Fermentation parameters in the rumen of goats supplemented with polyphenol oxidase derived from Gliricidia sepium leaves under in vitro conditions

##plugins.themes.bootstrap3.article.main##

ASRI NURUL HUDA
AKHMAD SABARUDIN
ANURAGA JAYANEGARA
HENDRAWAN SOETANTO

Abstract

Abstract. Huda AN, Sabarudin A, Jayanegara A, Soetanto H. 2023. Fermentation parameters in the rumen of goats supplemented with polyphenol oxidase derived from Gliricidia sepium leaves under in vitro conditions. Biodiversitas 24: 3282-3290. The growing demand for healthy foods derived from ruminant products is restricted by the high content of saturated fatty acids in meat or milk due to the process of rumen biohydrogenation. Recent reports from intensive studies using polyphenol oxidase (PPO), an enzyme in plants’ secondary metabolism, as the inhibitor of rumen biohydrogenation cost doubt of ruminant products. PPO is assumed to increase the supply of UFA by reducing the rate of biohydrogenation due to rumen microbes’ activity. Microbes of the rumen, including species of bacteria and protozoa are responsible for rumen biohydrogenation. The present study investigated the effect of adding PPO derived from Gliricidia sepium leaves on fermentation parameters in the rumen, including protozoa density and diversity, fatty acid profile, volatile fatty acid profile, and the efficiency of microbial protein synthesis under in vitro conditions. The experiment was carried out through an in vitro rumen fermentation method, consisting of five treatments, i.e., negative control, positive control, the addition of 0.1 ml, 0.3 ml, and 0.5 ml PPO emulsion. The most dominant type of protozoa among all treatments was Entodinium spp. PPO emulsion increases the efficiency of microbial protein synthesis and volatile fatty acid concentration. 0.5 ml PPO emulsion increases linoleic acid. In conclusion, this finding poses a question on the role of rumen protozoa in lipid biohydrogenation in the rumen. A further experiment on the benefits of adding PPO regarding rumen biohydrogenation under in vivo conditions is warranted.

##plugins.themes.bootstrap3.article.details##

References
Alende M, Lascano GJ, Jenkins TC, Koch LE, Volpi-Lagreca G, Andrae JG. 2018. Technical Note: Comparison of 4 methods for determining in vitro ruminal digestibility of annual ryegrass. The Professional Animal Scientist 34 (3): 306-309. DOI: https://doi.org/10.15232/pas.2017-01688.
Anggraeny, YN, Soetanto H, Kusmartono, Hartutik. 2015. Sinkronisasi suplai protein dan energi dalam rumen untuk meningkatkan efisiensi pakan berkualitas rendah. Wartozoa 25(3): 107-116. DOI: http://doi.org/10.14334/wartazoa.v25i3.1155.
Aprilia RM, Huda AN, Sumitro AM, Kusmartono S, H. 2021. Rumen protozoa diversity of Indonesian indigenous cattle. Jurnal Ilmu-Ilmu Peternakan 31(3): 267-273. DOI: https://doi.org/10.21776/ub.jiip.2021.031.03.10.
Baldin M, Garcia D, Zanton GI, Hao F, Patterson AD, Harvatine KJ. 2022. Effect of 2-hydroxy-4-(methylthio)butanoate (HMTBa) on milk fat, rumen environment and biohydrogenation, and rumen protozoa in lactating cows fed diets with increased risk for milk fat depression. Journal of Dairy Science 105(9): 7446-7461. DOI: https://doi.org/10.3168/jds.2022-21910.
Blümmel MH, Steingass H, Becker K. 1997. ‘The relationship between in vitro gas production, in vitro microbial biomass yield and 15N incorporation and its implications for the prediction of voluntary feed intake of roughages. British Journal of Nutrition 77(6): 911-921.
Boeckx T, Winters AL, Webb KJ, Kingston-Smith AH. 2015. Polyphenol oxidase in leaves: is there any significance to the chloroplastic localization? Journal of Experimental Botany 66(12): 3571-3579. DOI: https://doi.org/10.1093/jxb/erv141.
Castillo-González A, Burrola-Barraza M, Domínguez-Viveros J, Chávez-Martínez A. 2014. Rumen microorganisms and fermentation. Archivos de Medicina Veterinaria 46(3): 349-361. DOI: https://doi.org/10.4067/S0301-732X2014000300003.
Conte G, Serra A, Mele M. 2017. Dairy cow breeding and feeding on the milk fatty acid pattern. Nutrients in Dairy and Their Implications for Health and Disease. Elsevier Inc. 19–41. DOI: https://doi.org/10.1016/B978-0-12-809762-5.00002-4.
Daning DRA, Hanim C, Widyobroto BP, Yusiati LM. 2022a. Characteristics of ruminal fatty acids using in vitro culture system by addition of galangal (Alpinia galangal) essential oil. Advances in Biological Sciences Research. Proceedings of the 9th international seminar on tropical animal production (ISTAP 2021), 18 65-69. DOI: https://doi.org/10.2991/absr.k.220207.014.
Ratih Ayu Daning DRA, Yusiati LM, Hanim C, Widyobroto BP. 2021. Dietary supplementation of galangal (Alpinia galangal) essential oil affects rumen fermentation pattern. Advances in Animal and Veterinary Sciences 10(2): 323. DOI: http://doi.org/10.17582/journal.aavs/2022/10.2.323.334.
De Neve N, Vlaeminck B, Gadeyne F, Claeys E, Van der Meeren P, Fievez V. 2018. Promising perspectives for ruminal protection of polyunsaturated fatty acids through polyphenol-oxidase-mediated crosslinking of interfacial protein in emulsions. Animal 12(12): 2539-2550. DOI: https://doi.org/10.1017/S1751731118000423.
Dehority, BA. 2018. Laboratory manual for classification and morphology of rumen ciliate protozoa. In Laboratory manual for classification and morphology of rumen ciliate protozoa. CRC Press.
Dewanckele L, Vlaeminck B, Hernandez-Sanabria E, Ruiz-González A, deBruyne S, Jeyanathan J, Fievez V. 2018. Rumen biohydrogenation and microbial community changes upon early life supplementation of 22:6n-3 enriched microalgae to goats. Frontiers in Microbiology 9: 573. DOI: https://doi.org/10.3389/fmicb.2018.00573.
Dos Santos TAX, Fernandes LMG, Carvalho PPX, Júnior VSM, Fonseca SA, Chaves AS, Duarte ER. 2021. Performance and microbiota of the digestive tract of Nellore calves supplemented with fungi isolated from bovine rumen. Veterinary World 14(10): 2686-2693. DOI: https://doi.org/10.14202/vetworld.2021.2686-2693.
Duarte ER, Abrão FO, Oliveira Ribeiro IC, Vieira EA, Nigri AC, Silva KL, Virgínio Júnior GF, Prates Barreto SM, Geraseev LC. 2018. Rumen protozoa of different ages of beef cattle raised in tropical pastures during the dry season. Journal of Applied Animal Research 46(1): 1457-1461. DOI: https://doi.org/10.1080/09712119.2018.1530676.
Ebrahimi M, Rajion MA, Meng GY, Shokryzadan P, Sazili AQ, Jahromi MF. 2015. Feeding oil palm (Elaeis guineensis, Jacq.) fronds alters rumen protozoal population and ruminal fermentation pattern in goats. Italian Journal of Animal Science 14(3): 3877. DOI: https://doi.org/10.4081/ijas.2015.3877.
Enjalbert F, Combes S, Zened A, Meynadier A. 2017. Rumen microbiota and dietary fat: a mutual shaping. Journal of Applied Microbiology 123(4): 782-797. DOI: https://doi.org/10.1111/jam.13501.
Falguera V, Sánchez-Riaño AM, Quintero-Cerón JP, Rivera-Barrero CA, Méndez-Arteaga JJ, Ibarz A. 2012. Characterization of polyphenol oxidase activity in juices from 12 underutilized tropical fruits with high agroindustrial potential. Food and Bioprocess Technology 5(7): 2921-2927. DOI: https://doi.org/10.1007/s11947-011-0521-y.
Ferlay A, Bernard L, Meynadier A, Malpuech-Brugère C. 2017. Production of trans and conjugated fatty acids in dairy ruminants and their putative effects on human health: a review. Biochimie 141: 107-120. DOI: https://doi.org/10.1016/j.biochi.2017.08.006.
Firkins JL, Yu Z, Park T, Plank JE. 2020. Extending burk Dehority’s perspectives on the role of ciliate protozoa in the rumen. Frontiers in Microbiology 11: 123. DOI: https://doi.org/10.3389/fmicb.2020.00123.
Formato M, Cimmino G, Brahmi-Chendouh N, Piccolella S, Pacifico S. 2022. Polyphenols for livestock feed: sustainable perspectives for animal husbandry? Molecules 27(22): 7752. DOI: https://doi.org/10.3390/molecules27227752.
Francisco AE, Santos-Silva JM, Portugal APV, Alves SP, Bessa RJB. 2019. Relationship between rumen ciliate protozoa and biohydrogenation fatty acid profile in rumen and meat of lambs. PLOS ONE 14: 1-21. DOI: https://doi.org/10.1371/journal.pone.0221996.
Freitas JE, Takiya CS, Del Valle TA, Barletta RV, Venturelli BC, Vendramini THA, Mingoti RD, Calomeni GD, Gardinal R, Gandra JR, Bettero VP, Ferreira de Jesus EF, Oliveira MDS, Rennó FP. 2018. Ruminal biohydrogenation and abomasal flow of fatty acids in lactating cows fed diets supplemented with soybean oil, whole soybeans, or calcium salts of fatty acids. Journal of Dairy Science 101(9): 7881-7891. DOI: https://doi.org/10.3168/jds.2017-13666.
Gadeyne F, De Neve N, Vlaeminck B, Fievez V. 2017. State of the art in rumen lipid protection technologies and emerging interfacial protein cross-linking methods. European Journal of Lipid Science and Technology 119(5): 1-22. DOI: https://doi.org/10.1002/ejlt.201600345.
Gadeyne F, Van Ranst G, Vlaeminck B, Vossen E, Van Der Meeren P, Fievez V. 2015. Protection of polyunsaturated oils against ruminal biohydrogenation and oxidation during storage using a polyphenol oxidase containing extract from red clover. Food Chemistry 171: 241-250. DOI: https://doi.org/10.1016/j.foodchem.2014.08.109.
Gebreyowhans S, Lu J, Zhang S, Pang X, Lv J. 2019. Dietary enrichment of milk and dairy products with n-3 fatty acids: a review. International Dairy Journal 97: 158-166. DOI: https://doi.org/10.1016/j.idairyj.2019.05.011.
Hassan FU, Arshad MA, Ebeid HM, Rehman MS, Khan MS, Shahid S, Yang C. 2020. Phytogenic additives can modulate rumen microbiome to mediate fermentation kinetics and methanogenesis through exploiting diet–microbe interaction. Frontiers in Veterinary Science 7: 575801. DOI: https://doi.org/10.3389/fvets.2020.575801.
Henderson, G, Cox F, Ganesh S, Jonker A, Young W, Global Rumen Census Collaborators, 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: 14567. DOI: https://doi.org/10.1038/srep14567.
Hidayah N, Suharti S, Wiryawan KG. 2014. In vitro rumen fermentation of ration supplemented with protected vegetable oils. Media Peternakan 37(2): 129-135. DOI: https://doi.org/10.5398/medpet.2014.37.2.129.
Huda AN, Sumitro AM, Hanifah NA, Aprodita LRB, Lana RB, Dja’far SM, Aprilia RM, Sabarudin A, Soetanto H. 2022. Antiprotozoal properties of potato peels and linseed oil and their effect on in vitro gas production. IOP Conference Series: Earth and Environmental Science. IOP Publishing 977(1): 1-8. DOI: https://doi.org/10.1088/1755-1315/977/1/012128.
Ibrahim NA, Alimon AR, Yaakub H, Samsudin AA, Candyrine SCL, Mohamed WNW, Noh AM, Fuat MA, Mookiah S. 2021. Effects of vegetable oil supplementation on rumen fermentation and microbial population in ruminant: a review. Tropical Animal Health and Production 53: 1-11. DOI: https://doi.org/10.1007/s11250-021-02863-4.
Jafari S, Meng GY, Rajion MA, Jahromi MF, Ebrahimi M. 2016. Manipulation of rumen microbial fermentation by polyphenol rich solvent fractions from papaya leaf to reduce green-house gas methane and biohydrogenation of C18 PUFA. Journal of Agricultural and Food Chemistry 64(22): 4522-4530. DOI: https://doi.org/10.1021/acs.jafc.6b00846.
Jukanti A. 2017. Polyphenol oxidases (PPOs) in plants. Springer nature Singapore pte Ltd. 18: 1-131.
Kallas Z, Realini CE, Gil JM. 2014. Health information impact on the relative importance of beef attributes including its enrichment with polyunsaturated fatty acids (omega-3 and conjugated linoleic acid). Meat Science 97(4): 497-503. DOI: https://doi.org/10.1016/j.meatsci.2014.03.015.
Kholif AE, Olafadehan OA. 2022. Dietary strategies to enrich milk with healthy fatty acids – a review. Annals of Animal Science 22(2): 523-536. DOI: https://doi.org/10.2478/aoas-2021-0058.
Kliem KE, Reynolds CK, Humphries DJ, Kirkland RM, Barratt CES, Livingstone KM, Givens DI. 2013. Incremental effect of a calcium salt of cis-monounsaturated fatty acids supplement on milk fatty acid composition in cows fed maize silage-based diets. Journal of Dairy Science 96(5): 3211-3221. DOI: https://doi.org/10.3168/jds.2012-6211.
Lanier JS, Corl BA. 2015. Challenges in enriching milk fat with polyunsaturated fatty acids. Journal of Animal Science and Biotechnology.6:1–9. DOI: https://doi.org/10.1186/s40104-015-0025-0.
RA. 2014. Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation. Animal Production Science 54(5): 519-543. DOI: http://doi.org/10.1071/AN13381.
Lengowski MB, Zuber KHR, Witzig M, Möhring J, Boguhn J, Rodehutscord M. 2016. Changes in rumen microbial community composition during adaption to an in vitro system and the impact of different forages. PLOS ONE 11(2): e0150115. DOI: https://doi.org/10.1371/journal.pone.0150115.
Li Y, Gao J, Lv J, Lambo MT, Wang Y, Wang L, Zhang Y. 2023. Replacing soybean meal with high-oil pumpkin seed cake in the diet of lactating Holstein dairy cows modulated rumen bacteria and milk fatty acid profile. Journal of Dairy Science 106(3): 1803-1814. DOI: https://doi.org/10.3168/jds.2022-22503.
McSweeney PLH, Fox PF, O’Mahony JA. 2020. Advanced dairy chemistry. In Advanced Dairy Chemistry: Lipids, Fourth Edition (Vol. 2) Volume 2: Lipids. DOI: https://doi.org/10.1007/978-3-030-48686-0.
Morales R, Ungerfeld EM. 2015. Use of tannins to improve fatty acids profile of meat and milk quality in ruminants: a review. Chilean Journal of Agricultural Research 75(2): 239-248. DOI: https://doi.org/10.4067/S0718-58392015000200014.
A, Azizi G, Chekroun KB, Baghour M. 2016. The effects of livestock methane emission on the global warming: a review. International Journal of Global Warming 9(2): 229-253. DOI: http://doi.org/10.1504/IJGW.2016.074956.
Newbold CJ, de la Fuente G, Belanche A, Ramos-Morales E, McEwan NR. 2015. The role of ciliate protozoa in the rumen. Frontiers in Microbiology 6: 1313. DOI: https://doi.org/10.3389/fmicb.2015.01313.
Nguyen SH, Nguyen HDT, Hegarty RS. 2020. Defaunation and its impacts on ruminal fermentation, enteric methane production and animal productivity. Livestock Research for Rural Development 32(4).
Ostermann AI, Müller M, Willenberg I, Schebb NH. 2014. Determining the fatty acid composition in plasma and tissues as fatty acid methyl esters using gas chromatography – a comparison of different derivatization and extraction procedures. Prostaglandins, Leukotrienes, and Essential Fatty Acids 91(6): 235-241. DOI: https://doi.org/10.1016/j.plefa.2014.10.002.
Panadare D, Rathod VK. 2018. Extraction and purification of polyphenol oxidase: a review. Biocatalysis and Agricultural Biotechnology 14: 431-437. DOI: https://doi.org/10.1016/j.bcab.2018.03.010.
Patel S, Ambalam P. 2018. Role of rumen protozoa: metabolic and fibrolytic. Advances in Biotechnology and Microbiology 10(4): 79-84. DOI: http://doi.org/10.19080/AIBM.2018.10.555793.
Ribeiro WR, Vinolo MAR, Calixto LA, Ferreira CM. 2018. Use of gas chromatography to quantify short chain fatty acids in the serum, colonic luminal content and feces of mice. Bio-Protocol 8(22): e3089. DOI: https://doi.org/10.21769/BioProtoc.3089.
Soetanto H. 2019. Ilmu pengantar nutrisi Ternak Ruminansia. UB Press, Malang.
Sudarwati H, Nasir MH, Nurgiartiningsih VMA. 2019. Statistika dan Rancangan Percobaan Penerapan dalam Bidang Peternakan. UB Press, Malang.
Tilley JMA, Terry RA. 1963. A two-stage technique for the in vitro digestion of forage crops. Grass and Forage Science 18(2): 104-111. DOI: https://doi.org/10.1111/j.1365-2494.1963.tb00335.x.
Vargas JE, Andrés S, Snelling TJ, López-Ferreras L, Yáñez-Ruíz DR, García-Estrada C, López S. 2017. Effect of sunflower and marine oils on ruminal microbiota, in vitro fermentation and digesta fatty acid profile. Frontiers in Microbiology 8: 1124. DOI: https://doi.org/10.3389/fmicb.2017.01124.
Vasta V, Daghio M, Cappucci A, Buccioni A, Serra A, Viti C, Mele M. 2019 May. Invited review: plant polyphenols and rumen microbiota responsible for fatty acid biohydrogenation, fiber digestion, and methane emission: experimental evidence and methodological approaches. Journal of Dairy Science 102(5): 3781-3804. DOI: https://doi.org/10.3168/jds.2018-14985.
Wang L, Dong B, Yang T, Zhang A, Hu X, Wang Z, Chang G, Chen G. 2022. Dietary linseed oil affects the polyunsaturated fatty acid and transcriptome profiles in the livers and breast muscles of ducks. Frontiers in Nutrition 9(October): 1030712. DOI: https://doi.org/10.3389/fnut.2022.1030712.
Weatherly CA, Zhang Y, Smuts JP, Fan H, Xu C, Schug KA, Lang JC, Armstrong DW. 2016. Analysis of long-chain unsaturated fatty acids by ionic liquid gas chromatography. Journal of Agricultural and Food Chemistry 64(6): 1422-1432. DOI: https://doi.org/10.1021/acs.jafc.5b05988.
Williams CL, Thomas BJ, McEwan NR, Rees Stevens PR, Creevey CJ, Huws SA. 2020. Rumen protozoa play a significant role in fungal predation and plant carbohydrate breakdown. Frontiers in Microbiology 11: 720. DOI: https://doi.org/10.3389/fmicb.2020.00720.
Wu J, Gao J, Chen H, Liu X, Cheng W, Ma X, Tong P. 2013. Purification and characterization of polyphenol oxidase from agaricus bisporus. International Journal of Food Properties 16(7): 1483-1493. DOI: https://doi.org/10.1080/10942912.2011.595029.
Yuste S, Amanzougarene Z, de la Fuente G, de Vega A, Fondevila M. 2019. Rumen protozoal dynamics during the transition from milk/grass to high-concentrate based diet in beef calves as affected by the addition of tannins or medium-chain fatty acids. Animal Feed Science and Technology 257: 1-10. DOI: https://doi.org/10.1016/j.anifeedsci.2019.114273.
Zhao T, Ma Y, Qu Y, Luo H, Liu K, Zuo Z, Lu X. 2016. Effect of dietary oil sources on fatty acid composition of ruminal digesta and populations of specific bacteria involved in hydrogenation of 18-carbon unsaturated fatty acid in finishing lambs. Small Ruminant Research 144: 126-134. DOI: https://doi.org/10.1016/j.smallrumres.2016.06.012.
Zymon M, Strzetelski J, Skrzy?ski G. 2014. Aspects of appropriate feeding of cows for production of milk enriched in the fatty acids, EPA and DHA. A review. Journal of Animal and Feed Sciences 23(2): 109-116. DOI: https://doi.org/10.22358/jafs/65698/2014.

Most read articles by the same author(s)