in Europe: a review. Grass Forage Sci. 69, 206–228. https://doi.org/10.1111/gfs.12124 (2014).
doi: 10.1111/gfs.12124 pubmed: 26300574 pmcid: 4540161
Kölliker, R., Kempf, K., Malisch, C. S. & Lüscher, A. Promising options for improving performance and proanthocyanidins of the forage legume sainfoin (Onobrychis viciifolia Scop). Euphytica 213, 179. https://doi.org/10.1007/s10681-017-1965-6 (2017).
doi: 10.1007/s10681-017-1965-6
Lagrange, S., Beauchemin, K. A., MacAdam, J. & Villalba, J. J. Grazing diverse combinations of tanniferous and non-tanniferous legumes: Implications for beef cattle performance and environmental impact. Sci. Total Environ. 746, 140788. https://doi.org/10.1016/j.scitotenv.2020.140788 (2020).
doi: 10.1016/j.scitotenv.2020.140788 pubmed: 32758982
Orlandi, T., Kozloski, G. V., Alves, T. P., Mesquita, F. R. & Ávila, S. C. Digestibility, ruminal fermentation and duodenal flux of amino acids in steers fed grass forage plus concentrate containing increasing levels of Acacia mearnsii tannin extract. Anim. Feed Sci. Technol. 210, 37–45. https://doi.org/10.1016/j.anifeedsci.2015.09.012 (2015).
doi: 10.1016/j.anifeedsci.2015.09.012
Hassanat, F. & Benchaar, C. Assessment of the effect of condensed (acacia and quebracho) and hydrolysable (chestnut and valonea) tannins on rumen fermentation and methane production in vitro. J. Sci. Food Agric. 93, 332–339. https://doi.org/10.1002/jsfa.5763 (2013).
doi: 10.1002/jsfa.5763 pubmed: 22740383
Jayanegara, A., Goel, G., Makkar, H. P. S. & Becker, K. Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Anim. Feed Sci. Technol. 209, 60–68. https://doi.org/10.1016/j.anifeedsci.2015.08.002 (2015).
doi: 10.1016/j.anifeedsci.2015.08.002
Salami, S. A. et al. 2018 Characterisation of the ruminal fermentation and microbiome in lambs supplemented with hydrolysable and condensed tannins. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiy061
Lotfi, R. A commentary on methodological aspects of hydrolysable tannins metabolism in ruminant: a perspective view. Lett. Appl. Microbiol. 71, 466–478. https://doi.org/10.1111/lam.13346 (2020).
doi: 10.1111/lam.13346 pubmed: 32654165
Liu, H., Vaddella, V. & Zhou, D. Effects of chestnut tannins and coconut oil on growth performance, methane emission, ruminal fermentation, and microbial populations in sheep. J. Dairy Sci. 94, 6069–6077. https://doi.org/10.3168/jds.2011-4508 (2011).
doi: 10.3168/jds.2011-4508 pubmed: 22118094
González-Barrio, R. et al. Metabolism of oak leaf ellagitannins and urolithin production in beef cattle. J. Agric. Food Chem. 60, 3068–3077. https://doi.org/10.1021/jf300718k (2012).
doi: 10.1021/jf300718k pubmed: 22375726
Aboagye, I. A. et al. Effects of hydrolyzable tannin with or without condensed tannin on methane emissions, nitrogen use, and performance of beef cattle fed a high-forage diet1,2. J. Ani. Sci. 96, 5276–5286. https://doi.org/10.1093/jas/sky352 (2018).
doi: 10.1093/jas/sky352
Wischer, G. et al. Effects of long-term supplementation of chestnut and valonea extracts on methane release, digestibility and nitrogen excretion in sheep. Animal 8, 938–948. https://doi.org/10.1017/S1751731114000639 (2014).
doi: 10.1017/S1751731114000639 pubmed: 24679509
Berger, L. M. et al. Ruminal degradation of quercetin and its influence on fermentation in ruminants. J. Dairy Sci. 98, 5688–5698. https://doi.org/10.3168/jds.2015-9633 (2015).
doi: 10.3168/jds.2015-9633 pubmed: 26094220
Cui, K. et al. Effect of dietary supplementation of rutin on lactation performance, ruminal fermentation and metabolism in dairy cows. J. Anim. Physiol. Anim. Nutr. 99, 1065–1073. https://doi.org/10.1111/jpn.12334 (2015).
doi: 10.1111/jpn.12334
Seradj, A. R. et al. The effect of Bioflavex® and its pure flavonoid components on in vitro fermentation parameters and methane production in rumen fluid from steers given high concentrate diets. Anim. Feed Sci. Technol. 197, 85–91. https://doi.org/10.1016/j.anifeedsci.2014.08.013 (2014).
doi: 10.1016/j.anifeedsci.2014.08.013
Oskoueian, E., Abdullah, N. & Oskoueian, A. Effects of flavonoids on rumen fermentation activity, methane production, and microbial population. BioMed Res. Int. 2013, 349129. https://doi.org/10.1155/2013/349129 (2013).
doi: 10.1155/2013/349129 pubmed: 24175289 pmcid: 3794516
Nørskov, N. P. et al. Methane reduction by quercetin, tannic and salicylic acids: influence of molecular structures on methane formation and fermentation in vitro. Sci. Rep. 13, 16023. https://doi.org/10.1038/s41598-023-43041-w (2023).
doi: 10.1038/s41598-023-43041-w pubmed: 37749362 pmcid: 10519955
Ku-Vera, J. C. et al. Role of secondary plant metabolites on enteric methane mitigation in ruminants. Front. Vet. Sci. 7, 584. https://doi.org/10.3389/fvets.2020.00584 (2020).
doi: 10.3389/fvets.2020.00584 pubmed: 33195495 pmcid: 7481446
Engström, M. T. et al. Rapid qualitative and quantitative analyses of proanthocyanidin oligomers and polymers by UPLC–MS/MS. J. Agric. Food Chem. 62, 3390–3399. https://doi.org/10.1021/jf500745y (2014).
doi: 10.1021/jf500745y pubmed: 24665824
Engström, M. T., Pälijärvi, M. & Salminen, J.-P. Rapid fingerprint analysis of plant extracts for ellagitannins, gallic acid, and quinic acid derivatives and quercetin-, kaempferol- and myricetin-based flavonol glycosides by UPLC–QqQ-MS/MS. J. Agric. Food Chem. 63, 4068–4079. https://doi.org/10.1021/acs.jafc.5b00595 (2015).
doi: 10.1021/acs.jafc.5b00595 pubmed: 25853372
Salminen, J.-P. Two-dimensional tannin fingerprints by liquid chromatography tandem mass spectrometry offer a new dimension to plant tannin analyses and help to visualize the Tannin Diversity in Plants. J. Agric. Food Chem. 66, 9162–9171. https://doi.org/10.1021/acs.jafc.8b02115 (2018).
doi: 10.1021/acs.jafc.8b02115 pubmed: 30136834 pmcid: 6203188
Naumann, C., Bassler, R., Seibold, R. d. & Barth, C. Methodenbuch. Band III, Die chemische Untersuchung von Futtermitteln. 3. Aufl., 4. Ergänzungslieferung edn, Bd. 3 (loč. pag.): tabele ; 21 cm. (VDLUFA - Verlag Darmstadt, 1997).
GfE. In Proceedings of the Society of Nutrition Physiology. 143–146.
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org  (2021).

Auteurs

S Verma (S)

Grass and Forage Science / Organic Agriculture, Christian-Albrechts-University of Kiel, E24118, Kiel, Germany. sverma@gfo.uni-kiel.de.
Department of Agroecology, Aarhus University, 8830, Tjele, Denmark. sverma@gfo.uni-kiel.de.

T T Akpensuen (TT)

Net Zero and Resilient Farming, Rothamsted Research, Okehampton, EX20 2SD, UK.
Faculty of Agriculture, University of Jos, P.M.B 2084, Jos, Nigeria.

S Wolffram (S)

Animal Nutrition and Physiology, Christian-Albrechts-University of Kiel, E24118, Kiel, Germany.

J-P Salminen (JP)

Natural Chemistry Research Group, University of Turku, 20500, Turku, Finland.

F Taube (F)

Grass and Forage Science / Organic Agriculture, Christian-Albrechts-University of Kiel, E24118, Kiel, Germany.

R Blank (R)

Animal Nutrition and Physiology, Christian-Albrechts-University of Kiel, E24118, Kiel, Germany.

C Kluß (C)

Grass and Forage Science / Organic Agriculture, Christian-Albrechts-University of Kiel, E24118, Kiel, Germany.

C S Malisch (CS)

Department of Agroecology, Aarhus University, 8830, Tjele, Denmark.

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