Chinese Journal of Animal Nutrition >

2024 , Vol. 36 >Issue 10: 6479 - 6493

DOI: https://doi.org/10.12418/CJAN2024.551

RESEARCH PAPER

Effects of Dietary Supplemented with Different Levels of Garlic Skin on Growth Performance, Nutrient Apparent Digestibility, Rumen Fermentation Parameters and Microbial Structure of Fuqing Goats

  • XU Qian , 1, 2 ,
  • WU Xianfeng 1, 2 ,
  • LIU Yuan , 1, 2, * ,
  • LI Wenyang , 1, 2, *
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  • 1 Institute of Animal Husbandry and Veterinary, Fujian Academy of Agricultural Science, Fuzhou 350013, China
  • 2 Fujian Key Laboratory of Animal Genetics and Breeding, Fuzhou 350013, China
*LIU Yuan, associate professor, E-mail: ;
LI Wenyang, professor, E-mail:

Received date: 2024-04-22

  Online published: 2024-10-14

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Abstract

The aim of this experiment was to investigate the effects of dietary supplemented with different levels of garlic skin on growth performance, nutrient apparent digestibility, rumen fermentation parameters and microbial structure of Fuqing goats. A total of 60 healthy 9-month-old Fuqing male goats were randomly divided into 4 groups with 15 replicates in each group and 1 goat in each replicate. Goats in 4 groups were fed experimental diets which using 0 (control group), 8% (experiment group Ⅰ), 16% (experiment group Ⅱ) and 24% (experiment group Ⅲ) garlic skin replace peanut seedlings in diets, respectively. The pre-experimental period lasted for 10 days, and the experimental period lasted for 90 days. The results showed as follows: 1) the gross energy (GE) apparent digestibility of experiment group Ⅲ was significantly higher than that of other groups (P<0.05), the neutral detergent fiber (NDF) apparent digestibility was significantly higher than that of the control group (P<0.05), and the acid detergent fiber (ADF) apparent digestibility was significantly higher than that of other groups (P<0.01). 2) The rumen ammonia nitrogen content of experiment groups Ⅱ and Ⅲ was significantly lower than that of the control group (P<0.05), the rumen propionate content was significantly higher than that of the control group (P<0.05), and the rumen acetate/propionate was significantly lower than that of control group and experiment group Ⅰ (P<0.01). 3) The rumen microbial Ace index, Chao1 index and PD_whole_tree index of experiment groups Ⅰ, Ⅱ and Ⅲ were significantly higher than those of the control group (P<0.05), and the Shannon index of experiment groups Ⅰ and Ⅱ was significantly higher than that of the control group (P<0.05). At the phylum level, the rumen Firmicutes relative abundance of experiment group Ⅲ was significantly higher than that of other groups (P<0.05), and the Bacteroidetes relative abundance was significantly lower than that of other groups (P<0.05). At the genus level, the rumen Prevotella relative abundance of experiment group Ⅲ was significantly lower than that of experiment groups Ⅰ and Ⅱ (P<0.05), the relative abundances of Lachnospiraceae_XPB1014_group, NK4A214_group and Christensenellaceae_R_7_group in rumen of experiment group Ⅲ were significantly higher than that of other groups (P<0.05), and the rumen Rikenellaceae_RC9_gut_group relative abundance of experiment group Ⅱ was significantly higher than that of control group and experiment group Ⅲ (P<0.05). 4) The relative abundance of bacterial genera was significantly positively correlated with apparent digestibility of NDF (P=0.034, r=0.250) and ADF (P=0.040, r=0.225), the Shannon index was significantly positively correlated with apparent digestibility of NDF (P=0.003, r=0.487) and ADF (P=0.01, r=0.347), and the Simpson index was significantly positively correlated with apparent digestibility of NDF (P=0.001, r=0.582) and ADF (P=0.001, r=0.582). The Quinella relative abundance was significantly negatively correlated with apparent digestibility of NDF, GE and crude protein (CP) (P<0.05). In summary, dietary supplemented with garlic skin can enhance the relative abundance and diversity of rumen microbiota, and improve the apparent digestibility of energy and crude fiber of Fuqing goats through the regulation of specific bacterial groups, thereby improving the rumen fermentation parameters, and the key bacterial genera are Lachnospiraceae_XPB1014_group and Quinella.

Key words： garlic skin; Fuqing goats; nutrient apparent digestibility; rumen microbiota

Cite this article

XU Qian , WU Xianfeng , LIU Yuan , LI Wenyang . Effects of Dietary Supplemented with Different Levels of Garlic Skin on Growth Performance, Nutrient Apparent Digestibility, Rumen Fermentation Parameters and Microbial Structure of Fuqing Goats[J]. Chinese Journal of Animal Nutrition, 2024 , 36(10) : 6479 -6493 . DOI: 10.12418/CJAN2024.551

近年来,农产品加工副产物被视为一种可行的粗饲料资源,尤其在反刍动物养殖领域,可部分替代常规粗饲料,成为畜牧业节本增效的发展方向。我国大蒜种植广泛、产量丰富,因此,大蒜产品作为粗饲料资源和添加剂逐渐得到推广应用。大蒜中富含多种活性物质,如大蒜素、二烯丙基硫醚和二烯丙基三硫醚等,这些化合物具有抗菌、抗氧化、抗炎、抗癌等生理活性[1-2]。近年来的研究证实,大蒜制品对反刍动物具有多种生物学益处[3-4],大蒜及其成分可改变瘤胃发酵参数,提高营养物质消化率,减少瘤胃原虫数量,降低甲烷排放[5]。大蒜皮作为大蒜加工副产物,含有与大蒜相同的活性物质,且粗蛋白质(CP)和粗纤维含量较高,是一种优质、经济的粗饲料资源[6]。
大蒜皮的饲料化利用已有一定研究。王海波等[7]研究表明,饲粮中添加3%的大蒜皮可增强湖羊机体免疫力和抗氧化能力,改善血清生化指标,并提高生长性能。另有研究显示,饲粮中添加8%的大蒜皮可提升杂交绵羊生长性能,对瘤胃微生物无影响[8]。杨燕等[4]研究指出,饲粮中添加15%的大蒜皮对羔羊免疫力和抗氧化能力具有积极影响。然而,现有研究多集中于大蒜皮中生理活性物质对机体的影响,对其饲用价值评定的研究较少。本课题组前期研究结果表明,不同品种羊对粗饲料的利用效率存在差异[9],地方品种山羊对大蒜皮的利用效果尚未知。因此,本研究以福建本地山羊品种——福清山羊为试验对象,系统探讨不同大蒜皮添加水平其对生长性能、营养物质表观消化率、瘤胃发酵参数和微生物结构的影响,旨在为大蒜皮的高效饲料化利用提供理论依据。

1 材料与方法

1.1 试验材料

试验所用大蒜皮购自福建省某大型羊场,来源于山东省济宁市。大蒜皮营养成分经测定,其干物质(DM)含量为89.34%,以DM为基础的总能(GE)为17.36 MJ/kg,有机物(OM)含量为93.17%,CP含量为6.28%,中性洗涤纤维(NDF)含量为52.22%,酸性洗涤纤维(ADF)含量为36.12%,钙(Ca)和磷(P)含量分别为0.31%和0.16%。

1.2 试验设计

1.2.1 育肥试验

本研究使用的试验动物和试验设计方案已通过福建省农业科学院畜牧兽医研究所实验动物伦理委员会伦理审查,伦理批准编号为202307FJ016。
育肥试验选取60只体重[(15.42±1.04) kg]相近、体况良好的9月龄福清山羊公羊羯羊,采用单因素随机试验设计,将试验羊分成4组,每组15个重复,每个重复1只羊。各组分别饲喂以0(对照组)、8%(试验Ⅰ组)、16%(试验Ⅱ组)和24%(试验Ⅲ组)大蒜皮替代饲粮中花生秧的试验饲粮。试验饲粮按15 kg肉用山羊日增重0.1 kg所需营养需要量,参照《肉羊饲养标准》(NY/T 816—2021)[10]配制,其组成及营养水平见表1。育肥试验共进行100 d,其中预试期10 d,正试期90 d。
表1 基础饲粮组成及营养水平(干物质基础)

Table 1 Composition and nutrient levels of experimental diets (DM basis)%

项目
Items		 对照组
Control group		 试验Ⅰ组
Experiment group Ⅰ		 试验Ⅱ组
Experiment group Ⅱ		 试验Ⅲ组
Experiment group Ⅲ
原料 Ingredients
豆粕 Soybean meal 14.0 14.0 14.0 14.0
玉米 Corn 21.0 21.0 21.0 21.0
花生秧 Peanut seedling 26.0 17.0 9.0
杂交狼尾草 Hybrid Penisetum 35.0 35.0 35.0 35.0
大蒜皮Garlic skin 8.0 16.0 24.0
食盐 NaCl 0.5 0.5 0.5 0.5
石粉 Limestone 0.4 0.6 1.0 1.5
磷酸氢钙 CaHPO4 0.7 1.0 0.2 0.2
磷酸脲 Urea phosphate 0.4 0.9 1.3 1.8
预混料 Premix1) 2.0 2.0 2.0 2.0
合计 Total 100.0 100.0 100.0 100.0
营养水平 Nutrient levels2)
干物质(鲜样) DM (fresh) 34.17 34.24 34.28 34.35
有机物 OM 88.15 87.84 87.89 87.63
总能 GE/(MJ/kg) 15.35 15.35 15.45 15.37
代谢能 ME/(MJ/kg) 9.24 9.22 9.24 9.24
粗蛋白质 CP 14.26 14.21 14.26 14.28
中性洗涤纤维 NDF 44.42 44.64 44.47 44.47
酸性洗涤纤维 ADF 22.11 22.14 22.12 22.10
钙 Ca 0.98 0.97 0.99 0.99
总磷 TP 0.54 0.54 0.56 0.55

1)预混料为每千克饲粮提供 The premix provided the following per kg of diets:Cu 20.0 mg,Fe 80.0 mg,Mn 30.0 mg,Zn 80.0 mg,I 1 mg,Se 0.30 mg,VA 20 000 IU,VD 5 000 IU,VE 50.0 mg。

2)代谢能为计算值,其他均为实测值。ME was a calculated value, while the others were measured values.

1.2.2 消化代谢试验

育肥试验结束后第1天进行消化代谢试验,各组随机挑选6只试验羊进入1.5 m×0.8 m消化代谢笼单独饲养,消化代谢笼可实现粪便与尿液自动分离,试验期间饲粮与育肥试验一致。消化代谢试验共进行15 d,其中预试期10 d,正试期5 d。

1.3 饲养管理

本试验于2023年2—6月在福建省农业科学院渔溪试验基地进行,试验所用羊只为该基地负责养殖和提供。试验开始前,统一对羊舍、饮水系统和消化代谢笼进行清理和消毒处理,并对所有的试验羊进行常规的驱虫和健胃。预试期内,试验羊只自由采食和饮水,详细统计各试验羊只预试期内每天饲粮的采食量。正试期内,根据预试期采食量设计饲粮日投喂量,保证每只试验羊的剩余饲粮约为总投喂量的5%。投喂工作分为2个时段,即每天的08:00和16:00,每个时段投喂总投喂量的1/2,同时保证试验羊的自由饮水。

1.4 样品采集

消化代谢试验正试期每日第1次饲喂(晨饲)前,收集试验羊的粪便及未采食的剩余饲粮。分别称量并记录试验羊只的粪便和剩余饲粮的总重量,取10%粪便样本用10%硫酸进行固氮处理,后将剩余饲粮和固氮处理后的粪便样本放入65 ℃的烘箱中烘干48 h,烘干后将样本粉碎并过40目筛,后让其回潮24 h备用。瘤胃液于正式试验期结束后的第1天晨饲前采集,使用瘤胃液收集器通过口腔采集约100 mL瘤胃液,后用4层无菌纱布进行过滤,并立即将其装入灭菌的50 mL EP管中,放入液氮中速冻,后于-80 ℃保存备用。

1.5 指标测定

1.5.1 生长性能测定

育肥试验正试期开始前记录试验羊初始体重(IBW),正式期结束后次日早晨记录试验羊终末体重(FBW),计算平均日增重(ADG)。每天准确记录每日每栏干物质投喂量以及剩余饲粮量,并以栏为单位计算每只试验羊干物质采食量(DMI)。

1.5.2 营养成分和营养物质表观消化率测定

试验饲粮、剩余饲粮和粪便样本中的DM、粗灰分(Ash)、OM和GE的测定及计算参考刘远等[9]描述的方法进行,CP含量按照GB/T 6432—2018[11]中方法测定,NDF和ADF含量采用Van Soest[12]的方法(CAU滤袋购自中国农业大学)测定。
营养物质表观消化率参照Adeola[13]的方法计算:

某营养物质表观消化率(%)=100×(食入该营养物质总量-粪中该营养物质总量)/食入该营养物质总量。

1.5.3 瘤胃发酵参数测定

瘤胃液采样时立即用便携式酸度计(PHB-1型,杭州奥立龙仪器有限公司)测定pH;氨态氮含量参考冯宗慈等[14]的方法测定;挥发性脂肪酸(VFA)含量采用气相色谱仪(GC-4000A,东西分析仪器有限公司)测定。

1.5.4 瘤胃微生物结构测定

使用TGuide S96磁性土壤/粪便DNA试剂盒[天根生物科技(北京)有限公司],按照说明书从24个样本(每组6个样本)中提取总基因组DNA。用引物F:5'-ACTCCTACGGGAGGCAGCA-3';R:5'-GGACTACHVGGGTWTCTAAT-3'扩增细菌16S rRNA高变区V3~V4。PCR产物在琼脂糖凝胶上检测,并通过Omega DNA纯化试剂盒(Omega Inc.,美国)纯化。收集纯化的PCR产物,在Illumina NovaSeq 6000平台上进行配对。
信息分析内容:使用USEARCH(10.0版本)将相似阈值大于97%的符合条件的序列分配到一个操作分类单元(OTU)。基于QIIME 2[15]中的朴素贝叶斯分类器,使用SILVA数据库[16](release 138.1)对OTU进行分类标注,置信阈值为70%。利用QIIME 2软件对各样本物种多样性复杂性进行Alpha鉴定。采用主坐标分析(PCoA)方法计算Beta多样性,评价样品的物种复杂性。采用单因素方差分析比较细菌相对丰度。利用在线平台BMKCloud对测序数据进行关联性分析。

1.6 数据统计方法

使用Excel软件初步统计数据,再利用SPSS 26.0软件进行单因素方差分析(one-way ANOVA),差异显著者采用Duncan氏法进行多重比较。结果用平均值和均值标准误(SEM)表示,P<0.01为差异极显著,P<0.05为差异显著,P>0.05为差异不显著。

2 结果

2.1 饲粮中添加不同水平大蒜皮对福清山羊生长性能和营养物质表观消化率的影响

由表2可知,饲粮中添加不同水平大蒜皮对福清山羊DMI、FBW、ADG以及DM、OM、CP表观消化率均无显著影响(P>0.05)。试验Ⅲ组的GE表观消化率显著高于其他各组(P<0.05),NDF表观消化率显著高于对照组(P<0.05),ADF表观消化率极显著高于其他各组(P<0.01)。
表2 饲粮中添加不同水平大蒜皮对福清山羊生长性能和营养物质表观消化率的影响

Table 2 Effects of dietary supplemented with different levels of garlic skin on growth performance and nutrient apparent digestibility of Fuqing goats

项目
Items		 对照组
Control
group		 试验Ⅰ组
Experiment
group Ⅰ		 试验Ⅱ组
Experiment
group Ⅱ		 试验Ⅲ组
Experiment
group Ⅲ		 SEM P值
P-value
生长性能 Growth performance
干物质采食量 DMI/(g/d) 640.07 643.01 642.04 645.52 1.250 0.484
初始体重 IBW/kg 15.33 15.40 15.52 15.43 0.523 0.818
终末体重 FBW/kg 23.33 23.45 23.16 23.18 0.984 0.842
平均日增重 ADG/(g/d) 88.90 89.41 84.95 86.19 1.432 0.652
营养物质表观消化率 Nutrient apparent digestibility/%
干物质 DM 56.25 58.64 59.14 58.94 0.450 0.054
有机物 OM 62.34 61.82 61.75 61.96 0.363 0.945
粗蛋白质 CP 67.85 72.69 71.48 73.03 0.809 0.075
总能 GE 57.18b 58.67b 57.19b 61.98a 0.596 0.017
中性洗涤纤维 NDF 51.77b 54.40ab 55.09ab 56.35a 0.557 0.021
酸性洗涤纤维 ADF 35.06Bb 35.07Bb 37.37Bb 40.35Aa 0.628 0.007

同行数据肩标不同小写字母表示差异显著(P<0.05),不同大写字母表示差异极显著(P<0.01),相同小写字母或无字母表示差异不显著(P>0.05)。下表同。

In the same row, values with different small letter superscripts mean significant difference (P<0.05), and with different capital letter superscripts mean significant difference (P<0.01), while with the same small letter or no letter superscripts mean no significant difference (P>0.05). The same as below.

2.2 饲粮中添加不同水平大蒜皮对福清山羊瘤胃发酵参数的影响

由表3可知,饲粮中添加不同水平大蒜皮对福清山羊瘤胃pH及乙酸、异丁酸、丁酸、异戊酸、戊酸和总挥发性脂肪酸(TVFA)含量无显著影响(P>0.05)。试验Ⅱ和Ⅲ组的瘤胃氨态氮含量显著低于对照组(P<0.05),瘤胃丙酸含量显著高于对照组(P<0.05),瘤胃乙酸/丙酸极显著低于对照组和试验Ⅰ组(P<0.01)。
表3 饲粮中添加不同水平大蒜皮对福清山羊瘤胃发酵参数的影响

Table 3 Effects of dietary supplemented with different levels of garlic skin on rumen fermentation parameters of Fuqing goats

项目
Items		 对照组
Control
group		 试验Ⅰ组
Experiment
group Ⅰ		 试验Ⅱ组
Experiment
group Ⅱ		 试验Ⅲ组
Experiment
group Ⅲ		 SEM P值
P-value
pH 6.63 6.61 6.68 6.63 0.034 0.900
氨态氮 NH3-N/(mg/dL) 16.35a 14.75ab 13.91b 13.46b 0.350 0.014
乙酸 Acetate/(mmoL/L) 27.38 29.68 28.08 28.92 0.612 0.588
丙酸 Propionate/(mmoL/L) 9.76b 10.35ab 11.09a 11.49a 0.230 0.039
异丁酸 Isobutyrate/(mmoL/L) 4.00 4.53 4.44 4.31 0.277 0.926
丁酸 Butyrate/(mmoL/L) 8.72 8.29 9.04 9.35 0.236 0.470
异戊酸 Isovalerate/(mmoL/L) 1.81 1.58 1.57 1.82 0.098 0.721
戊酸 Valerate/(mmoL/L) 2.81 2.77 2.96 2.76 0.109 0.914
乙酸/丙酸 Acetate/propionate 2.82Aa 2.87Aa 2.53Bb 2.52Bb 0.050 0.005
总挥发性脂肪酸 TVFA/(mmoL/L) 54.48 57.20 57.17 58.64 0.826 0.426

2.3 饲粮中添加不同水平大蒜皮对福清山羊瘤胃微生物结构的影响

2.3.1 瘤胃微生物Alpha多样性及Beta多样性

由表4可知,饲粮中添加不同水平大蒜皮对福清山羊瘤胃微生物Simpson指数无显著影响(P>0.05)。试验Ⅰ、Ⅱ和Ⅲ组的瘤胃微生物Ace指数、Chao1指数和PD_whole_tree指数均显著高于对照组(P<0.05),试验Ⅰ和Ⅱ组的瘤胃微生物Shannon指数显著高于对照组(P<0.05)。
表4 饲粮中添加不同水平大蒜皮对福清山羊瘤胃微生物Alpha多样性指数的影响

Table 4 Effects of dietary supplemented with different levels of garlic skin on rumen microbiota Alpha diversity indexes of Fuqing goats

项目
Items		 对照组
Control
group		 试验Ⅰ组
Experiment
group Ⅰ		 试验Ⅱ组
Experiment
group Ⅱ		 试验Ⅲ组
Experiment
group Ⅲ		 SEM P值
P-value
Ace指数 Ace index 1 099.425b 1 329.230a 1 419.717a 1 259.012a 41.981 0.031
Chao1指数 Chao1 index 1 088.841b 1 316.940a 1 409.307a 1 247.844a 41.681 0.029
Simpson指数 Simpson index 0.989 0.993 0.994 0.991 0.001 0.150
Shannon指数 Shannon index 8.190b 8.635a 8.695a 8.356ab 0.071 0.022
PD_whole_tree指数 PD_whole_tree index 116.352b 145.142a 148.702a 142.773a 4.899 0.045
覆盖度 Coverage 0.999 0.999 0.999 0.999 <0.001 0.135
由图1可知,Beta多样性主坐标分析(PCoA)结果显示,对照组与试验Ⅰ、Ⅱ和Ⅲ组的瘤胃微生物菌群按不同结构聚类,组间差异明显。
图1 福清山羊瘤胃微生物菌群主坐标分析

Fig.1 PCoA of rumen microbial flora of Fuqing goats

2.3.2 瘤胃微生物菌群相对丰度

由表5可知,在门水平上,相对丰度前10的菌门分别为厚壁菌门(Firmicutes)、拟杆菌门(Bacteroidetes)、髌骨菌门(Patescibacteria)、疣微菌门(Verrucomicrobiota)、变形菌门(Proteobacteria)、脱硫菌门(Desulfobacterota)、互养菌门(Synergistetes)、放线菌门(Actinobacteria)、蓝藻菌门(Cyanobacteria)和未分类细菌(unclassified_Bacteria)。其中,试验Ⅲ组的瘤胃厚壁菌门相对丰度显著高于其他各组(P<0.05),瘤胃拟杆菌门相对丰度显著低于其他各组(P<0.05)。
表5 饲粮中添加不同水平大蒜皮对福清山羊瘤胃微生物门水平和属水平微生物菌群相对丰度的影响

Table 5 Effects of dietary supplemented with different levels of garlic skin on relative abundance of rumen microbial flora at phylum level and genus level of Fuqing goats%

项目
Items		 对照组
Control
group		 试验Ⅰ组
Experiment
group Ⅰ		 试验Ⅱ组
Experiment
group Ⅱ		 试验Ⅲ组
Experiment
group Ⅲ		 SEM P值
P-value
门水平 Phylum level
厚壁菌门 Firmicutes 49.43b 50.83b 44.01b 61.65a 2.286 0.049
拟杆菌门 Bacteroidetes 33.81a 33.56a 40.45a 19.95b 2.559 0.034
髌骨菌门 Patescibacteria 2.96 4.04 3.45 4.43 0.518 0.826
疣微菌门 Verrucomicrobiota 3.59 2.08 3.17 4.10 0.300 0.089
变形菌门 Proteobacteria 3.53 2.24 3.69 2.63 0.460 0.632
脱硫菌门 Desulfobacterota 2.64 2.09 1.20 2.47 0.326 0.414
互养菌门 Synergistetes 2.19 1.92 1.93 1.14 0.235 0.550
放线菌门 Actinobacteria 0.32 1.19 0.20 2.30 0.353 0.164
蓝藻菌门 Cyanobacteria 0.70 0.91 1.02 0.24 0.147 0.299
未分类细菌 Unclassified_Bacteria 0.29 0.22 0.44 0.37 0.065 0.640
属水平 Genus level
普雷沃氏菌属 Prevotella 9.15ab 13.32a 14.66a 4.49b 1.399 0.048
未培养的瘤胃菌属
Uncultured_rumen_bacterium		 14.79 10.21 9.42 9.26 1.209 0.363
未分类毛螺菌科
Unclassified_Lachnospiraceae		 6.26 4.75 3.72 5.62 0.453 0.209
毛螺菌科XPB1014群
Lachnospiraceae_XPB1014_group		 3.14b 3.66b 4.37b 9.53a 0.714 0.005
奎氏菌属 Quinella 8.98 3.95 4.66 0.19 1.091 0.055
理研菌科RC9肠道群
Rikenellaceae_RC9_gut_group		 2.77b 4.15ab 7.21a 1.67b 0.766 0.047
NK4A214群 NK4A214_group 3.65b 3.40b 2.28b 8.21a 0.587 0.001
克里斯滕森菌科R_7群
Christensenellaceae_R_7_group		 3.53b 2.79b 1.84b 5.86a 0.415 0.002
候选单胞生糖菌属
Candidatus_Saccharimonas		 1.92 3.12 2.86 3.99 0.423 0.487
未分类F082
Unclassified_F082		 2.02 2.74 3.74 2.70 0.336 0.338
在属水平上,相对丰度前10的菌属分别为普雷沃氏菌属(Prevotella)、未培养的瘤胃菌属(uncultured_rumen_bacterium)、未分类毛螺菌科(unclassified_Lachnospiraceae)、毛螺菌科XPB1014群(Lachnospiraceae_XPB1014_group)、奎氏菌属(Quinella)、理研菌科RC9肠道群(Rikenellaceae_RC9_gut_group)、NK4A214群(NK4A214_group)、克里斯滕森菌科R_7群(Christensenellaceae_R_7_group)、候选单胞生糖菌属(Candidatus_Saccharimonas)和未分类F082(unclassified_F082)。其中,试验Ⅲ组的瘤胃普雷沃氏菌属相对丰度显著低于试验Ⅰ和Ⅱ组(P<0.05),试验Ⅲ组的瘤胃毛螺菌科XPB1014群、NK4A214群和克里斯滕森菌科R_7群相对丰度显著高于其他各组(P<0.05),试验Ⅱ组的瘤胃理研菌科RC9肠道群相对丰度显著高于对照组和试验Ⅲ组(P<0.05)。
采用随机森林分类法进一步分析对照组和试验Ⅲ组之间关键的差异瘤胃微生物,由图2和图3可知,在相对丰度前10的瘤胃微生物菌属中,重要度最高的是毛螺菌科XPB1014群和奎氏菌属,其丰相对度分别为3.14%、9.53%和8.98%、0.19%。
图2 基于福清山羊瘤胃微生物菌群的随机森林模型分析

Lachnospiraceae_XPB1014_group:毛螺菌科XPB1014群;Quinella:奎氏菌属;Sphingobacterium:鞘脂杆菌属;unclassified_Cyanobacteriales:未分类蓝藻菌目;[Anaerorhabdus]_furcosa_group:棍状厌氧菌属;Candidatus_Saccharimonas:糖类假丝酵母菌属;unclassified_Oxalobacteraceae:未分类草酸杆菌科;Lachnoclostridium:乳酸菌属;Lactococcus:乳球菌属;Pseudomonas:假单胞菌属;uncultured_rumen_bacterium_5C0d_16:未培养瘤胃细菌5C0d_16;unclassified_Eggerthellaceae:未分类的伊格尔兹氏菌科;[Eubacterium]_ventriosum_group:凸腹真杆菌属;unclassified_Coriobacteriales:未分类红蝽菌目;Atopobium:奇异菌属;Incertae Sedis:分类未定;Pyramidobacter:锥形杆菌属;Papillibacter:乳头杆菌属;Lachnospiraceae_ND3007_group:毛螺菌科ND3007群;unclassified_Coriobacteriales_Incertae_Sedis:未分类的赤毛杆菌目分类未定;uncultured_Erysipelotrichaceae_bacterium:未培养丹毒丝菌科细菌;Syntrophococcus:互养球菌属;Lachnospiraceae_NK4A136_group:毛螺菌科NK4A136群;unclassified_Diplorickettsiaceae:未分类梁立克星科;unclassified_Erysipelotrichaceae:未分类丹毒丝菌科;Chryseobacterium:金黄杆菌属;Family_ⅩⅢ_AD3011 group:Family_ⅩⅢ_AD3011群;Levilactobacillus:促生乳杆菌属;Mean Decrease Gini:基尼指数。

Fig.2 A random-forest model based on rumen microbial flora of Fuqing goats

图3 对照组和试验Ⅲ组奎氏菌属和毛螺菌科XPB1014群相对丰度

Quinella:奎氏菌属;Lachnospiraceae_XPB1014_group:毛螺菌科XPB1014群;Control:对照组 control group;Group3:试验Ⅲ组 experiment group Ⅲ。

Fig.3 Relative abundances of Quercella and Lachnospiraceae_XPB1014_group in control group and experiment group Ⅲ

2.4 营养物质表观消化率与瘤胃微生物菌群相关性分析

营养物质表观消化率与瘤胃微生物菌群相关性分析热图结果显示(图4),菌属相对丰度与NDF(P=0.034,r=0.250)和ADF(P=0.040,r=0.225)表观消化率显著正相关,Shannon指数与NDF(P=0.003,r=0.487)和ADF(P=0.010,r=0.347)表观消化率极显著正相关,Simpson指数与NDF(P=0.001,r=0.582)和ADF(P=0.001,r=0.582)表观消化率极显著正相关。进一步分析相对丰度前10的菌属与各营养物质表观消化率结果显示(图5),大部分菌属相对丰度与营养物质表观消化率呈现正相关,少数菌属呈现负相关,其中奎氏菌属相对丰度与NDF、GE和CP表观消化率显著负相关(P<0.05)。
图4 营养物质表观消化率与菌属和Alpha指数相关性分析网络组合图

Mantel’s p:环境因子与菌属和Alpha指数Mantel分析的P值 P-value of Mantel analysis between environmental factors and bacterial genera and Alpha index;Mantel’s r:环境因子与菌属和Alpha指数Mantel分析的r值 r value of Mantel analysis between environmental factors and bacterial genera and Alpha index;Pearson’s r:环境因子与菌属和Alpha指数相关性P值 P-value of correlation between environmental factors and bacterial genera and Alpha index;DM:干物质表观消化率 dry matter apparent digestibility;OM:有机物表观消化率 organic matter apparent digestibility;CP:粗蛋白质表观消化率 crude protein apparent digestibility;GE:总能表观消化率 gross energy apparent digestibility;NDF:中性洗涤纤维表观消化率 neutral detergent fiber apparent digestibility;ADF:酸性洗涤纤维表观消化率 acid detergent fiber apparent digestibility;Genus:菌属相对丰度 bacterial genera relative abundance;Shannon:Shannon指数 Shannon index;Simpson:Simpson指数 Simpson index;chao1:Chao1指数 Chao1 index;ACE:Ace指数 Ace index。

Fig.4 Network combination diagram of correlation analysis between nutrient apparent digestibility and bacterial genera and Alpha index

图5 营养物质表观消化率与相对丰度前10菌属相关性分析热图

GE:总能表观消化率 gross energy apparent digestibility;ADF:酸性洗涤纤维表观消化率 acid detergent fiber apparent digestibility;DM:干物质表观消化率 dry matter apparent digestibility;CP:粗蛋白质表观消化率 crude protein apparent digestibility;OM:有机物表观消化率 organic matter apparent digestibility;NDF:中性洗涤纤维表观消化率 neutral detergent fiber apparent digestibility;Quinella:奎氏菌属;uncultured_rumen_bacterium:未培养瘤胃细菌;unclassified_Lachnospiraceae:未分类毛螺菌科;Christensenellaceae_R_7_group:克里斯滕森菌科R_7群;NK4A214_group:NK4A214群;Prevotella:普雷沃氏菌属;Rikenellaceae_RC9_gut_group:理研菌科RC9肠道群;Candidatus_Saccharimonas:候选单胞生糖菌属;Lachnospiraceae_XPB1014_group:毛螺菌科XPB1014群。

*:显著相关(P<0.05)。*: significant correlation (P<0.05).

Fig.5 Heat map of correlation analysis between nutrient apparent digestibility and relative abundance of top 10 bacterial genera

3 讨论

3.1 饲粮中添加不同水平大蒜皮对福清山羊生长性能和营养物质表观消化率的影响

大蒜制品由于含有丰富的活性物质,已成为抗生素和非营养性化学饲料添加剂的替代品,被用在反刍动物中以促进其生长性能[17]。前人在大蒜制品对生长性能的研究结果不尽相同。有研究表明,饲粮中添加大蒜粉可以提高饲粮的适口性,从而增加羔羊的食欲,提升采食量[18];饲粮中添加大蒜皮显著提升湖羊的采食量[7]。另有研究显示,饲粮中添加大蒜粉对6~7月龄的山羊生长性能没有影响[19]。本试验结果显示,饲粮中添加不同水平大蒜皮对福清山羊DMI和ADG无显著影响,分析原因可能与肉羊品种、年龄及饲喂方式不同有关。此外,本课题组前期对福清山羊生长曲线的研究结果显示,参考NRC(2007)标准设计饲粮营养水平,9月龄福清山羊ADG约为60 g[20]。本研究中基础饲粮采用《肉羊饲养标准》(NY/T 816—2021)中ADG为100 g的营养需要量配制,试验期间试验羊的DMI和ADG均未达到预期,但较此前研究有明显提升。这一结果同时也反映出适宜的营养需求标准对地方品种山羊的重要性。总体来说,饲粮中添加大蒜皮对福清山羊DMI和ADG无不良影响。
营养物质表观消化率能够直观地反映机体对饲粮的消化吸收及利用效率。目前有关大蒜皮对营养物质表观消化率的研究较少,但已有研究表明大蒜粉可以提高ADF和NDF表观消化率[21]。Ma等[1]研究显示,大蒜粉中的大蒜素可以增加纤维素分解细菌的数量,进而提高ADF和NDF表观消化率。
在本试验中,饲粮中添加不同水平大蒜皮可提高福清山羊的ADF和NDF表观消化率,与上述研究结果相一致。这可能是由于大蒜皮中含有大蒜素[22],增加了瘤胃中纤维素分解相关微生物的数量,从而提高了纤维素的利用率。纤维素和半纤维素等结构性碳水化合物是饲粮中主要的能量来源,因此机体对ADF和NDF的利用效率也影响GE表观消化率[23]。在本试验中,饲粮中添加不同水平大蒜皮可提高GE表观消化率,这与机体对纤维素的消化率结果相一致,表明添加大蒜皮有助于提高饲粮中GE的利用效率。此外,含有活性物质的草本植物可以通过刺激瘤胃中纤维素分解细菌的活性,抑制原生动物和产甲烷细菌的生长来提高营养物质的利用,从而降低甲烷排放造成的能量损失[24]。Zhu等[25]的研究结果显示,大蒜皮中的活性物质可减少瘤胃甲烷排放,进而提高能量利用率,这能进一步解释本试验中大蒜皮对GE表观消化率的提升作用。DM和OM表观消化率反映的是饲粮的平均消化能力,CP表观消化率是评价饲粮饲用效率的关键因素之一。有研究结果显示,饲粮中添加大蒜粉能提高羔羊DM、CP和OM表观消化率[26]。另一项研究显示,大蒜粉对于6~7月龄的山羊生长性能和采食量没有影响,甚至会以剂量依赖性的方式降低CP表观消化率[19]。本试验中,饲粮中添加不同水平大蒜皮对福清山羊的CP、DM和OM表观消化率无显著影响,分析原因可能与肉羊年龄、品种以及饲粮原料组成和饲喂方式等因素相关。总体来说,饲粮中添加不同水平大蒜皮可提升福清山羊ADF、NDF和GE表观消化率。

3.2 饲粮中添加不同水平大蒜皮对瘤胃发酵参数和微生物结构的影响

瘤胃发酵参数可以反映饲粮营养物质在瘤胃内的利用效率。瘤胃pH是反映反刍动物瘤胃环境稳态和瘤胃发酵程度的综合指标,瘤胃的适宜pH在6.00~7.00,此时瘤胃纤维素降解菌的活性最高[27]。本试验中,各组之间瘤胃pH差异不显著,且均在正常范围内,表明添加大蒜皮不会影响瘤胃发酵稳态。饲粮中蛋白质和非蛋白氮(尿素和氨基酸)代谢的主要最终产物是瘤胃氨态氮,它是瘤胃微生物合成菌体蛋白的前体物质[28]。研究表明,添加大蒜制品可以通过提升瘤胃微生物相对丰度,增加瘤胃微生物蛋白质合成,进而降低瘤胃氨态氮含量[29]。本试验中,饲粮中添加16%和24%大蒜皮可显著降低瘤胃氨态氮含量,Alpha多样性和Beta多样性结果显示饲粮中添加大蒜皮后福清山羊瘤胃微生物在相对丰度和多样性方面都高于对照组,表明添加大蒜皮能改善瘤胃微生物结构。瘤胃内VFA提供反刍动物70%~80%的能量需求[7]。本试验研究结果显示,饲粮中添加16%和24%大蒜皮可显著提高瘤胃丙酸含量,显著降低乙酸/丙酸,该结果与大蒜制品在其他反刍动物中的研究结果[29-30]一致。丙酸是肝脏糖异生的主要底物,占反刍动物总能量需求的24%~61%[31],乙酸/丙酸与能量利用效率相关,该值的高低与能量利用率成反比。本试验结果表明,饲粮中添加大蒜皮可提升动物对能量的利用率,这与前文GE表观消化率的结果一致。
瘤胃微生物菌群与反刍动物生长性能和营养物质表观消化率密切相关[32]。厚壁菌门和拟杆菌门是反刍动物瘤胃微生物的优势菌群,是对粗饲料利用的关键菌群[33],厚壁菌门主要参与纤维素半纤维素的降解利用,拟杆菌门在反刍动物瘤胃的发酵过程中主要参与非纤维植物成分的分解和吸收过程中[34]。有研究表明,厚壁菌门相对丰度的增加和拟杆菌门相对丰度的减少可促进山羊生长[35]。本试验结果显示,饲粮中添加不同水平大蒜皮可影响福清山羊瘤胃微生物结构,添加24%大蒜皮可显著提高瘤胃厚壁菌门相对丰度,显著降低瘤胃拟杆菌门相对丰度,同时这一效果与大蒜皮的添加水平有关,这可能与大蒜皮所含生理活性物质含量相关。瘤胃菌属相对丰度分析结果显示,饲粮中添加24%大蒜皮可显著提高瘤胃毛螺菌科XPB1014群、NK4A214群和克里斯滕森菌科R_7群相对丰度。Dai等[36]报道,克里斯滕森菌科R_7群可能在半纤维素和纤维素的降解中起重要作用。最近的研究表明,克里斯滕森菌科R_7群参与氨基酸和脂质代谢[37]。研究表明,这些菌属与多种结构碳水化合物的降解以及丙酸盐和丁酸盐的产生有关[38-39],可能为宿主提供更多的能量和健康的瘤胃环境。奎氏菌属是一种条件致病菌[40],有研究表明,植物中的活性多糖能减少致病菌奎氏菌属的相对丰度,促进有益瘤胃细菌的生长繁殖,减少致病菌对碳水化合物等营养物质的消耗[41]。另有研究显示,随着瘤胃中奎氏菌属相对丰度的降低,湖羊免疫力得到提升[42]。本研究结果显示,毛螺菌科XPB1014群和奎氏菌属是组间差异的关键瘤胃微生物,在改变瘤胃发酵状态中可能起到主要作用,随着饲粮中大蒜皮添加水平增加,瘤胃毛螺菌科XPB1014群相对丰度上升,瘤胃奎氏菌属相对丰度下降,表明饲粮中添加一定水平大蒜皮可以提升瘤胃有益菌的相对丰度,具体是否是由于蒜皮中的活性成分所起到作用还有待进一步研究。

3.3 营养物质表观消化率与瘤胃微生物菌群相关性分析

反刍动物通过瘤胃发酵来完成营养物质的消化利用,而瘤胃微生物在瘤胃发酵活性中起关键作用,直接影响饲粮整体消化效率[43]。在上文的研究中发现,大蒜皮对瘤胃微生物的相对丰度和多样性以及对纤维素消化相关菌属的相对丰度影响较大,分析认为这是影响营养物质表观消化率的关键,因此本试验评估了菌属相对丰度和Alpha多样性与各营养物质表观消化率的相关性。结果显示,饲粮中添加大蒜皮后菌属相对丰度与ADF和NDF表观消化率显著正相关。进一步研究菌属与表观消化率的关联性分析结果显示,奎氏菌属相对丰度与NDF、GE和CP表观消化率显著负相关,这与前文研究结果一致,即饲粮中添加大蒜皮有降低瘤胃中奎氏菌属相对丰度的趋势,表明添加大蒜皮可提升饲粮的营养物质表观消化率,虽然奎氏菌属相对丰度下降未达到显著水平,可能是由于样本量不够及个体差异大造成。总的来说,本试验结果表明饲粮中添加大蒜皮可能通过调节瘤胃微生物相对丰度以及与纤维消化相关的特定瘤胃微生物群来提升NDF和ADF表观消化率。

4 结论

饲粮中添加大蒜皮可提升瘤胃微生物相对丰度及多样性,并通过对特定菌群的调控提升福清山羊对能量和粗纤维的表观消化率,改善瘤胃发酵参数,其中起到关键作用的菌属是毛螺菌科XPB1014群和奎氏菌属。

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
MA T, CHEN D D, TU Y, et al. Effect of supplementation of allicin on methanogenesis and ruminal microbial flora in Dorper crossbred ewes[J]. Journal of Animal Science and Biotechnology, 2016,7:1.

[2]
PANYOD S, WU W K, HO C T, et al. Diet supplementation with allicin protects against alcoholic fatty liver disease in mice by improving anti-inflammation and antioxidative functions[J]. Journal of Agricultural and Food Chemistry, 2016, 64(38):7104-7113.

DOI PMID

[3]
ZAFARIAN R, MANAFI M. Effect of garlic powder on methane production,rumen fermentation and milk production of buffaloes[J]. Annual Review & Research in Biology, 2013, 3(4):1013-1019.

[4]
杨燕, 王慧, 吕慎金. 不同比例大蒜皮对沂蒙黑山羊血清生化、免疫力及抗氧化功能的影响[J]. 饲料研究, 2021, 44(8):1-5.

YANG Y, WANG H, LV S J. Effect of different proportions of garlic skin on serum biochemical,immunity and antioxidation of Yimeng-black goats[J]. Feed Research, 2021, 44(8):1-5. (in Chinese)

[5]
WANAPAT M, CHERDTHONG A, PHESATCHA K, et al. Dietary sources and their effects on animal production and environmental sustainability[J]. Animal Nutrition, 2015, 1(3):96-103.

DOI PMID

[6]
王敬林, 魏源浩, 武小娇, 等. 大蒜不同部位副产物与奶牛常规粗饲料瘤胃降解特性对比研究[J]. 动物营养学报, 2021, 33(10):5708-5716.

DOI

WANG J L, WEI Y H, WU X Q, et al. Comparative study on rumen degradation characteristics of different parts of garlic by-products and common roughages for dairy cows[J]. Animal Nutrition, 2021,10:5708-5716. (in Chinese).

[7]
王海波, 占今舜, 谷志勇, 等. 饲粮中添加大蒜皮对湖羊生长性能、瘤胃发酵参数及血清生化、免疫和抗氧化指标的影响[J]. 动物营养学报, 2024, 36(1):406-415.

DOI

WANG H B, ZHAN J S, GU Z Y, et al. Effects of dietary garlic peel on growth performance,rumen fermentation parameters,serum biochemical,immune and antioxidant indices of Hu sheep[J]. Chinese Journal of Animal Nutrition, 2024, 36(1):406-415. (in Chinese)

[8]
苏震. 大蒜皮对肉羊瘤胃微生物生长代谢的影响[D]. 硕士学位论文. 合肥: 安徽农业大学, 2021.

SU Z. Effects of garlic peel on rumen microbial growth and metabolism of mutton sheep[D]. Master’s Thesis. Hefei: Anhui Agricultural University, 2020. (in Chinese)

[9]
刘远, 吴贤锋, 王迎港, 等. 饲粮中发酵豆渣添加水平对不同品种山羊营养物质消化代谢的影响[J]. 动物营养学报, 2022, 34(10):6565-6575.

DOI

LIU Y, WU X F, WANG Y G, et al. Effects of dietary fermented soybean curd residue supplemental level on digestion and metabolism of different goat breeds[J]. Chinese Journal of Animal Nutrition, 2022, 34(10):6565-6575. (in Chinese)

DOI

[10]
中华人民共和国农业部. 肉羊饲养标准:NY/T 816—2021[S]. 北京: 中国农业出版社, 2021.

The Ministry of Agriculture of the People’s Republic of China. Feeding standard of meat-producing sheep and goats:NY/T 816—2021[S]. Beijing: China Agriculture Press, 2021. (in Chinese).

[11]
国家市场监督管理总局, 中国国家标准化管理委员会.饲料中粗蛋白的测定凯氏定氮法:GB/T 6432—2018[S]. 北京: 中国标准出版社, 2018.

State Administration for Market Regulation, Standardization Administration. Determination of crude protein in feeds-Kjeldahl method:GB/T 6432—2018[S]. Beijing: Standards Press of China, 2018. (in Chinese)

[12]
VAN SOEST P J. Development of a comprehensive system of feed analyses and its application to forages[J]. Journal of Animal Science, 1967, 26(1):119-128.

[13]
ADEOLA O. Digestion and balance techniques in pigs[M]. 2nd ed. Bocaraton: CRC Press, 2000.

[14]
冯宗慈, 高民. 通过比色测定瘤胃液氨氮含量方法的改进[J]. 畜牧与饲料科学, 2010 (6):37.

FENG Z C, GAO M. Improvement of colorimetric method for determination of ammonia nitrogen content in rumen fluid[J]. Animal Husbandry and Feed Science, 2010(6):37. (in Chinese)

[15]
BOLYEN E, RIDEOUT J R, DILLON M R, et al. Reproducible,interactive,scalable and extensible microbiome data science using QIIME 2[J]. Nature Biotechnology, 2019, 37(8):852-857.

[16]
CALLAHAN B J, MCMURDIE P J, ROSEN M J, et al. DADA2:high-resolution sample inference from illumina amplicon data[J]. Nature Methods, 2016, 13(7):581-583.

[17]
DING H, AO C J, ZHANG X Q. Potential use of garlic products in ruminant feeding:a review[J]. ANIMAL NUTRITION, 2023,14:343-355.

[18]
EL N S, IBRAHIM E M. Impact of incorporating garlic or cumin powder in lambs ration on nutrients digestibility,blood constituents and growth performance[J]. Egyptian Journal of Nutrition and Feeds, 2018,21:355-364.

[19]
IKYUME T T, SOWANDE O S, DELE P A, et al. Effect of varying levels of garlic (Allium sativum) powder on growth,apparent nutrient digestibility,rumen ecology,blood profile and cost analysis of feeding West African Dwarf goats[J]. Malaysian Journal of Animal Science, 2017, 20(2):61-74.

[20]
刘远, 吴贤锋, 李文杨, 等. 不同饲养方式对福清山羊生长曲线的影响[J]. 福建农业学报, 2018, 33(6):566-570.

LIU Y, WU X F, LI W Y, et al. Growth of Fuqing goats raised under different husbandry methods[J]. Fujian Journal of Agricultural Sciences, 2018, 33(6):566-570. (in Chinese)

[21]
PATRA A K, KAMRA D N, BHAR R, et al. Effect of terminalia chebula and Allium sativum on in vivo methane emission by sheep[J]. Journal of Animal Physiology and Animal Nutrition, 2011, 95(2):187-191.

[22]
SHANG A, CAO S Y, XU X Y, et al. Bioactive compounds and biological functions of garlic (Allium sativum L.)[J]. Foods, 2019, 8(7):246.

[23]
刘远, 吴贤锋, 占今舜, 等. 饲粮中添加过瘤胃赖氨酸对福清山羊生长性能、养分表观消化率和氮代谢的影响[J]. 动物营养学报, 2022, 34(1):432-441.

DOI

LIU Y, WU X F, ZHAN J S, et al. Effects of dietary rumen protected lysine on growth performance,nutrient apparent digestibilities and nitrogen metabolism of Fuqing goats[J]. Chinese Journal of Animal Nutrition, 2022, 34(1):432-441. (in Chinese)

[24]
LAN W, YANG C L. Ruminal methane production:associated microorganisms and the potential of applying hydrogen-utilizing bacteria for mitigation[J]. Science of the Total Environment, 2019,654:1270-1283.

[25]
ZHU W, SU Z, XU W, et al. Garlic skin induces shifts in the rumen microbiome and metabolome of fattening lambs[J]. Animal, 2021, 15(5):100216.

[26]
KEWAN K Z, ALI M M, AHMED B M, et al. The effect of yeast (Saccharomyces cerevisiae),garlic (Allium sativum) and their combination as feed additives in finishing diets on the performance,ruminal fermentation,and immune status of lambs[J]. Egyptian Journal of Nutrition and Feeds, 2021,24:55-76.

[27]
VIENNASAY B, WANAPAT M. Strategic supplementation of Flemingia silage to enhance rumen fermentation efficiency,microbial protein synthesis and methane mitigation in beef cattle[J]. BMC Veterinary Research, 2020, 16(1):480.

[28]
徐倩, 张富, 吴贤锋, 等. 饲粮发酵啤酒糟水平对闽东山羊生长性能、消化代谢、血清生化指标及瘤胃发酵的影响[J]. 动物营养学报, 2024, 36(1):416-427.

DOI

XU Q, ZHANG F, WU X F, et al. Effects of dietary fermented brewer’s grains level on growth performance,digestion and metabolism,serum biochemical indices and rumen fermentation of mindong goats[J]. Chinese Journal of Animal Nutrition, 2024, 36(1):416-427. (in Chinese)

[29]
ZHONG R Z, XIANG H, CHENG L, et al. Effects of feeding garlic powder on growth performance,rumen fermentation,and the health status of lambs infected by gastrointestinal nematodes[J]. Animals, 2019, 9(3):102.

[30]
PATRA A K, KAMRA D N, AGARWAL N. Effects of extracts of spices on rumen methanogenesis,enzyme activities and fermentation of feeds in vitro[J]. Journal of the Science of Food and Agriculture, 2010, 90(3):511-520.

[31]
VYAS D, ALEMU A W, MCGINN S M, et al. The combined effects of supplementing monensin and 3-nitrooxypropanol on methane emissions,growth rate,and feed conversion efficiency in beef cattle fed high-forage and high-grain diets[J]. Journal of Animal Science, 2018, 96(7):2923-2938.

[32]
DU H X, ERDENE K, CHEN S Y, et al. Correlation of the rumen fluid microbiome and the average daily gain with a dietary supplementation of Allium mongolicum regel extracts in sheep[J]. Journal of Animal Science, 2019, 97(7):2865-2877.

[33]
GHARECHAHI J, VAHIDI M F, SHARIFI G, et al. Lignocellulose degradation by rumen bacterial communities:new insights from metagenome analyses[J]. Environmental Research, 2023,229:115925.

[34]
WANG B, LUO H L. Effects of mulberry leaf silage on antioxidant and immunomodulatory activity and rumen bacterial community of lambs[J]. BMC Microbiology, 2021, 21(1):250.

DOI PMID

[35]
WANG M Y, WU L F, GUO Y Q, et al. Effects of fermented herbal tea residue on meat quality,rumen fermentation parameters and microbes of black goats[J]. AMB Express, 2023, 13(1):106.

[36]
DAI X, TIAN Y, LI J T, et al. Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in the cow rumen[J]. Applied and Environmental Microbiology, 2015, 81(4):1375-1386.

PMID

[37]
WATERS J L, LEY R E. The human gut bacteria Christensenellaceae are widespread,heritable,and associated with health[J]. BMC Biology, 2019, 17(1):83.

[38]
MOROTOMI M, NAGAI F, WATANABE Y. Description of Christensenella minuta gen.nov.,sp. nov.,isolated from human faeces,which forms a distinct branch in the order Clostridiales,and proposal of Christensenellaceae fam.nov[J]. International Journal of Systematic and Evolutionary Microbiology, 2012, 62(Pt 1):144-149.

[39]
WEINERT-NELSON J R, BIDDLE A S, WILLIAMS C A. Fecal microbiome of horses transitioning between warm-season and cool-season grass pasture within integrated rotational grazing systems[J]. Animal Microbiome, 2022, 4(1):41.

[40]
WANG B, LIU J T, LEI R Y, et al. Cold exposure,gut microbiota,and hypertension:a mechanistic study[J]. Science of the Total Environment, 2022,833:155199.

[41]
ZHANG X Y, LIU X L, CHANG S H, et al. Effect of Cistanche deserticola on rumen microbiota and rumen function in grazing sheep[J]. Frontiers in Microbiology, 2022,13:840725.

[42]
DU X, CHENG X D, DONG Q X, et al. Dietary supplementation of fruit from Nitraria tangutorum improved immunity and abundance of beneficial ruminal bacteria in Hu sheep[J]. Animals:an Open Access Journal from MDPI, 2022, 12(22):3211.

[43]
YI S M, DAI D W, WU H, et al. Dietary concentrate-to-forage ratio affects rumen bacterial community composition and metabolome of yaks[J]. Frontiers in Nutrition, 2022,9:927206.

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