综述 REVIEW

生物类黄酮调控瘤胃微生态系统的作用——聚焦甲烷减排

  • 赵玉超 ,
  • 余诗强 ,
  • 蒋林树
展开
  • 北京农学院动物科学技术学院, 奶牛营养学北京市重点实验室, 北京 102206
赵玉超(1994—),男,山西高平人,博士,主要从事奶牛营养与天然植物功能组分的开发应用研究。E-mail:zhaoyuchao2019@126.com

收稿日期: 2022-03-29

  网络出版日期: 2022-10-17

基金资助

北京市教委重点项目(KZ202010020029)

Roles of Bioflavonoids in Regulating Rumen Microecosystems: Focus on Methane Emission Reduction

  • ZHAO Yuchao ,
  • YU Shiqiang ,
  • JIANG Linshu
Expand
  • Beijing Key Laboratory of Dairy Nutrition, College of Animal Science and Technology, Beijing University of Agriculture, Beijing 102206, China

Received date: 2022-03-29

  Online published: 2022-10-17

摘要

瘤胃是反刍动物体内重要的微生物生态系统,微生物消化饲料的同时,也生成甲烷。反刍动物甲烷排放量约占到全球人为温室气体排放量的6%。因此,迫切需要采取营养策略调控瘤胃微生态系统,降低甲烷生成。类黄酮作为植物次级代谢产物中分布最广的化合物之一,具备抑菌、抗氧化等多种生物活性。类黄酮在瘤胃内代谢会影响瘤胃发酵模式,抑制原虫和古菌等与甲烷生成密切相关的菌群,进而降低甲烷排放,是潜在的甲烷抑制剂。鉴于此,本文对类黄酮在瘤胃内的代谢、调控瘤胃发酵和抑制甲烷排放的作用及机理作一综述,旨在为进一步研究类黄酮代谢与瘤胃微生物相互作用机制提供参考,也为未来开发类黄酮作为甲烷抑制剂提供思路。

本文引用格式

赵玉超 , 余诗强 , 蒋林树 . 生物类黄酮调控瘤胃微生态系统的作用——聚焦甲烷减排[J]. 动物营养学报, 2022 , 34(9) : 5452 -5465 . DOI: 10.3969/j.issn.1006-267x.2022.09.002

Abstract

The rumen is an important microbial ecosystem in ruminants. When microorganisms digest feed, they also generate methane. Methane emissions from ruminants account for about 6% of global anthropogenic greenhouse gas emissions. Therefore, there is an urgent need to adopt nutritional strategies to modulate the rumen microecosystem and reduce methanogenesis. As one of the most widely distributed compounds in plant secondary metabolites, flavonoids have various biological activities, such as antibacterial and antioxidant. The metabolism of flavonoids in rumen can affect the rumen fermentation pattern, inhibit the protozoa and archaea and other bacterial flora closely related to methanogenesis, thereby reducing methane emission, which is regarded as a potential methane inhibitor. In view of this, this review summarized the metabolism of flavonoids in the rumen, the regulation of rumen fermentation and the inhibition of methane emission and its mechanism, providing a reference for further research on the interaction of flavonoid metabolism and rumen microorganisms, and also contributing to the development of flavonoids as methane inhibitors.

参考文献

[1] MALMUTHUGE N, LIANG G X, GUAN L L.Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes[J].Genome Biology, 2019, 20(1):172.
[2] GERBER P J, STEINFELD H, HENDERSON B, et al.Tackling climate change through livestock:a global assessment of emissions and mitigation opportunities[M].Rome:FAO, 2013.
[3] MAASAKKERS J D, JACOB D J, SULPRIZIO M P, et al.Global distribution of methane emissions, emission trends, and OH concentrations and trends inferred from an inversion of GOSAT satellite data for 2010-2015[J].Atmospheric Chemistry and Physics, 2019, 19:7859-7881.
[4] MCALLISTER T A, MEALE S J, VALLE E, et al.Ruminant nutrition symposium:use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis[J].Journal of Animal Science, 2015, 93(4):1431-1449.  
[5] JOHNSON K A, JOHNSON D E.Methane emissions from cattle[J].Journal of Animal Science, 1995, 73(8):2483-2492.  
[6] MOSS A R, JOUANY J P, NEWBOLD J.Methane production by ruminants:its contribution to global warming[J].Annales de Zootechnie, 2000, 49(3):231-253.  
[7] PATRA A K, SAXENA J.A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen[J].Phytochemistry, 2010, 71(11/12):1198-1222.
[8] PATRA A K, SAXENA J.Dietary phytochemicals as rumen modifiers:a review of the effects on microbial populations[J].Antonie Van Leeuwenhoek, 2009, 96(4):363-375.  
[9] MA J, ZHENG Y M, TANG W J, et al.Dietary polyphenols in lipid metabolism:a role of gut microbiome[J].Animal Nutrition, 2020, 6(4):404-409.  
[10] WILLIAMSON G, KAY C D, CROZIER A, et al.The bioavailability, transport, and bioactivity of dietary flavonoids:a review from a historical perspective[J].Comprehensive Reviews in Food Science and Food Safety, 2018, 17(5):1054-1112.  
[11] JANSSEN P H, KIRS M.Structure of the archaeal community of the rumen[J].Applied and Environmental Microbiology, 2008, 74(12):3619-3625.  
[12] MORAÏS S, MIZRAHI I.Islands in the stream:from individual to communal fiber degradation in the rumen ecosystem[J].FEMS Microbiology Reviews, 2019, 43(4):362-379.  
[13] HACKMANN T J, NGUGI D K, FIRKINS J L, et al.Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids[J].Environmental Microbiology, 2017, 19(11):4670-4683.  
[14] HAQUE M N.Dietary manipulation:a sustainable way to mitigate methane emissions from ruminants[J].Journal of Animal Science and Technology, 2018, 60(1):15.
[15] ELLIS J L, DIJKSTRA J, KEBREAB E, et al.Aspects of rumen microbiology central to mechanistic modelling of methane production in cattle[J].Journal of Agricultural Science, 2008, 146(2):213-233.  
[16] UNGERFELD E M.Shifts in metabolic Hydrogen sinks in the methanogenesis-inhibited ruminal fermentation:a meta-analysis[J].Frontiers in Microbiology, 2015, 6:37.
[17] SUN K, LIU H H, FAN H Y, et al.Research progress on the application of feed additives in ruminal methane emission reduction:a review[J].PeerJ, 2021, 9:e11151.
[18] MIZRAHI I, WALLACE R J, MORAÏS S.The rumen microbiome:balancing food security and environmental impacts[J].Nature Reviews Microbiology, 2021, 19(9):553-566.  
[19] HONAN M, FENG X, TRICARICO J M, et al.Feed additives as a strategic approach to reduce enteric methane production in cattle:modes of action, effectiveness and safety[J/OL].Animal Production Science, 2021:1-15.[2022-01-10].https://www.publish.csiro.au/an/pdf/AN20295.DOI:10.1071/AN20295.
[20] FRIEDMAN N, SHRIKER E, GOLD B, et al.Diet-induced changes of redox potential underlie compositional shifts in the rumen archaeal community[J].Environmental Microbiology, 2017, 19(1):174-184.  
[21] HARBORNE J B, WILLIAMS C A.Advances in flavonoid research since 1992[J].Phytochemistry, 2000, 55(6):481-504.  
[22] PASSAMONTI S, TERDOSLAVICH M, FRANCA R, et al.Bioavailability of flavonoids:a review of their membrane transport and the function of bilitranslocase in animal and plant organisms[J].Current Drug Metabolism, 2009, 10(4):369-394.  
[23] GONG X, LI X, BO A, et al.The interactions between gut microbiota and bioactive ingredients of traditional Chinese medicines:a review[J].Pharmacological Research, 2020, 157:104824.
[24] GONZALES G B, SMAGGHE G, GROOTAERT C, et al.Flavonoid interactions during digestion, absorption, distribution and metabolism:a sequential structure-activity/property relationship-based approach in the study of bioavailability and bioactivity[J].Drug Metabolism Reviews, 2015, 47(2):175-190.  
[25] OSKOUEIAN E, ABDULLAH N, OSKOUEIAN A.Effects of flavonoids on rumen fermentation activity, methane production, and microbial population[J].BioMed Research International, 2013, 2013:349129.
[26] BERGER L M, WEIN S, BLANK R, et al.Bioavailability of the flavonol quercetin in cows after intraruminal application of quercetin aglycone and rutin[J].Journal of Dairy Science, 2012, 95(9):5047-5055.  
[27] BERGER L M, BLANK R, ZORN F, et al.Ruminal degradation of quercetin and its influence on fermentation in ruminants[J].Journal of Dairy Science, 2015, 98(8):5688-5698.  
[28] CUI K, GUO X D, TU Y, et al.Effect of dietary supplementation of rutin on lactation performance, ruminal fermentation and metabolism in dairy cows[J].Journal of Animal Physiology and Animal Nutrition, 2015, 99(6):1065-1073.  
[29] MUROTA K, NAKAMURA Y, UEHARA M.Flavonoid metabolism:the interaction of metabolites and gut microbiota[J].Bioscience, Biotechnology, and Biochemistry, 2018, 82(4):600-610.  
[30] BRAUNE A, BLAUT M.Bacterial species involved in the conversion of dietary flavonoids in the human gut[J].Gut Microbes, 2016, 7(3):216-234.  
[31] NYONYO T, SHINKAI T, MITSUMORI M.Improved culturability of cellulolytic rumen bacteria and phylogenetic diversity of culturable cellulolytic and xylanolytic bacteria newly isolated from the bovine rumen[J].FEMS Microbiology Ecology, 2014, 88(3):528-537.  
[32] JAMI E, ISRAEL A, KOTSER A, et al.Exploring the bovine rumen bacterial community from birth to adulthood[J].ISME Journal, 2013, 7(6):1069-1079.  
[33] LESSER S, CERMAK R, WOLFFRAM S.The fatty acid pattern of dietary fat influences the oral bioavailability of the flavonol quercetin in pigs[J].British Journal of Nutrition, 2006, 96(6):1047-1052.  
[34] LUNDH T J O, PETTERSSON H I, MARTINSSON K A.Comparative levels of free and conjugated plant estrogens in blood plasma of sheep and cattle fed estrogenic silage[J].Journal of Agricultural and Food Chemistry, 1990, 38(7):1530-1534.  
[35] WARNER D, DIJKSTRA J, HENDRIKS W H, et al.Stable isotope-labelled feed nutrients to assess nutrient-specific feed passage kinetics in ruminants[J].Journal of the Science of Food and Agriculture, 2014, 94(5):819-824.  
[36] GOHLKE A, INGELMANN C J, NVRNBERG G, et al.Bioavailability of quercetin from its aglycone and its glucorhamnoside rutin in lactating dairy cows after intraduodenal administration[J].Journal of Dairy Science, 2013, 96(4):2303-2313.  
[37] HEIM K E, TAGLIAFERRO A R, BOBILYA D J.Flavonoid antioxidants:chemistry, metabolism and structure-activity relationships[J].The Journal of Nutritional Biochemistry, 2002, 13(10):572-584.  
[38] KUMAR S, PANDEY A K.Chemistry and biological activities of flavonoids:an overview[J].The Scientific World Journal, 2013, 2013:162750.
[39] BODAS R, PRIETO N, GARCÍA-GONZÁLEZ R, et al.Manipulation of rumen fermentation and methane production with plant secondary metabolites[J].Animal Feed Science and Technology, 2012, 176(1/4):78-93.
[40] CUSHNIE T P T, LAMB A J.Antimicrobial activity of flavonoids[J].International Journal of Antimicrobial Agents, 2005, 26(5):343-356.  
[41] LOURENÇO M, CARDOZO P W, CALSAMIGLIA S, et al.Effects of saponins, quercetin, eugenol, and cinnamaldehyde on fatty acid biohydrogenation of forage polyunsaturated fatty acids in dual-flow continuous culture fermenters[J].Journal of Animal Science, 2008, 86(11):3045-3053.  
[42] LÓPEZ-CAMPOS O, BODAS R, PRIETO N, et al.Naringin dietary supplementation at 0.15% rates does not provide protection against sub-clinical acidosis and does not affect the responses of fattening lambs to road transportation[J].Animal, 2010, 4(6):958-964.  
[43] BALCELLS J, ARIS A, SERRANO A, et al.Effects of an extract of plant flavonoids (Bioflavex) on rumen fermentation and performance in heifers fed high-concentrate diets[J].Journal of Animal Science, 2012, 90(13):4975-4984.  
[44] SERADJ A R, ABECIA L, CRESPO J, 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[J].Animal Feed Science and Technology, 2014, 197:85-91.
[45] SINZ S, KUNZ C, LIESEGANG A, et al.In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formation[J].Czech Journal of Animal Science, 2018, 63(8):293-304.  
[46] LEIBER F, KUNZ C, KREUZER M.Influence of different morphological parts of buckwheat (Fagopyrum esculentum) and its major secondary metabolite rutin on rumen fermentation in vitro[J].Czech Journal of Animal Science, 2012, 57:10-18.
[47] ANDRÉS S, BODAS R, TEJIDO M L, et al.Effects of the inclusion of flaxseed and quercetin in the diet of fattening lambs on ruminal microbiota, in vitro fermentation and biohydrogenation of fatty acids[J].The Journal of Agricultural Science, 2016, 154(3):542-552.  
[48] JIMÉNEZ-OCAMPO R, MONTOYA-FLORES M D, HERRERA-TORRES E, et al.Effect of chitosan and naringin on enteric methane emissions in crossbred heifers fed tropical grass[J].Animals, 2021, 11(6):1599.
[49] STOLDT A K, DERNO M, DAS G, et al.Effects of rutin and buckwheat seeds on energy metabolism and methane production in dairy cows[J].Journal of Dairy Science, 2016, 99(3):2161-2168.  
[50] BROUDISCOU L P, PAPON Y, BROUDISCOU A F.Effects of dry plant extracts on fermentation and methanogenesis in continuous culture of rumen microbes[J].Animal Feed Science and Technology, 2000, 87(3/4):263-277.
[51] BROUDISCOU L P, LASSALAS B.Effects of Lavandula officinalis and Equisetum arvense dry extracts and isoquercitrin on the fermentation of diets varying in forage contents by rumen microorganisms in batch culture[J].Reproduction Nutrition Development, 2000, 40(5):431-440.  
[52] TAVENDALE M H, MEAGHER L P, PACHECO D, et al.Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis[J].Animal Feed Science and Technology, 2005, 123/124:403-419.
[53] 白齐昌, 郝小燕, 项斌伟, 等.沙棘黄酮对绵羊体外产气量、瘤胃发酵参数和微生物菌群的影响[J].动物营养学报, 2020, 32(3):1405-1414. BAI Q C, HAO X Y, XIANG B W, et al.Effects of sea buckthorn flavone on gas production, rumen fermentation parameters and microflora population of sheep in vitro[J].Chinese Journal of Animal Nutrition, 2020, 32(3):1405-1414.(in Chinese)
[54] BOUSSAADA A, ARHAB R, CALABRÒ S, et al.Effect of Eucalyptus globulus leaves extracts on in vitro rumen fermentation, methanogenesis, degradability and protozoa population[J].Annals of Animal Science, 2018, 18(3):753-767.  
[55] KIM E T, GUAN L L, LEE S J, et al.Effects of flavonoid-rich plant extracts on in vitro ruminal methanogenesis, microbial populations and fermentation characteristics[J].Asian-Australasian Journal of Animal Sciences, 2015, 28(4):530-537.  
[56] MA T, CHEN D D, TU Y, et al.Dietary supplementation with mulberry leaf flavonoids inhibits methanogenesis in sheep[J].Animal Science Journal, 2017, 88(1):72-78.  
[57] SZULC P, MRAV Č ÁKOVÁ D, SZUMACHER-STRABEL M, et al.Ruminal fermentation, microbial population and lipid metabolism in gastrointestinal nematode-infected lambs fed a diet supplemented with herbal mixtures[J].PLoS One, 2020, 15(4):e0231516.
[58] RAMOS-MORALES E, ROSSI G, CATTIN M, et al.The effect of an isoflavonid-rich liquorice extract on fermentation, methanogenesis and the microbiome in the rumen simulation technique[J].FEMS Microbiology Ecology, 2018, 94(3):fiy009.
[59] MORSY A S, SOLTAN Y A, SALLAM S M A, et al.Comparison of the in vitro efficiency of supplementary bee propolis extracts of different origin in enhancing the ruminal degradability of organic matter and mitigating the formation of methane[J].Animal Feed Science and Technology, 2015, 199:51-60.
[60] SANTOS N W, ZEOULA L M, YOSHIMURA E H, et al.Brazilian propolis extract used as an additive to decrease methane emissions from the rumen microbial population in vitro[J].Tropical Animal Health and Production, 2016, 48(5):1051-1056.  
[61] MORSY A S, SOLTAN Y A, EL-ZAIAT H M, et al.Bee propolis extract as a phytogenic feed additive to enhance diet digestibility, rumen microbial biosynthesis, mitigating methane formation and health status of late pregnant ewes[J].Animal Feed Science and Technology, 2021, 273:114834.
[62] 陈丹丹.四种植物提取物对肉羊甲烷排放、物质代谢及瘤胃微生物区系的影响[D].硕士学位论文.乌鲁木齐:新疆农业大学, 2014. CHEN D D.Effects of four plant extracts on methane emission, nutrients metabolism and rumen microflora in mutton sheep[D].Master's Thesis.Urumchi:Xinjiang Agricultural University, 2014.(in Chinese)
[63] EGER M, GRAZ M, RIEDE S, et al.Application of MootralTM reduces methane production by altering the archaea community in the rumen simulation technique[J].Frontiers in Microbiology, 2018, 9:2094.
[64] PATRA A K.Enteric methane mitigation technologies for ruminant livestock:a synthesis of current research and future directions[J].Environmental Monitoring and Assessment, 2012, 184(4):1929-1952.  
[65] GARCÍA-GONZÁLEZ R, LÓPEZ S, FERNÁNDEZ M, et al.Screening the activity of plants and spices for decreasing ruminal methane production in vitro[J].Animal Feed Science and Technology, 2008, 147(1/3):36-52.
[66] BEAUCHEMIN K A, MCGINN S M, MARTINEZ T F, et al.Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle[J].Journal of Animal Science, 2007, 85(8):1990-1996.  
[67] CALSAMIGLIA S, BUSQUET M, CARDOZO P W, et al.Invited review:essential oils as modifiers of rumen microbial fermentation[J].Journal of Dairy Science, 2007, 90(6):2580-2595.  
[68] JOUANY J P, MORGAVI D P.Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production[J].Animal, 2007, 1(10):1443-1466.  
文章导航

/