Exploration of Methane Mitigation Efficacy Using Asparagopsis-Derived Bioactives Stabilized in Edible Oil Compared to Freeze-Dried Asparagopsis in Vitro
Asparagopsis oil
products are of interest due to the stabilizing effects of the Asparagopsis-derived antimethanogenic bioactive compound bromoform
(CHBr3). The objective of this in vitro series is to
characterize antimethanogenic efficacy of
freeze-dried Asparagopsis (FD-Asp) and Asparagopsis oil
(Asp-Oil) and compare relative antimethanogenic response over time at multiple
levels of CHBr3 delivery. Relative methane (CH4)
emissions (mL/g) are based on in vitro apparent feed digested dry matter
(IVDDM) after 24, 48, and 72 h of fermentation. CHBr3 contained in
FD-Asp was included at 95, 191, and 286 mg/kg, and CHBr3 contained
in Asp-Oil was included at 78, 117, and 175
mg/kg, to produce the Low, Mid, and High inclusions, respectively. Low FD-Asp
had no significant impact on CH4 emissions, Mid FD-Asp demonstrated
91%, 44%, and 37% reductions, and the High FD-Asp demonstrated complete
inhibition of CH4, after 24, 48, and 72 h of fermentation,
respectively. Comparatively, Low Asp-Oil demonstrated a 46%, 28%, and 18% CH4 reduction, Mid Asp-Oil resulted in 99%, 92%, and 73% reductions, and the High
Asp-Oil demonstrated complete inhibition of CH4 after 24, 48, and 72 h of fermentation, respectively. IVDDM and total
volatile fatty acid (tVFA) production were not changed by the inclusion of FD-Asp and Asp-Oil. The
results from this study show that Asparagopsis is not only a compelling
CH4 mitigating feed supplement
but is also able to be delivered in edible oil forms which will strengthen its
applicability to on-farm use. This study is promising for the utility of
Asp-Oil, and in vivo trials are essential to demonstrate the extent of
efficacy of Asp-Oil in ruminant animals because FD-Asp has consistently
demonstrated greater antimethanogenic efficacy in vivo compared to in
vitro.
References
[1]
Herrero, M., Henderson, B., Havlík, P., Thornton, P.K., Conant, R.T., Smith, P., Wirsenius, S., Hristov, A.N., Gerber, P., Gill, M., Butterbach-Bahl, K., Valin, H., Garnett, T. and Stehfest, E. (2016) Greenhouse Gas Mitigation Potentials in the Livestock Sector. Nature Climate Change, 6, 452-461.
https://doi.org/10.1038/nclimate2925
[2]
Mayberry, D., Bartlett, H., Moss, J., Davison, T. and Herrero, M. (2019) Pathways to Carbon-Neutrality for the Australian Red Meat Sector. Agricultural Systems, 175, 13-21. https://doi.org/10.1016/j.agsy.2019.05.009
[3]
Kinley, R.D., Martinez-Fernandez, G., Matthews, M.K., de Nys, R., Magnusson, M. and Tomkins, N.W. (2020) Mitigating the Carbon Footprint and Improving Productivity of Ruminant Livestock Agriculture Using a Red Seaweed. Journal of Cleaner Production, 259, Article ID: 120836.
https://doi.org/10.1016/j.jclepro.2020.120836
[4]
Roque, B.M., Venegas, M., Kinley, R.D., de Nys, R., Duarte, T.L., Yang, X. and Kebreab, E. (2021) Red Seaweed (Asparagopsis taxiformis) Supplementation Reduces Enteric Methane by over 80 Percent in Beef Steers. PLOS ONE, 16, e0247820.
https://doi.org/10.1371/journal.pone.0247820
[5]
Machado, L., Magnusson, M., Paul, N.A., Kinley, R., De Nys, R. and Tomkins, N. (2016) Identification of Bioactives from the Red Seaweed Asparagopsis taxiformis That Promote Antimethanogenic Activity in Vitro. Journal of Applied Phycology, 28, 3117-3126. https://doi.org/10.1007/s10811-016-0830-7
[6]
Vucko, M.J., Magnusson, M., Kinley, R.D., Villart, C. and de Nys, R. (2016) The Effects of Processing on the in Vitro Antimethanogenic Capacity and Concentration of Secondary Metabolites of Asparagopsis taxiformis. Journal of Applied Phycology, 29, 1577-1586. https://doi.org/10.1007/s10811-016-1004-3
[7]
Magnusson, M., Vucko, M.J., Neoh, T.L. and de Nys, R. (2020) Using Oil Immersion to Deliver a Naturally-Derived, Stable Bromoform Product from the Red Seaweed Asparagopsis taxiformis. Algal Research, 51, Article ID: 102065.
https://doi.org/10.1016/j.algal.2020.102065
[8]
Kinley, R.D., Vucko, M.J., Machado, L. and Tomkins, N.W. (2016) In Vitro Evaluation of the Antimethanogenic Potency and Effects on Fermentation of Individual and Combinations of Marine Macroalgae. American Journal of Plant Science, 7, 2038-2054.
https://doi.org/10.4236/ajps.2016.714184
[9]
Kinley, R.D., de Nys, R., Vucko, M.J., Machado, L. and Tomkins, N.W. (2016) The Red Macroalgae Asparagopsis taxiformis Is a Potent Natural Antimethanogenic That Reduces Methane Production during in Vitro Fermentation with Rumen Fluid. Animal Production Science, 56, 282-289. https://doi.org/10.1071/AN15576
[10]
Meat and Livestock Australia (MLA) (2020) The Australian Red Meat Industry’s Carbon Neutral by 2030 Roadmap. Meat and Livestock Australia, North Sydney.
https://www.mla.com.au/globalassets/mla-corporate/research-and- development/program-areas/livestock-production/mla-cn30-roadmap_031221.pdf
[11]
Ridoutt, B., Lehnert, S.A., Denman, S., Charmley, E., Kinley, R. and Dominik, S. (2022) Potential GHG Emission Benefits of Asparagopsis taxiformis Feed Supplement in Australian Beef Cattle Feedlots. Journal of Cleaner Production, 337, Article ID: 130499. https://doi.org/10.1016/j.jclepro.2022.130499
[12]
Australian Government Department of Industry, Science, Energy and Resources (2021) Australia’s Data for Land Use, Land Use Change and Forestry (LULUCF) and Waste, Recalculations and Improvements. In: Commonwealth of Australia, Ed., 2019 National Inventory Report, Commonwealth of Australia, Canberra, 37-42.
https://www.industry.gov.au/sites/default/files/April%202021/document/national- inventory-report-2019-volume-2.pdf
[13]
Jia, Y., Quack, B., Kinley, R.D., Pisso, I. and Tegtmeier, S. (2022) Potential Environmental Impact of Bromoform from Asparagopsis Farming in Australia. Atmospheric Chemistry and Physics, 22, 7631-7646.
https://doi.org/10.5194/acp-22-7631-2022
[14]
Paul, N.A., de Nys, R. and Steinberg, P.D. (2006) Chemical Defence against Bacteria in the Red Alga Asparagopsis armata: Linking Structure with Function. Marine Ecology Progress Series, 306, 87-101. https://doi.org/10.3354/meps306087
[15]
Horowitz, W. (2000) Agricultural Chemicals, Contaminants, Drugs, Vol. 1, 17th edition, Official Methods of Analysis of AOAC International, AOAC International, Rockville.
[16]
National Health and Medical Research Council (2013) Australian Code for the Care and Use of Animals for Scientific Purposes. 8th Edition, National Health and Medical Research Council, Canberra.
[17]
Goering, H.K. and Van Soest, P.J. (1970) Forage Fiber Analysis (Apparatus Reagents, Procedures and Some Applications). United States Department of Agriculture, Washington DC.
[18]
Kinley, R.D., Tan, S., Turnbull, J., Askew, S. and Roque, B.M. (2021) Changing the Proportions of Grass and Grain in Feed Substrate Impacts the Efficacy of Asparagopsis taxiformis to Inhibit Methane Production in Vitro. American Journal of Plant Sciences, 12, 1835-1858. https://doi.org/10.4236/ajps.2021.1212128
[19]
Machado, L., Magnusson, M., Paul, N.A., Kinley, R., de Nys, R. and Tomkins, N. (2016) Dose-Response Effects of Asparagopsis taxiformis and Oedogonium sp. on in Vitro Fermentation and Methane Production. Journal of Applied Phycology, 28, 1443-1452. https://doi.org/10.1007/s10811-015-0639-9
[20]
Roque, B.M., Brooke, C.G., Ladau, J., Polley, T., Marsh, L.J., Najafi, N., Pandey, P., Singh, L., Kinley, R., Salwen, J.K., Eloe-Fadrosh, E., Kebreab, E. and Hess, M. (2019) Effect of the Macroalgae Asparagopsis taxiformis on Methane Production and Rumen Microbiome Assemblage. Animal Microbiome, 1, Article No. 3.
https://doi.org/10.1186/s42523-019-0004-4
[21]
Brooke, C.G., Roque, B.M., Shaw, C., Najafi, N., Gonzalez, M., Pfefferlen, A., De Anda, V., Ginsburg, D.W., Harden, M.C., Nuzhdin, S.V., Salwen, J.K., Kebreab, E. and Hess, M. (2020) Methane Reduction Potential of Two Pacific Coast Macroalgae during in Vitro Ruminant Fermentation. Frontiers in Marine Science, 7, Article No. 561. https://doi.org/10.3389/fmars.2020.00561
[22]
Belanche, A., de la Fuente, G. and Newbold, C.J. (2014) Study of Methanogen Communities Associated with Different Rumen Protozoal Populations. FEMS Microbiology Ecology, 90, 663-677. https://doi.org/10.1111/1574-6941.12423
[23]
Roque, B.M., Salwen, J.K., Kinley, R. and Kebreab, E. (2019) Inclusion of Asparagopsis armata in Lactating Dairy Cows’ Diet Reduces Enteric Methane Emission by over 50 Percent. Journal of Cleaner Production, 234, 132-138.
https://doi.org/10.1016/j.jclepro.2019.06.193
[24]
Mayberry, D. (2019) Raising the Steaks: Reducing GHG Emissions from Red Meat. 2019 Weathering the ‘Perfect Storm’: Addressing the Agriculture, Energy, Water, Climate Change Nexus, 12-13 August 2019, 47-50.
[25]
Stefenoni, H.A., Räisänen, S.E., Cueva, S.F., Wasson, D.E., Lage, C.F.A., Melgar, A., Fetter, M.E., Smith, P., Hennessy, M., Vecchiarelli, B., Bender, J., Pitta, D., Cantrell, C.L., Yarish, C. and Hristov, A.N. (2021) Effects of the Macroalga Asparagopsis taxiformis and Oregano Leaves on Methane Emission, Rumen Fermentation, and Lactational Performance of Dairy Cows. Journal of Dairy Science, 104, 4157-4173.
https://doi.org/10.3168/jds.2020-19686
[26]
Li, X., Norman, H.C., Kinley, R.D., Laurence, M., Wilmot, M., Bender, H., de Nys, R. and Tomkins, N. (2018) Asparagopsis taxiformis Decreases Enteric Methane Production from Sheep. Animal Production Science, 58, 681-688.
https://doi.org/10.1071/AN15883
[27]
Beauchemin, K.A., Kreuzer, M., O’Mara, F. and McAllister, T.A. (2008) Nutritional Management for Enteric Methane Abatement: A Review. Australian Journal of Experimental Agriculture, 48, 21-27. https://doi.org/10.1071/EA07199
[28]
Patra, A.K. (2013) The Effect of Dietary Fats on Methane Emissions, and Its Other Effects on Digestibility, Rumen Fermentation and Lactation Performance in Cattle: A Meta-Analysis. Livestock Science, 155, 244-254.
https://doi.org/10.1016/j.livsci.2013.05.023
[29]
Dohme, F., Machmuller, A., Estermann, B.L., Pfister, P., Wasserfallen, A. and Kreuzer, M. (1999) The Role of the Rumen Ciliate Protozoa for Methane Suppression Caused by Coconut Oil. Letters in Applied Microbiology, 29, 187-192.
https://doi.org/10.1046/j.1365-2672.1999.00614.x
[30]
Yanza, Y.R., Szumacher-Strabel, M., Jayanegara, A., Kasenta, A.M., Gao, M., Huang, H., Patra, A.K., Warzych, E. and Cieślak, A. (2021) The Effects of Dietary Medium-Chain Fatty Acids on Ruminal Methanogenesis and Fermentation in vitro and in Vivo: A Meta-Analysis. Journal of Animal Physiology and Animal Nutrition, 105, 874-889. https://doi.org/10.1111/jpn.13367
[31]
Machmüller, A. (2006) Medium-Chain Fatty Acids and Their Potential to Reduce Methanogenesis in Domestic Ruminants. Agriculture, Ecosystems & Environment, 112, 107-114. https://doi.org/10.1016/j.agee.2005.08.010
[32]
Czerkawski, J.W., Blaxter, K.L. and Wainman, F.W. (1966) The Metabolism of Oleic, Linoleic and Linolenic Acids by Sheep with Reference to Their Effects on Methane Production. The British Journal of Nutrition, 20, 349-362.
https://doi.org/10.1079/BJN19660035
[33]
Johnson, K.A. and Johnson, D.E. (1995) Methane Emissions from Cattle. Journal of Animal Science, 73, 2483-2492. https://doi.org/10.2527/1995.7382483x
[34]
Van Nevel, C.J. and Demeyer, D.I. (1996) Control of Rumen Methanogenesis. Environmental Monitoring and Assessment, 42, 73-97.
https://doi.org/10.1007/BF00394043
[35]
Lunsin, R., Wanapat, M. and Rowlinson, P. (2012) Effect of Cassava Hay and Rice Bran Oil Supplementation on Rumen Fermentation, Milk Yield and Milk Composition in Lactating Dairy Cows. Asian-Australasian Journal of Animal Sciences, 25, 1364-1373. https://doi.org/10.5713/ajas.2012.12051
[36]
Wang, M., Wang, R., Zhang, X., Ungerfeld, E.M., Long, D., Mao, H., Jiao, J., Beauchemin, K.A. and Tan, Z. (2017) Molecular Hydrogen Generated by Elemental Magnesium Supplementation Alters Rumen Fermentation and Microbiota in Goats. The British Journal of Nutrition, 118, 401-410.
https://doi.org/10.1017/S0007114517002161
[37]
Ungerfeld, E.M. (2020) Metabolic Hydrogen Flows in Rumen Fermentation: Principles and Possibilities of Interventions. Frontiers in Microbiology, 11, Article No. 589.
https://doi.org/10.3389/fmicb.2020.00589
[38]
Miller, T.L. and Jenesel, S.E. (1979) Enzymology of Butyrate Formation by Butyrivibrio fibrisolvens. Journal of Bacteriology, 138, 99-104.
https://doi.org/10.1128/jb.138.1.99-104.1979
[39]
Machado, L., Tomkins, N., Magnusson, M., Midgley, D.J., de Nys, R. and Rosewarne, C.P. (2018) In Vitro Response of Rumen Microbiota to the Antimethanogenic Red Macroalga Asparagopsis taxiformis. Microbial Ecology, 75, 811-818.
https://doi.org/10.1007/s00248-017-1086-8