Chinese Journal of Animal Nutrition >

2026 , Vol. 38 >Issue 3: 2068 - 2085

DOI: https://doi.org/10.12418/CJAN2026.166

RESEARCH PAPER

Effects of Dextran and Polyglutamic Acid on Rumen Fermentation Parameters, Microbial Flora and Metabolome in Perinatal Dairy Goats

  • ZHAO Meng , 1, 2 ,
  • WANG Yang 3 ,
  • LIANG Yating 1 ,
  • WANG Xiao 3 ,
  • DU Ruiping , 1, 2, *
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  • 1 Institute of Animal Nutrition and Feed Science, Inner Mongolia Academy of Agricultural & Animal Husbandry Science, Hohhot 010031, China
  • 2 Key Laboratory of Grass-Feeding Livestock Healthy Breeding and Livestock Product Quality Control (Co-Construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Hohhot 010031, China
  • 3 School of Life Science, Inner Mongolia University, Hohhot 010018, China
*professor, E-mail:

Received date: 2025-09-02

  Online published: 2026-03-16

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Abstract

This experiment was conducted to investigate the effects of dextran and polyglutamic acid on rumen fermentation parameters, microbial flora and metabolome of perinatal dairy goats. Eighteen healthy primiparous Saanen dairy goats in late pregnancy with similar body weight [(40.00±1.73) kg] were randomly divided into 3 groups (6 goats per group): a high-dose group (HI group), a low-dose group (LO group) and a control group (CON group). Goats in the HI group were orally administered with 3 g dextran+20 g polyglutamic acid per day, those in the LO group were orally administered with 1.5 g dextran+10 g polyglutamic acid per day, and those in the CON group were orally administered with the same volume of normal saline per day. The continuous oral administration lasted for 42 days (21 days before parturition and 21 days after parturition). Rumen fluid samples were collected on day 1 and day 21 postpartum for the determination of rumen fermentation parameters, microbial flora and metabolome. The results showed as follows: 1) on day 21 postpartum, the valeric acid content in rumen fluid of the LO group and HI group was significantly higher than that of the CON group (P<0.05), the butyric acid content tended to be higher than that of the CON group (P=0.057), and the ammonia nitrogen content tended to be lower than that of the CON group (P=0.073). On day 21 postpartum, there were no significant differences in all rumen fermentation parameters among the three groups (P>0.05). 2) On day 21 postpartum, the α diversity indexes of rumen microbiota (except Goods_coverage index) in the HI group were higher than those in the CON group and LO group, but the differences were not significant (P>0.05). On day 21 postpartum, the proportion and abundance of Prevotella in rumen of the HI group were higher than those in the CON group and LO group. The two significantly different microbial predictive functions with the highest enrichment degree in the HI group were RNA polymerase and biosynthesis of unsaturated fatty acids. On day 21 postpartum, the differential microorganisms between the HI group and CON group showed significant differences in the functions of Staphylococcus aureus infection and ECM-receptor interaction (P<0.05). 3) On day 21 postpartum, compared with the CON group, the significantly up-regulated differential metabolites in rumen fluid of the HI group included 4,4'-diaminodibutylamine classified as heterocyclic compounds, pyridoxamine-5'-phosphate classified as organic acids and their derivatives, and L-methionine sulfoxide classified as amino acids and their metabolites (P<0.05); the significantly down-regulated differential metabolites included 4-(3-methylbutoxy) aniline hydrochloride classified as benzene and its derivatives, trans-2-hexenal dimethyl acetal, and Trp-Ile classified as amino acids and their metabolites (P<0.05). The metabolic pathways with high significant differences between the two groups were cysteine and methionine metabolism and inflammatory mediator regulation of TRP channels. In conclusion, oral administration of dextran and polyglutamic acid can promote the rumen fermentation function, increase the proportion and abundance of rumen dominant microbiota, and improve the abundance of energy-supplying nutrient metabolites in the rumen of perinatal dairy goats.

Key words： dextran; polyglutamic acid; perinatal period; dairy goat; rumen microbiota; metabolome

Cite this article

ZHAO Meng , WANG Yang , LIANG Yating , WANG Xiao , DU Ruiping . Effects of Dextran and Polyglutamic Acid on Rumen Fermentation Parameters, Microbial Flora and Metabolome in Perinatal Dairy Goats[J]. Chinese Journal of Animal Nutrition, 2026 , 38(3) : 2068 -2085 . DOI: 10.12418/CJAN2026.166

围产期是奶山羊生产周期的关键阶段,此阶段奶山羊需经历妊娠-分娩-泌乳的剧烈生理转变,机体随之启动复杂的生理适应与代谢重构进程。在此过程中,奶山羊的消化系统功能发生显著改变,妊娠后期瘤胃容积因胎儿挤压而缩小,导致采食量下降;同时内分泌系统发生剧烈调整,催乳素、生长激素等激素水平显著波动,免疫系统功能呈现暂时性抑制状态[1]。这些生理变化共同促使奶山羊陷入能量负平衡状态,不仅极易诱发酮病、低血钙症、胎衣不下等代谢紊乱性疾病,还会因免疫功能削弱,大幅增加子宫内膜炎、乳房炎等感染性疾病的发生风险。上述病症不仅严重损害奶山羊的健康状况,还会导致其产奶量下降、繁殖性能降低,最终影响生产经济效益[2-3]。因此,有效调控围产期奶山羊的机体代谢,提升其健康水平和生产性能,是当前奶畜养殖产业亟待解决的重要课题之一。
营养调控是应对奶山羊围产期能量负平衡及改善奶山羊瘤胃健康和生产性能的重要策略。在绿色减抗的大环境下,养殖业对天然、安全、高效饲料添加剂的需求急剧增长。在此趋势下,天然绿色的营养活性物质逐渐成为饲料添加剂领域的研究热点,其在畜牧生产中的应用受到广泛关注[4-5]。葡聚糖(dextran,DEX)是一类广泛存在于植物、真菌和细菌中的天然多糖,其分子结构复杂多样,具有显著的免疫调节[6]、抗氧化[7]、改善肠道健康[8]等多种生物活性功能,能够通过增强动物机体的免疫功能、清除自由基、维持肠道微生态平衡等多种途径,提升动物的健康水平和生产性能。聚谷氨酸(polyglutamic acid,PGA)属于生物高分子物质,其分子结构由多个谷氨酸单元经生物合成聚合而成,具有优异的生物相容性和多功能性,能够促进矿物质吸收、增强免疫力、改善动物生产性能等,尤其是在提高饲料利用率、增强动物抗病能力以及改善肉、蛋、奶品质方面表现出显著优势[9]。作为备受关注的天然营养活性成分,葡聚糖与聚谷氨酸因其特有的生物学效应及潜在的生理调节功能,在减抗替代及营养调控应用方面拥有广阔的前景。
然而,目前关于葡聚糖与聚谷氨酸作为功能性营养调控剂在围产期奶山羊中应用的研究仍较少,尤其二者对围产期奶山羊瘤胃功能的影响尚不明确,需通过系统性试验研究与数据结果进行佐证。基于此,本研究通过对围产期奶山羊灌服葡聚糖与聚谷氨酸,系统探究其对奶山羊瘤胃发酵参数、微生物区系及代谢组的影响,旨在为二者作为围产期奶山羊功能性饲料添加剂提供数据支持,助力畜牧业减抗替抗进程,为畜牧业绿色、健康、可持续发展提供理论依据。

1 材料与方法

1.1 试验动物选择及分组

选取18只健康状况良好、体重[(40.00±1.73) kg]相近的头胎妊娠后期萨能奶山羊,随机分为3组,分别为高剂量组(HI组)、低剂量组(LO组)和对照组(CON组),每组6只羊。

1.2 试验设计

本研究的动物试验在内蒙古呼和浩特市内蒙古盛乐生物科技有限公司动物基地进行,试验过程中涉及的动物福利与动物试验伦理等内容符合内蒙古自治区农牧业科学院科研处要求,批准号为ZD20232311。
试验用葡聚糖和聚谷氨酸均为市购产品,葡聚糖中β-1,3-1,6-D-葡聚糖含量>50%,聚谷氨酸纯度为25%。试验期间,采用羊用灌胃器经口腔每日固定时间对奶山羊进行灌服处理,HI组每只羊每日灌服3 g葡聚糖+20 g聚谷氨酸,LO组每只羊每日灌服1.5 g葡聚糖+10 g聚谷氨酸,葡聚糖和聚谷氨酸均于当日使用80 mL生理盐水溶解后灌服,所用剂量根据已有文献[10-11]等效剂量及体重换算得出,CON组则灌服等体积的生理盐水,连续灌服42 d(产前21 d,产后21 d)。

1.3 饲养管理

试验动物统一饲养管理,参照《奶山羊饲养管理技术规范》(NY/T 2835—2015)执行。组间隔离,组内混群饲养;羊舍自然通风,设遮蔽棚,各组均配备独立料槽与饮水设施,自由采食与饮水。奶山羊围产期饲粮组成及营养水平见表1,饲粮干物质、粗蛋白质、钙和磷含量分别参照GB/T 6435—2014、GB/T 6432—2018、GB/T 6436—2018和GB/T 6437—2018的方法进行测定,中性洗涤纤维和酸性洗涤纤维含量参照Vogel等[12]和Van Soest等[13]的方法进行测定,消化能依据《中国饲料成分及营养价值表(2020年第31版)》[14]计算得出。
表1 围产期饲粮组成及营养水平(风干基础)

Table 1 Composition and nutrient levels of the periparturient diet (air-dry basis)

项目 Items 含量 Content
原料 Ingredients
全株玉米青贮 Whole plant corn silage 6.00
苜蓿干草 Alfalfa hay 16.00
燕麦草 Oat hay 38.00
玉米 Corn 22.00
豆粕 Soybean meal 10.00
麸皮 Wheat bran 5.50
石粉 Limestone 0.50
小苏打 NaHCO3 0.50
氯化钠 NaCl 0.50
预混料 Premix1) 1.00
合计 Total 100.00
营养水平 Nutrient levels2)
消化能 DE/(MJ/kg) 13.24
干物质 DM 85.68
粗蛋白质 CP 13.33
中性洗涤纤维 NDF 37.20
酸性洗涤纤维 ADF 25.19
钙 Ca 0.62
磷 P 0.33

1)预混料为每千克饲粮提供 The premix provided the following per kg of the diet:VA 3 000 IU,VD 1 250 IU,VE 40 IU,Cu 6.25 mg,Fe 62.5 mg,Zn 62.5 mg,Mn 50 mg,I 0.25 mg,Se 0.125 mg,Co 0.125 mg。

2)消化能为计算值,其余为实测值。DE was a calculated value, while the others were measured values.

1.4 瘤胃液样本采集及前处理

于各组奶山羊产羔后第1天和第21天,采用口腔瘤胃液采样器采集瘤胃液。采集的瘤胃液按不同检测目的,分为以下3部分进行分装与前处理。

1.4.1 瘤胃发酵参数检测样本

取部分新鲜瘤胃液置于干净烧杯中,立即使用testo 206-pH1酸碱度测定仪(Testo公司,德国)测定其pH;另取部分瘤胃液,经4层无菌纱布过滤后,分为2部分进行处理:一部分分装于15 mL预先加入偏磷酸的无菌离心管中(25%偏磷酸3 mL,瘤胃液12 mL),-20 ℃保存,用于测定挥发性脂肪酸(VFA)含量;另一部分分装于不加偏磷酸的15 mL无菌离心管中,-20 ℃保存,用于测定氨态氮和微生物蛋白(MCP)含量。

1.4.2 瘤胃微生物检测样本

取部分新鲜瘤胃液,立即分装于15 mL无菌冻存管中,迅速投入液氮中进行冷冻保存,用于后续瘤胃微生物的检测。其中,产后第1天的CON组、HI组和LO组样本分别命名为CON_F、HI_F和LO_F;产后第21天的CON组、HI组和LO组样本分别命名为CON_S、HI_S和LO_S。

1.4.3 瘤胃代谢组检测样本

取部分新鲜瘤胃液,经4层无菌纱布过滤后分装于1.5 mL无菌离心管中,4 ℃条件下送至实验室,4 ℃、6 000×g离心15 min,取上清液于-20 ℃保存,用于后续瘤胃液代谢组的检测。样本命名同1.4.2。

1.5 指标检测方法与分析

1.5.1 瘤胃发酵参数

瘤胃液VFA含量采用气相色谱法,使用Thermo气相色谱-质谱联用仪(Trace1310-Isq7000,Thermo Fisher Scientific,美国)进行测定;氨态氮含量采用凯氏定氮法,使用凯氏定氮仪(K9840,山东海能科学仪器有限公司)进行测定;MCP含量采用考马斯亮蓝法,使用Agilent 8453紫外分光光度计(Agilent公司,美国)进行测定。

1.5.2 瘤胃微生物

将瘤胃液样本置于干冰中运输至武汉菲沙基因信息有限公司,委托其进行瘤胃微生物16S rRNA基因测序。测序主要步骤包括:采用苯酚-氯仿法提取DNA,使用TransGen AP221-02试剂盒(北京全式金生物技术股份有限公司)完成PCR扩增,在Illumina二代高通量测序平台上构建文库并进行上机测序。下机数据经系列软件处理获得优化序列,具体参数设置为:使用Trimmomatic(v0.63)采用滑动窗口策略(窗口大小50 bp、平均质量值20、最小保留序列长度120 bp)过滤低质量序列;通过Pear(v0.9.6)去除含N的序列;联合Flash(v1.20)与Pear根据PE reads的overlap关系进行序列拼接(最小overlap长度10 bp、错配率0.1);最终经Vsearch(v2.7.1)去嵌合体后得到质控合格的高质量Fasta序列。随后,利用QIIME(v1.8.0)及Vsearch(v2.7.1),采用UPARSE聚类法、Unoise3降噪法并调用“qiime taxa barplot”命令进行瘤胃微生物操作分类单元(OTU)聚类及注释组成分析。基于聚类结果,通过QIIME 2软件调用“qiime diversity alpha-rarefaction”命令进行微生物多样性分析,并借助R语言及对应软件包进行统计与作图;基于注释结果获取各组微生物不同分类水平的信息,利用Mothur软件的Metastats分析进行组间微生物多样性差异分析;通过PICRUSt2软件进行组间差异微生物潜在功能预测。

1.5.3 瘤胃代谢组

将瘤胃液样本置于干冰中运输至武汉菲沙基因信息有限公司,委托其进行瘤胃液非靶代谢组数据分析。采用液相色谱-串联质谱(LC-MS/MS)技术进行代谢物的分离、筛选和鉴定,所用液相色谱仪为Thermo Fisher Scientific公司的Vanquish型号仪器,质谱仪为该公司的Q Exactive HF-X型号仪器。
质谱下机原始数据经ProteoWizard转换为mzML格式后,使用XCMS程序完成峰提取、峰对齐及保留时间校正。对缺失率>50%的峰进行过滤,缺失值按以下规则填补:若某峰缺失率>50%,则使用其峰面积最小值的1/5填充;若缺失率≤50%,则采用K最近邻(KNN)方法填充。随后,采用支持向量回归(SVR)对峰面积进行校正。校正筛选后的峰通过检索实验室自建数据库、整合公共库、预测库及metDNA方法进行代谢物鉴定,最终提取鉴定综合打分≥0.5且质量控制(QC)样本变异系数(CV)<0.3的物质,经正、负模式合并(保留定性等级最高且CV值最小的物质)后,获得可用于后续分析的高质量数据。
高质量数据的统计分析包含单变量统计分析与多变量统计分析:单变量统计分析采用t检验,以P<0.05为差异显著标准;多变量统计分析采用正交偏最小二乘法(OPLS-DA),通过R软件MetaboAnalystR包中的OPLSR.Anal函数实现,以变量重要性投影(VIP)值>1为差异显著标准,进而筛选得到组间差异代谢物。利用KEGG数据库对差异代谢物进行功能注释(http://www.kegg.jp/kegg/compound/)及富集分析(http://www.kegg.jp/kegg/pathway.html)获得组间差异代谢物的功能作用。

1.6 数据统计分析

瘤胃发酵参数数据经Excel 2019软件初步整理计算后,采用SPSS 23.0软件进行单因素方差分析,并利用Duncan氏法进行多重比较。结果用平均值和均值标准误(SEM)表示,以P<0.05为差异显著。

2 结果与分析

2.1 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃发酵参数的影响

由表2可知,产后第1天各组间瘤胃液氨态氮、MCP、乙酸、丙酸、丁酸和总挥发性脂肪酸(TVFA)含量及乙丙比均无显著差异(P>0.05),其中,LO组和HI组瘤胃液丁酸含量有高于CON组的趋势(P=0.057),瘤胃液氨态氮含量有低于CON组的趋势(P=0.073);而瘤胃液pH及戊酸含量在组间存在显著差异(P<0.05),LO组与HI组瘤胃液戊酸含量显著高于CON组(P<0.05)。由表3可知,产后第21天3组之间各瘤胃发酵参数差异均不显著(P>0.05)。
表2 产后第1天奶山羊瘤胃发酵参数

Table 2 Rumen fermentation parameters of dairy goats on day 1 postpartum

项目
Items		 组别 Groups 均值标准误
SEM		 P值
P-value
LO HI CON
pH 6.33b 7.43a 6.90ab 0.197 0.044
氨态氮 NH3-N/(mg/dL) 2.16 2.26 3.10 0.194 0.073
微生物蛋白 MCP/(g/dL) 0.17 0.14 0.19 0.012 0.272
乙酸 Acetic acid/(mmol/L) 4.31 8.17 6.52 0.826 0.160
丙酸 Propionic acid/(mmol/L) 2.73 3.48 1.82 0.365 0.183
乙丙比 Acetic acid/propionic acid 1.77 2.36 3.65 0.376 0.092
戊酸 Valeric acid/(mmol/L) 0.18a 0.21a 0.06b 0.027 0.024
丁酸 Butyric acid/(mmol/L) 1.80 2.15 0.84 0.249 0.057
总挥发性脂肪酸 TVFA/(mmol/L) 9.02 14.01 9.23 1.202 0.159
占总挥发性脂肪酸的摩尔比 Molar ratio of TVFA/%
乙酸 Acetic acid 49.28 58.30 69.47 3.526 0.127
丙酸 Propionic acid 29.15 24.80 20.21 1.815 0.320
戊酸 Valeric acid 1.97 1.47 0.79 0.194 0.074
丁酸 Butyric acid 19.61 15.42 9.52 1.675 0.703

同列数据肩标无字母或相同小写字母表示差异不显著(P>0.05),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)。下表同。

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

表3 产后第21天奶山羊瘤胃发酵参数

Table 3 Rumen fermentation parameters of dairy goats on day 21 postpartum

项目
Items		 组别 Groups 均值标准误
SEM		 P值
P-value
LO HI CON
pH 6.90 6.77 7.13 0.097 0.337
氨态氮 NH3-N/(mg/dL) 5.07 7.20 5.60 0.524 0.246
微生物蛋白 MCP/(g/dL) 0.34 0.31 0.31 0.017 0.827
乙酸 Acetic acid/(mmol/L) 6.07 7.03 6.67 0.279 0.420
丙酸 Propionic acid/(mmol/L) 2.81 3.27 3.45 0.232 0.574
乙丙比 Acetic acid/propionic acid 2.16 2.17 2.05 0.122 0.923
戊酸 Valeric acid/(mmol/L) 0.22 0.18 0.18 0.008 0.130
丁酸 Butyric acid/(mmol/L) 2.16 2.11 2.47 0.088 0.206
总挥发性脂肪酸 TVFA/(mmol/L) 11.25 12.59 12.77 0.459 0.383
占总挥发性脂肪酸的摩尔比 Molar ratio of TVFA/%
乙酸 Acetic acid 53.93 55.69 52.53 1.348 0.216
丙酸 Propionic acid 24.94 26.10 26.55 1.068 0.071
戊酸 Valeric acid 1.92 1.43 1.45 0.092 0.237
丁酸 Butyric acid 19.21 16.77 19.46 0.668 0.238

2.2 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃微生物区系的影响

2.2.1 瘤胃微生物α多样性分析

由图1可知,各组间产后第1天和第21天的瘤胃微生物α多样性分析结果均无显著差异(P>0.05),但产后第21天HI组瘤胃微生物丰富度及Chao1、Shannon、Simpson、Invsimpson、Pielou、ACE、PD_whole_tree指数均高于CON组和LO组。
图1 瘤胃微生物α多样性分析

CON_F、HI_F和LO_F分别表示产后第1天的CON组、HI组和LO组样本,CON_S、HI_S和LO_S分别表示产后第21天的CON组、HI组和LO组样本。下图同。

Fig.1 α diversity analysis of rumen microbiota

CON_F, HI_F and LO_F represented the samples from CON group, HI group and LO group on day 1 postpartum, respectively; CON_S, HI_S and LO_S represented the samples from CON group, HI group and LO group on day 21 postpartum, respectively. The same as below.

2.2.2 瘤胃微生物物种组成分析

对产后第1天和第21天各组瘤胃微生物测序数据进行物种组成分析,各组样本在科水平上相对丰度排名前30的微生物组成如图2所示。结果表明,各组瘤胃微生物科水平物种组成存在差异,其中产后第21天HI组瘤胃普雷沃氏菌科(Prevotellaceae)的相对丰度高于CON组和LO组。
图2 瘤胃微生物科水平组成柱状图

Fig.2 Bar plot of rumen microbiota composition at family level

2.2.3 瘤胃微生物注释聚类分析

为进一步比较各组之间瘤胃微生物的群落组成差异,并分析其物种丰度的分布趋势,本研究对产后第1天和第21天的3组瘤胃微生物样本开展了物种丰度相似性聚类分析,并通过热图(图3)直观展示了微生物注释的聚类结果。结果表明,各组在属水平上的差异微生物主要集中于普雷沃氏菌属(Prevotella),且产后第21天HI组瘤胃微生物中普雷沃氏菌属的富集丰度高于CON组和LO组。
图3 瘤胃微生物属水平注释聚类结果

Fig.3 Clustering results of rumen microbiota annotation at genus level

2.2.4 组间显著差异微生物功能预测

由各组瘤胃微生物注释聚类分析结果可知,丰度差异物种主要集中于普雷沃氏菌属。本研究进一步对各组间显著差异微生物的潜在预测功能进行线性判别分析效应大小(LEfSe)分析。如图4所示,产后第1天HI组中富集程度排名前3的显著差异微生物预测功能为氰基氨基酸代谢(cyanoamino acid metabolism)、其他聚糖降解(other glycan degradation)和硫辛酸代谢(lipoic acid metabolism);产后第21天HI组中富集程度最高的2个显著差异微生物预测功能为RNA聚合酶(RNA polymerase)和不饱和脂肪酸的生物合成(biosynthesis of unsaturated fatty acids)。
图4 瘤胃微生物功能的LEfSe分析

Fig.4 LEfSe analysis of rumen microbial functions

2.2.5 产后第21天HI组与CON组间显著差异微生物功能分析

采用Metastats方法进行组间差异显著性分析,进一步探究产后第21天HI组与CON组间显著差异微生物潜在预测功能。如图5所示,产后第21天HI组与CON组差异微生物在金黄色葡萄球菌感染(Staphylococcus aureus infection)及细胞外基质-受体相互作用(ECM-receptor interaction)功能上表现出显著差异(P<0.05)。
图5 产后第21天HI组与CON组间差异显著微生物功能Metastats分析

Fig.5 Metastats analysis of significantly different microbial functions between HI group and CON group on day 21 postpartum

2.3 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃代谢组的影响

2.3.1 产后第21天HI组与CON组间瘤胃液差异代谢物筛选

产后第21天HI组和CON组间瘤胃液差异代谢物数据统计如表4所示,共有171个差异代谢物,其中73个下调差异代谢物,98个上调差异代谢物。
表4 产后第21天HI组与CON组间瘤胃液差异代谢物数据统计表

Table 4 Statistical table of differential metabolites in rumen fluid between HI group and CON group on day 21 postpartum

项目
Item		 差异代谢物
Differential
metabolites		 下调差异代谢物
Down-regulated differential
metabolites		 上调差异代谢物
Up-regulated differential
metabolites
HI组vs. CON组 HI group vs. CON group 171 73 98
产后第21天HI组与CON组间|log2[差异倍数(FC)]|排名前20的瘤胃液差异代谢物如图6所示。其中,HI组较CON组显著上调的瘤胃液差异代谢物包括4,4'-二氨基二丁胺(4,4'-diaminodibutylamine)、有机酸及其衍生物分类的吡哆胺-5'-磷酸(pyridoxamine-5'-phosphate)和氨基酸及其代谢物分类的L-甲硫氨酸亚砜(L-methionine sulfoxide)等,显著下调且|log2(FC)|排名前3的瘤胃液差异代谢物分别为苯及其衍生物类的4-(3-甲基丁氧基)苯胺盐酸盐[4-(3-methylbutoxy) aniline hydrochloride]、反式-2-己烯醛二甲基缩醛(trans-2-hexenal dimethyl acetal)及氨基酸及其代谢物色氨酰异亮氨酸(Trp-Ile)。
图6 产后第21天HI组与CON组间|log2(FC)|排名前20的瘤胃液差异代谢物

红色代表HI组相较于CON组显著上调的差异代谢物,绿色代表HI组相较于CON组显著下调的差异代谢物。

Fig.6 Top 20 differential metabolites in rumen fluid ranked by |log2(FC)| between HI group and CON group on day 21 postpartum

Red represented the significantly up-regulated differential metabolites in the HI group compared with the CON group, while green represented the significantly down-regulated differential metabolites in the HI group compared with the CON group.

2.3.2 产后第21天HI组与CON间瘤胃液差异代谢通路分类

产后第21天HI组与CON组间瘤胃液差异代谢物的通路分类注释结果如图7所示。2组间差异代谢物富集的主要通路为代谢通路(metabolic pathway),该通路共注释到21个差异代谢物,占被注释到的差异代谢物总数的80.77%。
图7 产后第21天HI组与CON组间瘤胃液差异代谢物的KEGG通路分类

通路右侧数值依次为注释到的差异代谢物个数及其占被注释到的差异代谢物总数的百分比。

Fig.7 KEGG pathway classification of differential metabolites in rumen fluid between the HI group and CON group on day 21 postpartum

Values to the right of each pathway represented the number of annotated differential metabolites and their percentage of total number of annotated differential metabolites, respectively.

2.3.3 产后第21天HI组与CON间瘤胃液差异代谢物富集分析及通路变化情况

产后第21天HI组与CON组间的瘤胃液差异代谢物富集分析及通路整体变化分析如图8所示。HI组与CON组间差异显著性最高的代谢通路为半胱氨酸和蛋氨酸代谢(cysteine and methionine metabolism),但HI组该通路整体代谢物丰度较CON组无变化。差异显著性次之的代谢通路为炎症介质对TRP通道的调控(inflammatory mediator regulation of TRP channels),HI组该通路整体代谢物丰度较CON组下调。
图8 产后第21天HI组与CON组间瘤胃液差异代谢通路整体变化分析

纵坐标为差异代谢通路名称(按照P值排序),横坐标为差异丰度得分(DA score)。DA score反映代谢途径中所有代谢物的整体变化趋势,得分为1表示该通路中所有鉴定到的代谢物呈上调趋势,得分为-1表示该通路中所有鉴定到的代谢物呈下调趋势。线段的长度表示DA score的绝对值,线段端点的圆点大小表示该通路中差异代谢物的个数,圆点分布在中轴左侧且线段越长,表示该通路整体变化趋势越倾向于下调,圆点分布在中轴右侧且线段越长,表示该通路整体变化趋势越倾向于上调,圆点越大表示代谢物数量越多。线段和圆点颜色反映P值大小,越接近红色表示P值越小,越接近紫色表示P值越大。

Fig.8 Overall variation analysis of differential metabolic pathways in rumen fluid between HI group and CON group on day 21 postpartum

The vertical axis displayed the names of differential pathways (sorted by P-value), while the horizontal axis displayed the differential abundance score (DA Score). The DA score reflected the overall change of all metabolites in a metabolic pathway. A score of 1 indicated that all identified metabolites in the pathway showed an up-regulation trend, while a score of -1 indicated that all identified metabolites in the pathway showed a down-regulation trend. The length of the line segment represented the absolute value of the DA score, and the size of the dot at the end of the segment represented the number of differential metabolites in the corresponding pathway. Dots distributed on the left side of the central axis with longer line segments indicated a stronger overall down-regulation trend of the pathway, whereas dots distributed on the right side of the central axis with longer line segments indicated a stronger overall up-regulation trend of the pathway. Larger dots indicated a greater number of metabolites. The colors of the line segments and dots reflected the magnitude of the P-value. Colors closer to red indicated smaller P-value, while colors closer to purple indicated larger P-value.

3 讨论

3.1 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃发酵参数的影响

瘤胃发酵参数是反映瘤胃内环境稳态的直接指标,也是体现瘤胃微生物发酵性能的关键指标,可作为评价反刍动物营养吸收及瘤胃健康的重要依据。瘤胃pH以及VFA、氨态氮和MCP含量是其中的核心检测指标[15-16]。其中,pH能够综合反映瘤胃发酵过程,并受发酵底物与产物的共同影响,在发酵过程中pH通常于6.0~7.5内波动[17]。瘤胃微生物通过发酵作用产生的VFA与MCP是反刍动物体内重要的能量与蛋白质来源[18]。VFA主要包括乙酸、丙酸和丁酸,乙酸和丁酸是合成乳脂中脂肪酸的重要原料,其中丁酸主要以β-羟基丁酸形式参与物质代谢,乳脂中碳链长度十四碳以下的脂肪酸及部分十六碳脂肪酸均由乙酸和β-羟基丁酸合成[19-20]。氨态氮是维持瘤胃内环境稳定的重要指标,适宜的氨态氮含量有利于瘤胃微生物的生长,可提高微生物的消化效率[21]。
本试验中,各组奶山羊的瘤胃液pH均处于正常生理范围内。产后第1天的检测结果显示,HI组和LO组瘤胃液戊酸含量显著高于CON组,丁酸含量有高于CON组的趋势;而瘤胃液氨态氮含量则呈现出HI组和LO组低于CON组的趋势。产后第21天的检测结果显示,3组之间各瘤胃发酵参数均无显著差异。Pinloche等[22]对荷斯坦奶牛饲喂不同剂量的酵母补充剂(含β-葡聚糖)后,发现瘤胃液氨态氮含量显著降低,TVFA、丙酸和丁酸含量升高。杨云天[23]对关中奶山羊持续饲喂酿酒酵母(含β-葡聚糖),结果也显示瘤胃液氨态氮含量显著降低,丁酸含量显著升高,改善了奶山羊瘤胃饲粮蛋白质利用效率,生长性能亦有所提升。李耀光等[24]研究表明,在肉牛饲粮中添加浒苔多糖后,其瘤胃液中MCP、TVFA及丙酸含量均大幅提高。曹琪娜等[11]研究饲粮中添加聚谷氨酸对小尾寒羊瘤胃发酵及菌群结构的影响,结果显示添加20 g/(只·d)聚谷氨酸可提高瘤胃液乙酸和氨态氮含量,并能增加瘤胃微生物多样性,提高普雷沃氏菌属的相对丰度。本试验结果表明,灌服葡聚糖与聚谷氨酸对围产期奶山羊瘤胃发酵未产生负面影响,且可能促进了瘤胃微生物对氨态氮的利用,提高了氮转化效率,同时增加了瘤胃液戊酸与丁酸的含量,在一定程度上增强了围产期奶山羊的瘤胃发酵功能。

3.2 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃微生物区系的影响

反刍动物瘤胃内栖息着复杂多样的微生物群落,涵盖细菌、真菌、古细菌及原生生物等类群。瘤胃微生物群落与瘤胃内环境共同构成一个高效精密的发酵系统,可通过微生物发酵作用分解植物纤维素、半纤维素等碳水化合物,并将其转化为VFA,为反刍动物机体提供营养物质[25-27]。因此,瘤胃是反刍动物至关重要的消化器官[28-29]。研究表明,瘤胃微生物的区系组成及多样性与瘤胃健康状况直接相关,并进一步影响反刍动物的营养消化与吸收功能[30]。
本试验瘤胃微生物多样性分析结果显示,产后第21天HI组瘤胃微生物α多样性指数中,除Goods_coverage指数外,其余指标均高于LO组和CON组,但组间差异未达到显著水平。α多样性可用于评价微生物群落的物种组成多样性与丰富度[31]。相关研究证实,瘤胃微生物多样性是影响反刍动物生产性能与饲料利用效率的重要因素[32-33]。本试验结果说明灌服葡聚糖与聚谷氨酸可在一定程度上提高产后奶山羊瘤胃微生物群落的丰度和多样性,进而有助于增强瘤胃发酵功能。
本研究发现,围产期奶山羊灌服葡聚糖与聚谷氨酸后,其瘤胃微生物的变化主要集中于普雷沃氏菌。产后第21天HI组瘤胃微生物中普雷沃氏菌科的相对丰度显著高于LO组与CON组;且在属水平上,该组普雷沃氏菌属的富集程度同样高于其他2组。已有研究证实,拟杆菌门中的普雷沃氏菌属是瘤胃细菌群落的优势菌属[34],其对反刍动物的营养消化具有至关重要的作用[35]。该菌属可促进饲粮中蛋白质与碳水化合物的分解,进而转化为VFA为反刍动物供能[36-37],且其丰度与饲料利用效率呈正相关[38]。由此可见,围产期奶山羊灌服葡聚糖与聚谷氨酸可提高瘤胃关键功能菌群——普雷沃氏菌属的相对丰度,从而增强瘤胃的消化吸收能力[39-40]。
本研究通过对3组间丰度差异显著的微生物进行功能预测,发现产后第21天HI组中富集程度最高的2个差异显著微生物功能为RNA聚合酶和不饱和脂肪酸的生物合成。研究表明,RNA聚合酶的表达水平能够反映微生物群落整体代谢活性,是微生物生长代谢的关键指标[41],RNA聚合酶高丰度表达说明灌服葡聚糖与聚谷氨酸可能增强了奶山羊瘤胃微生物的代谢活动[42]。而不饱和脂肪酸的生物合成功能的高丰度,则提示灌服葡聚糖与聚谷氨酸可能提高了瘤胃微生物为宿主分解供能的速率[43],这与普雷沃氏菌属高丰度表达可提高瘤胃消化效率的作用相符[44]。因此,基于差异微生物的功能筛选结果可以推断,灌服葡聚糖与聚谷氨酸能够增加瘤胃普雷沃氏菌的占比并提升其代谢活性,从而促进围产期奶山羊瘤胃菌群的生长与代谢,对提高瘤胃功能及营养物质消化率具有积极作用。
本研究通过比较产后第21天HI组与CON组之间瘤胃差异微生物的预测生物功能,发现HI组较CON组在金黄色葡萄球菌感染功能上表现为显著下调,在细胞外基质-受体相互作用功能上表现为显著上调。研究表明,细胞外基质-受体相互作用与瘤胃真核生物增殖呈正相关[45],说明灌服葡聚糖与聚谷氨酸有助于促进围产期奶山羊瘤胃真核生物增殖,进而改善瘤胃营养代谢效率。而金黄色葡萄球菌感染相关功能与瘤胃微生物竞争性繁殖密切相关[46],这进一步提示该营养调控方式可通过调控瘤胃微生物区系的代谢功能特征,间接保障真核生物增殖的微生态环境。但鉴于瘤胃微生物区系存在复杂的网络调控结构,微生物各功能通路间亦呈现多维度的交联关系,因此葡聚糖与聚谷氨酸对瘤胃微生物功能的具体调控机制,仍需后续深入研究阐明。

3.3 葡聚糖与聚谷氨酸对围产期奶山羊瘤胃代谢组的影响

健康的瘤胃微生物区系维持在一个动态平衡的稳定状态,其代谢活动也随之处于稳定平衡之中,因此瘤胃微生物代谢状态可间接反映微生物区系的健康程度[47]。瘤胃液代谢组学是通过代谢检测技术手段,对瘤胃液内小分子化合物进行定性与定量的研究[48]。越来越多的研究表明,代谢组分析在动物健康评估、疾病诊断以及新型饲粮营养成分定型方面具有筛选生物标志物的重要作用[49-50]。研究发现,瘤胃中特定的差异代谢物及相关代谢通路与动物的生产性能密切相关[51-52]。通过筛选瘤胃代谢标志物并开展代谢组检测,能够反映瘤胃健康状况与消化效率,进而评估动物机体生理状态,为饲粮水平及营养物质作用效果的判定提供依据[53]。
本研究对产后第21天HI组与CON组瘤胃液差异代谢物的筛选结果显示,HI组较CON组显著上调的差异代谢物包括杂环化合物分类的4,4-二氨基二丁胺(又称对称-高亚精胺)、吡哆胺-5'-磷酸和L-甲硫氨酸亚砜等。其中,对称-高亚精胺多存在于具有固氮能力的细菌中,其丰度与瘤胃氮转化效率呈正相关[54];吡哆胺-5'-磷酸可作为评估生物体内核黄素状态的标志物[55];L-甲硫氨酸亚砜则是甲硫氨酸的氧化产物[56]。多胺类化合物、有机酸及氨基酸衍生物等代谢物的增加,是瘤胃营养代谢功能增强的表现[57]。HI组较CON组显著下调且|log2(FC)|排名前3的差异代谢物分别为苯及其衍生物类的4-(3-甲基丁氧基)苯胺盐酸盐、反式-2-己烯醛二甲基缩醛及氨基酸及其代谢物色氨酰异亮氨酸。苯及其衍生物对瘤胃微生物具有一定的潜在毒性,是瘤胃微生物异常代谢产生的中间代谢产物[58],其丰度下调同样表明瘤胃营养代谢功能的改善;而色氨酰异亮氨酸丰度的下调,则提示瘤胃中以其为代谢底物的梭菌属(Clostridium)、普雷沃氏菌属和丁酸弧菌属(Butyrivibrio)代谢活动较为旺盛[59]。综上所述,本研究为围产期奶山羊灌服葡聚糖与聚谷氨酸,可提高瘤胃氮转化效率,增加维生素及甲硫氨酸等相关营养代谢物的丰度,下调苯胺盐酸盐类异常代谢物丰度,并促进瘤胃梭菌属、普雷沃氏菌属和丁酸弧菌属的代谢活动,表明聚谷氨酸与葡聚糖对围产期奶山羊瘤胃营养代谢具有积极作用。
本研究对产后第21天HI组与CON组瘤胃液差异代谢物的富集分析及通路变化分析结果表明,HI组与CON组间差异显著性最高的代谢通路为半胱氨酸和蛋氨酸代谢,但HI组该通路代谢物丰度较CON组无变化。研究表明,该通路与含硫氨基酸的生物合成密切相关,而含硫氨基酸在机体内发挥多种调节作用[60],并对糖代谢具有促进作用[61-62]。HI组与CON组间差异显著性次之的代谢通路为炎症介质对TRP通道的调控,HI组该通路代谢物丰度较CON组下调。炎症介质对TRP通道的调控通常由瘤胃环境失衡、释放炎症介质并激活免疫系统所引发,是瘤胃病理状态被机体感知的调控机制之一,该代谢通路的下调,说明HI组的瘤胃营养代谢功能优于CON组,瘤胃微生物代谢系统更为健康[63]。

4 结论

灌服葡聚糖与聚谷氨酸对围产期奶山羊瘤胃发酵功能未产生负面影响,且能够促进瘤胃氨态氮消化利用,提高氮转化效率和VFA含量,从而有助于瘤胃发酵供能;同时,该处理提高了奶山羊瘤胃中普雷沃氏菌的占比和丰度。此外,灌服葡聚糖与聚谷氨酸还上调了奶山羊瘤胃中供能营养代谢物的丰度及氨基酸代谢通路,同时下调了苯及其衍生物等异常代谢产物丰度以及炎症激活通路。综上可知,葡聚糖与聚谷氨酸对围产期奶山羊的瘤胃健康及营养代谢具有积极作用,可作为奶山羊围产期营养调控剂开展进一步研发与利用。

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