Chinese Journal of Animal Nutrition >

2024 , Vol. 36 >Issue 9: 5566 - 5580

DOI: https://doi.org/10.12418/CJAN2024.475

RESEARCH PAPER

Effects of Kelp Enzymatic Hydrolysate on Growth Performance, Intestinal Morphology and Microbiota Composition of Weaned Piglets

  • QU Yuankai , 1 ,
  • LI Mingtan 1 ,
  • ZANG Jianjun , 2, *
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  • 1 Shandong Shidai Marine Biological Technology Co., Ltd., Weihai 264319, China
  • 2 College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
* professor, E-mail:

Received date: 2024-03-28

  Online published: 2024-09-08

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Abstract

This study was conducted to investigate the effects of kelp hydrolysate on growth performance, intestinal morphology and microbiota composition of weaned piglets. A total of 230 Duroc×Landrace×Yorkshire weaned piglets at 28 days of age with body weight of (8.44±1.50) kg were randomly divided into 5 groups: antibiotic free control group (basic diet), antibiotic group (basic diet+50 mg/kg kelp enzymatic hydrolysate), low level kelp enzymatic hydrolysate group [basic diet+25 g/(head·d) kelp enzymatic hydrolysate], medium level kelp enzymatic hydrolysate group [basic diet+50 g/(head·d) kelp enzymatic hydrolysate], and high level kelp enzymatic hydrolysate group [basic diet+75 g/(head·d) kelp enzymatic hydrolysate]. Each group had 6 replications (5 replications with 8 pigs per pen, and 1 repetition with 6 pigs). The experimental period lasted for 28 days. The results were as follows: 1) there was a significant difference in feed/gain (F/G) of weaned piglets among different groups (P=0.09), and the F/G of high level kelp enzymatic hydrolysate group was the lowest. 2) Compared with the antibiotic free control group, the jejum crypt depth of weaned piglets in the high level kelp enzymatic hydrolysate group was significantly decreased (P<0.01), but there was no significantly difference compared with antibiotic group (P>0.05). The villus height in ileum of weaned piglets in the high level kelp enzymatic hydrolysate group was significantly higher than that in antibiotic free control group and antibiotic group (P<0.01); compared with the antibiotic free group and antibiotic group, the villus height and crypt depth of jejunum and ileum of weaned piglets were significantly increased in the high level kelp enzymatic hydrolysate group (P<0.01). 3) There was no significant difference in volatile fatty acid (VFA) content in cecum and colon of weaned piglets under different treatments (P>0.05). 4) The composition and abundance of microorganisms in the ileum of weaned piglets in the high level kelp enzymatic hydrolysate group were similar to those in the antibiotic group, and the dominant bacteria in both groups were Streptococcus, indicating that the kelp enzymatic hydrolysate had similar regulatory effects on ileal microbiota and antibiotics. In conclusion, kelp enzymatic hydrolysate supplementation [75 g/(head·d)] can improve intestinal morphology and regulate intestinal microbial composition in weaned piglets.

Key words： kelp enzymatic hydrolysate; weaned piglets; growth performance; intestinal morphology; intestinal microbial composition

Cite this article

QU Yuankai , LI Mingtan , ZANG Jianjun . Effects of Kelp Enzymatic Hydrolysate on Growth Performance, Intestinal Morphology and Microbiota Composition of Weaned Piglets[J]. Chinese Journal of Animal Nutrition, 2024 , 36(9) : 5566 -5580 . DOI: 10.12418/CJAN2024.475

断奶仔猪的生长性能与健康状况对养猪企业的生产水平影响很大。断奶应激会造成诸如生长速度变缓、饲料利用率低下、胃肠功能不完善等问题,结果导致腹泻和免疫功能下降[1⇓-3],严重时甚至可引起仔猪死亡[4-5],最终影响养殖效益。因此,在饲料中全面禁止添加抗生素促生长剂的背景下,通过营养调控技术改善断奶仔猪的健康状况、通过改善断奶仔猪的肠道微生物组成进而提高断奶仔猪的生长性能成为猪饲料与营养研究的热点[6]。
由于在饲粮中添加天然植物提取物具有安全、无残留,且能提高饲料利用效率等优点[7],更适宜作为抗生素替代品添加至断奶仔猪饲粮中。海带是我国最大的养殖海藻品种,2020年我国海带年产量已达165×104 t[8],另外,海带也是生产海藻酸钠和海带提取物主要原料之一[9]。海带酶解液是新鲜海带经生物酶法酶解的产物,其中纤维被转化为各种糖类,蛋白质被降解成小分子的肽和氨基酸,具有丰富的营养成分和生物活性物质[10⇓-12]。有研究表明,海带酶解液中的海藻多糖和海藻寡糖对鱼类和反刍动物等具有促进生长、改善肠道形态结构和加强肝脏的糖、脂代谢能力等作用[13-14]。在生长育肥猪饲粮中添加海带酶解物通过降低料重比(F/G)和增加平均日增重(ADG)从而提高生产性能[15],但断奶仔猪饲粮中添加海带酶解液的功效研究鲜有报道。因此,本研究旨在探究海带酶解液对断奶仔猪生长性能、肠道形态和微生物组成的影响,为缓解断奶应激反应、促进断奶仔猪的生长和改善健康提供新的解决方案。

1 材料与方法

1.1 试验设计

选取230头初始体重[(8.44±1.50) kg]接近且健康的杜×长×大三元杂交断奶仔猪,随机分为5个组,分别为无抗对照组(基础饲粮)、抗生素组(基础饲粮+50 mg/kg金霉素)、低剂量海带酶解液组[基础饲粮+25 g/(头·d)海带酶解液]、中剂量海带酶解液组[基础饲粮+50 g/(头·d)海带酶解液]和高剂量海带酶解液组[基础饲粮+75 g/(头·d)海带酶解液],每组6个重复(5个重复每栏8头猪,1个重复6头猪)。每天饲喂前将海带酶解液与基础饲粮均匀混合,即混即用。各组饲粮能量与营养水平保持一致,均满足NRC(2012)[16]推荐标准,基础饲粮组成及营养水平见表1。动物饲养试验在位于河北省承德市丰宁满族自治县的国家饲料工程技术研究中心(农业农村部饲料工业中心)动物试验基地进行。动物福利与动物试验伦理批准文号:AW42604202-1-1。
表1 基础饲粮组成及营养水平(饲喂基础)

Table 1 Composition and nutrient levels of basal diets (as-fed basis) %

项目Items 第1~14天Days 1 to 14 第15~28天Days 15 to 28
原料Ingredients
玉米Corn 59.82 64.39
豆粕Soybean meal 15.00 15.80
膨化全脂大豆Extruded full-fat soybean 6.30 6.00
乳清粉Whey powder 4.00 3.15
鱼粉Fish meal 4.00 3.50
大豆浓缩蛋白Soy protein concentrate 4.80 2.80
豆油Soybean oil 2.20 1.12
磷酸氢钙CaHPO4 1.15 1.00
石粉Limestone 0.82 0.60
食盐NaCl 0.30 0.30
L-赖氨酸L-Lys 0.52 0.44
DL-蛋氨酸DL-Met 0.18 0.13
苏氨酸Thr 0.18 0.14
色氨酸Trp 0.03 0.03
氯化胆碱Choline chloride 0.20 0.10
预混剂Premix1) 0.50 0.50
合计Total 100.00 100.00
营养水平Nutrient levels2)
消化能DE/(MJ/kg) 14.86 14.64
粗蛋白质CP 21.11 20.47
钙Ca 0.90 0.77
总磷TP 0.67 0.63
赖氨酸Lys 1.55 1.42
蛋氨酸Met 0.57 0.46

1)预混料为每千克饲粮提供The premix provided the following per kg of diets: VA 12 000 IU,VD3 2 500 IU,VE 30 IU,VK3 3.0 mg,VB12 0.012 mg,核黄素 riboflavin 4.0 mg,D-泛酸D-pantothenic acid 15.0 mg,烟酸 nicotinic acid 30.0 mg,叶酸 folic acid 0.7 mg,VB1 1.5 mg,VB6 3 mg,Mg 40.0 mg,Fe 75.0 mg,Zn 75.0 mg,Cu 100.0 mg,I 0.3 mg,Se 0.3 mg。

2)消化能为计算值[17],其余均为实测值。DE was a calculated value[17], while the others were measured values。

1.2 试验材料

海带酶解液是由整棵鲜海带经过复合酶(纤维素酶、蛋白酶、果胶酶、褐藻胶裂解酶等)低温生物酶解制备而成。试验用海带酶解液产品(干物质含量6%)主要成分为:海藻寡糖21 g/L,海藻多糖14 g/L,海藻酸9 g/L,有机质22 g/L。

1.3 饲粮营养成分测定

从每组饲粮中各取50 g样品后,按照四分法再次取样后放于密封袋中,于-4 ℃冷库保存,在检测样品前使用高速粉碎机粉碎,过40目筛后于密封袋中保存待测。不同组饲粮的粗蛋白质、氨基酸、钙和总磷含量分别按照GB/T 6432—2018、GB/T 18246—2019、GB/T 6436—2018和GB/T 6437—2018方法[18⇓⇓-21]进行测定。

1.4 检测指标

1.4.1 生长性能

分别在试验开始前1天和试验第28天对每头试验仔猪空腹称重,并以重复为单位计算平均日采食量(ADFI)、ADG和F/G。

1.4.2 腹泻频率

在试验期内的每天15:00左右察看每栏猪腹泻情况并记录,栏内连续2 d发生腹泻记入腹泻天数。腹泻频率计算公式如下:
腹泻频率(%)=试验期腹泻仔猪头次数/(试验仔猪头数×试验天数)×100。

1.4.3 血清免疫指标

试验结束时,在每个重复选取接近平均体重的1头仔猪进行前腔静脉采血10 mL,真空采血管中在室温静置30 min后,3 500×g离心15 min,分离血清,保存于-20 ℃下,用于血清免疫指标的测定。使用日立7600全自动生化仪对血清样品中免疫球蛋白G(IgG)、免疫球蛋白A(IgA)和免疫球蛋白M(IgM)含量进行测定。

1.4.4 肠道形态

试验结束时,从无抗对照组、抗生素组、高剂量海带酶解液组(ADG最大的组)中各挑选3头最接近该栏平均体重的仔猪屠宰。取每头屠宰仔猪的十二指肠、空肠、回肠肠段各约3 cm用缓冲液冲洗干净置于50 mL离心管中,用4%多聚甲醛将肠道组织于常温下充分固定,做常规石蜡切片,苏木精-伊红(HE)染色,中性树胶封片。观察并测定绒毛高度(VH)和隐窝深度(CD),计算绒毛高度/隐窝深度(V/C)。

1.4.5 肠道挥发性脂肪酸(VFA)含量

试验结束屠宰取肠段样品的同时,收集盲肠和结肠肠段食糜于冻存管,放入液氮速冻后转入-80 ℃冰箱保存,用于测定VFA含量。无菌称取样品0.5 g左右于离心管中,加入200 μL的VFA内标液与4 mL 1% HCl-5%甲酸溶液,涡旋10 s,40 kHz下超声10 min,8 000×g下离心5 min,上清液于50 000×g下离心10 min,将上清液使用0.45 μm滤膜过滤(Millipore,美国),注入气相色谱(Agilent HP 6890 series,美国)检测肠道食糜中VFA的含量。

1.4.6 肠道微生物组成

屠宰取样时,另取1份回肠、盲肠、结肠肠段食糜于冻存管,放入液氮速冻,用于肠道16S rRNA微生物多样性分析。16S rRNA微生物多样性分析中,测序和分析工作委托上海美吉生物医药科技有限公司完成。具体步骤如下:使用DNA试剂盒(Omega Bio-tek,美国)提取样品中细菌的总DNA,利用NanoDrop2000检测DNA浓度和纯度。根据细菌通用引物338F (5'-ACTCCTACGGGAGGCAGCAG-3')和806R (5'-GGACTACHVGGGTWTCTAAT-3'),扩增细菌16S rRNA的V3~V4区。参照电泳结果,用Promega公司的QuantiFluorTM-ST蓝色荧光定量系统将PCR产物进行检测定量。采用MiSeq平台测序并使用Usearch平台进行操作分类单元(OTU)聚类分析和物种分类学分析。本试验中使用的比对数据库为Silva(Release132 http://www.arb-silva.de)。根据97%的相似度对序列进行OTU聚类,分析肠道微生物组成。

1.5 数据统计分析

试验数据采用R i386 3.6.1以及SPSS 20.0软件进行统计分析,数据进行one-way ANOVA分析,腹泻频率数据进行非参数检验(Kruskal-Wallis Test),所有指标以每个重复为单位。若组间差异显著,则用Duncan氏法进行多重比较。统计结果用平均值±标准误(mean±SEM)表示,P<0.01为差异极显著,P<0.05为差异显著,0.05≤P<0.10为有差异显著的趋势。
基于上海美吉生物医药科技有限公司开发的美吉云平台(www.majorbio.com)完成肠道微生物相关的生信分析。

2 结果与分析

2.1 海带酶解液对断奶仔猪生长性能的影响

如表2所示,试验全期各组断奶仔猪ADG、ADFI均无显著差异(P>0.05)。不同组间F/G有差异显著的趋势(P=0.09),其中高剂量海带酶解液组的F/G最低。
表2 海带酶解液对断奶仔猪生长性能的影响

Table 2 Effects of kelp enzymatic hydrolysate on growth performance of weaned piglets

项目
Items		 无抗对照组
Antibiotic
free control
group		 抗生素组
Antibiotic
group		 低剂量海带
酶解液组
Low level kelp
enzymatic
hydrolysate
group		 中剂量海带
酶解液组
Medium level
kelp enzymatic
hydrolysate
group		 高剂量海带
酶解液组
High level kelp
enzymatic
hydrolysate
group		 P值
P-value
初始体重IBW/kg 8.29±1.38 8.53±1.62 8.46±1.56 8.42±1.53 8.44±1.54 0.99
终末体重FBW/kg 20.90±3.20 20.48±2.95 20.71±3.04 21.27±3.04 21.98±1.92 0.94
平均日采食量ADFI/g 706.2±46.3 746.2±35.5 734.1±49.0 742.7±52.0 710.5±21.1 0.78
平均日增重ADG/g 431.8±23.1 439.9±24.2 437.5±33.9 452.2±30.2 457.8±20.1 0.30
料重比F/G 1.64±0.06 1.70±0.04 1.69±0.04 1.64±0.03 1.56±0.05 0.09

同行数据肩标无字母或相同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 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 significant difference (P<0.01). The same as below.

2.2 海带酶解液对断奶仔猪腹泻频率的影响

如表3所示,不同组间断奶仔猪腹泻频率无显著差异(P>0.05),各组断奶仔猪的腹泻频率均不高。
表3 海带酶解液对断奶仔猪腹泻频率的影响

Table 3 Effects of kelp enzymatic hydrolysate on diarrhea rate of weaned piglets %

项目
Item		 无抗对照组
Antibiotic
free control
group		 抗生素组
Antibiotic
group		 低剂量海带
酶解液组
Low level kelp
enzymatic
hydrolysate
group		 中剂量海带
酶解液组
Medium level
kelp enzymatic
hydrolysate
group		 高剂量海带
酶解液组
High level kelp
enzymatic
hydrolysate
group		 P值
P-value
腹泻频率Diarrhea rate 2.71±0.53 3.77±0.85 3.41±0.78 4.60±0.87 3.93±0.72 0.50

2.3 海带酶解液对断奶仔猪血清免疫球蛋白含量的影响

如表4所示,各组间断奶仔猪血清免疫球蛋白(IgG、IgA、IgM)含量差异不显著(P>0.05)。
表4 海带酶解液对断奶仔猪血清免疫球蛋白含量的影响

Table 4 Effects of kelp enzymatic hydrolysate on serum immune globulin contents of weaned pigletsg/L

项目
Items		 无抗对照组
Antibiotic
free control
group		 抗生素组
Antibiotic
group		 低剂量海带
酶解液组
Low level kelp
enzymatic
hydrolysate
group		 中剂量海带
酶解液组
Medium level
kelp enzymatic
hydrolysate
group		 高剂量海带
酶解液组
High level kelp
enzymatic
hydrolysate
group		 P值
P-value
免疫球蛋白G IgG 6.30±0.26 6.38±0.20 6.06±0.38 5.91±0.46 6.83±0.41 0.45
免疫球蛋白A IgA 0.99±0.07 1.02±0.10 1.16±0.12 1.04±0.08 1.29±0.16 0.30
免疫球蛋白M IgM 0.72±0.03 0.85±0.13 0.92±0.12 0.78±0.54 0.96±0.11 0.39

2.4 海带酶解液对断奶仔猪肠道形态的影响

如表5所示,各组间十二指肠CD有差异显著的趋势(P=0.07),其中高剂量海带组断奶仔猪十二指肠CD最浅。与无抗对照组相比,高剂量海带酶解液组断奶仔猪空肠CD极显著降低(P<0.01)。高剂量海带酶解液组断奶仔猪空肠V/C较无抗对照组和抗生素组极显著提高(P<0.01)。高剂量海带酶解液组断奶仔猪回肠VH较无抗对照组和抗生素组均极显著提高(P<0.01),无抗对照组较抗生素组也有极显著的提高作用(P<0.01)。与无抗对照组及抗生素组相比,高剂量海带酶解液组断奶仔猪回肠V/C极显著提高(P<0.01)。
表5 海带酶解液对断奶仔猪肠道形态的影响

Table 5 Effects of kelp enzymatic hydrolysate on intestinal morphology of weaned piglets

项目
Items		 无抗对照组
Antibiotic free
control group		 抗生素组
Antibiotic group		 高剂量海带酶解液组
High level kelp enzymatic
hydrolysate group		 P值
P-value
十二指肠Duodenum
绒毛高度Villus height/μm 232.61±22.74 265.27±17.22 214.51±11.25 0.10
隐窝深度Crypt depth/μm 62.10±3.77 83.87±4.43 75.94±7.66 0.07
绒毛高度/隐窝深度V/C 3.88±0.51 3.32±0.27 3.41±0.60 0.71
空肠Jejunum
绒毛高度Villus height/μm 173.65±7.58 177.90±7.00 172.25±7.82 0.87
隐窝深度Crypt depth/μm 98.22±6.92Bc 78.42±3.61Ab 61.51±3.58Aa <0.01
绒毛高度/隐窝深度V/C 2.17±0.16Aa 2.40±0.10Aa 3.03±0.10Bb <0.01
回肠Ileum
绒毛高度Villus height/μm 176.63±5.21Bb 142.01±6.40Aa 197.99±6.83Bc <0.01
隐窝深度Crypt depth/μm 68.79±2.77 64.98±2.29 66.19±2.81 0.72
绒毛高度/隐窝深度V/C 2.74±0.10Bb 2.24±0.10Aa 3.14±0.15Bc <0.01

2.5 海带酶解液对断奶仔猪肠道VFA含量的影响

如表6所示,与无抗对照组和抗生素组相比,高剂量海带酶解液组仔猪盲肠、结肠中的VFA含量没有显著差异(P>0.05)。
表6 海带酶解液对断奶仔猪肠道VFA含量的影响

Table 6 Effects of kelp enzymatic hydrolysate on intestine VFA contents of weaned pigletsμg/g

项目
Items		 无抗对照组
Antibiotic free
control group		 抗生素组
Antibiotic group		 高剂量海带酶解液组
High level kelp enzymatic
hydrolysate group		 P值
P-value
盲肠Cecum
乙酸Acetic acid 4 216.00±309.50 4 344.00±301.90 4 782.00±162.10 0.49
丙酸Propionic acid 2 548.00±300.00 2 749.00±178.30 2 984.00±89.20 0.27
异丁酸Isobutyric acid 37.10±13.56 26.20±10.09 31.40±5.78 0.77
丁酸Butyric acid 1 012.00±335.10 1 342.00±382.00 1 252.00±136.20 0.74
异戊酸Isovaleric acid 68.90±27.88 49.40±18.99 59.80±11.62 0.81
戊酸Valeric acid 202.20±83.16 138.70±44.49 130.70±17.69 0.63
总挥发性脂肪酸Total VFA 8 083.00±792.90 8 649.00±738.30 9 240.00±234.20 0.49
结肠Colon
乙酸Acetic acid 3 770.00±476.30 4 172.00±489.00 4 288.00±270.00 0.23
丙酸Propionic acid 2 234.00±334.80 2 354.00±184.70 2 888.00±233.00 0.24
异丁酸Isobutyric acid 98.50±20.95 76.50±5.83 85.00±2.30 0.50
丁酸Butyric acid 1 016.00±238.10 1 330.00±289.30 1 401.00±203.90 0.54
异戊酸Isovaleric acid 178.30±45.80 128.30±18.40 130.20±11.80 0.44
戊酸Valeric acid 248.50±87.00 219.90±38.10 216.20±3.55 0.90
总挥发性脂肪酸Total VFA 7 546.00±888.70 8 280.00±689.70 9 642.00±540.40 0.19

2.6 海带酶解液对断奶仔猪肠道微生物的影响

2.6.1 海带酶解液对断奶仔猪肠道微生物α多样性的影响

如表7所示,在回肠和盲肠内,对照组的α多样性较高,而在结肠中则是抗生素组的α多样性较高。在高剂量海带酶解液组中,相比于盲肠与结肠,回肠中微生物多样性较低。
表7 海带酶解液对断奶仔猪肠道微生物α多样性的影响

Table 7 Effects of kelp enzymatic hydrolysate on intestinal microorganism α diversity of weaned piglets

项目
Items		 无抗对照组
Antibiotic free
control group		 抗生素组
Antibiotic group		 高剂量海带酶解液组
High level kelp enzymatic
hydrolysate group		 P值
P-value
回肠Ileum
Shannon指数Shannon index 2.18±0.01Cc 0.58±0.01Aa 1.25±0.01Bb <0.01
Simpson指数Simpson index 0.31±0.01Aa 0.79±0.01Cc 0.40±0.01Bb <0.01
盲肠Cecum
Shannon指数Shannon index 3.99±0.31 3.64±0.34 3.25±0.13 0.24
Simpson指数Simpson index 0.05±0.02 0.08±0.03 0.11±0.03 0.41
结肠Colon
Shannon指数Shannon index 3.86±0.36 4.17±0.59 3.66±0.57 0.79
Simpson指数Simpson index 0.09±0.03 0.05±0.01 0.09±0.03 0.56

2.6.2 海带酶解液对断奶仔猪肠道微生物组成的影响(门水平)

从图1可知,不同组断奶仔猪肠道微生物在门水平上相对丰度不小于1%的菌门由多到少依次为厚壁菌门(Firmicutes)、拟杆菌门(Bacteroidetes)、放线菌门(Actinobacteria)、变形菌门(Proteobacteria)、ε-变形菌(Epsilonbacteraeota)。
图1 海带酶解液对断奶仔猪肠道微生物组成的影响(门水平)

Firmicutes:厚壁菌门;Bacteroidetes:拟杆菌门; Actinobacteria:放线菌门;Proteobacteria:变形菌门;Epsilonbacteraeota:ε-变形菌;other:其他。

样品按“肠段_处理”命名,H、M、J分别代表回肠、盲肠、结肠,CON、ANTI、75分别代表无抗对照组、抗生素组、高剂量海带酶解液组。下图同。

Fig.1 Effects of kelp enzymatic hydrolysate on composition of gut microbiota of weaned piglets (phylum level)

The samples were named as “intestinal segment_treatment”, with H, M and J representing ileum, cecum and colon, and CON, ANTI and 75 representing antibiotic free control diet, antibiotic diet and high level kelp enzymatic hydrolysate diet, respectively. The same as below.

2.6.3 海带酶解液对断奶仔猪肠道微生物组成的影响(属水平)

由图2可知,不同组断奶仔猪肠道微生物在属水平上相对丰度不小于1%的前3种由多到少依次为链球菌属(Streptococcus)、乳杆菌属(Lactobacillus)、罕见小球菌属(Subdoligranulum)。其中,抗生素组和高剂量海带酶解液组断奶仔猪回肠微生物中Streptococcus相对丰度最高,分别达到了92%和88%,但对照组中Lactobacillus相对丰度最高,达到了70%。除这2个属外的微生物在盲肠、结肠中占比之和都比回肠中多。前3种和相对丰度小于1%菌属占据了各样本中微生物的40%以上。
图2 带酶解液对断奶仔猪肠道微生物组成的影响(属水平)

Streptococcus:链球菌属;Lactobacillus:乳杆菌属;Subdoligranulum:罕见小球菌属;Blautia:布劳特氏菌属;Clostridium_sensu_stricto-1:狭义梭状芽胞杆菌1;Terrisporobacter:土孢杆菌属;Ruminococcaceae_UCG-008: 瘤胃球菌科UCG-008; [Ruminococcus]_gauvreauii_group:高氏瘤胃球菌属群;Ruminococcaceae_UCG-005: 瘤胃球菌科UCG-005;unclassified_o_Lactobacillales:未分类乳杆菌目;Collisella:柯林斯菌属;Ruminococcaceae_UCG-014: 瘤胃球菌科UCG-014;Alloprevotella:异普雷沃菌属;Faecalibacterium:粪杆菌属;Dorea:多尔氏菌属;Turicibacter:苏黎世杆菌属;unclassified_f_Lachnospiraceae:未分类毛螺菌科;[Eubacterium]_hallii_group: 霍氏真杆菌群;Phascolarctobacterium: 考拉杆菌属;Coprococcus_3:粪球菌属3; Escherichia-Shigella:大肠杆菌志贺菌属;Christensenellaceae_R-7_group:克里斯滕森菌科R-7群;Ruminococcus_1: 瘤胃球菌属1; norank_f_Eggerthellaceae: 未分类伊格尔兹氏菌目;Rikenellaceae-RC9_gut_group:理研菌科RC9肠群;Prevotellaceae_NK3B31_group: 普雷沃氏菌科NK3B31群;Campylobacter:弯曲杆菌属;Prevotella_9;普雷沃菌属9;Parabacteroides:副拟杆菌属;Solobacterium:拟杆菌属;Intestinibacter:肠杆菌属;Ruminococcaceae_UCG-002: 瘤胃球菌科UCG-002;Actinobacillus:放线菌属;unclassified_o_Bacteroidales:未分类拟杆菌目;Olsenella: 欧陆森氏菌属 ;uncalssified_f_Veillonellaceae:未分类韦荣氏球菌科;Others:其他。

Fig.2 Effects of kelp enzymatic hydrolysate on composition of gut microbiota of weaned piglets (genus level)

图3是使用海带酶解液对断奶仔猪肠道微生物组成的影响在属水平上的heatmap图,包括分类水平总丰度前50的物种。由图3可知,高剂量海带酶解液组和抗生素组的回肠微生物组成及丰度更为相似,与无抗对照组的差异较大。在回肠中,对照组Lactobacillus相对丰度最高,抗生素组和高剂量海带酶解液组Streptococcus相对丰度最高。
图3 海带酶解液对断奶仔猪肠道微生物组成的影响(属水平heatmap图)

Streptococcus:链球菌属;Lactobacillus:乳杆菌属;Actinobacillus:放线菌属;Escherichia-Shigella:大肠杆菌志贺菌属;Parabacteroides:副拟杆菌属;Intestinibacter :肠杆菌属;Subdoligranulum:罕见小球菌属;Blautia:布劳特氏菌属;Clostridium_sensu_stricto-1:狭义梭状芽胞杆菌1;Terrisporobacter:土孢杆菌属;unclassified_o_Lactobacillales:未分类乳杆菌目;Turicibacter:苏黎世杆菌属;Ruminococcaceae_UCG-008: 瘤胃球菌科UCG-008;Agathobacter:阿加索杆菌属;Collisella:柯林斯菌属;Ruminococcaceae_UCG-005: 瘤胃球菌科UCG-005;Dorea:多尔氏菌属;unclassified_f_Lachnospiraceae:未分类毛螺菌科;Alloprevotella:异普雷沃菌属;Faecalibacterium:粪杆菌属;unclassified_o_Bacteroidales:未分类拟杆菌目;Ruminococcaceae_UCG-002: 瘤胃球菌科UCG-002;Olsenella:欧陆森氏菌属;Ruminococcus_1: 瘤胃球菌属1;Prevotellaceae_NK3B1_group:普雷沃氏菌科NK3B1群;Prevotella_9:普雷沃氏菌属9;Coprococcus_1:粪球菌属1;Ruminococcus_2: 瘤胃球菌属2; Christensenellaceae_R-7_group:克里斯滕森菌科R-7群;norank_f_Eggerthellaceae:未分类伊格尔兹氏菌科;Rikenellaceae-RC9_gut_group:理研菌科_RC9肠群;Coprococcus_3:粪球菌属3;[Eubacterium]_coprostanoligenes_group:产粪甾醇真杆菌群;Marvinbryantia:马文布莱恩特氏菌;[Eubacterium]_hallii_group:霍氏真杆菌群;Phascolarctobacterium:考拉杆菌属;Mogibacterium:艰难杆菌属;Solobacteroides:拟杆菌属;Lachnospira:毛螺菌属;Intestinimonas:肠单胞球菌属;Peptococcus:消化球菌属;norank_f_norank_o_Mollicutes_RF38:未分类柔膜细菌纲RF38群;Negativibacillus:阴沟杆菌属;Butyricicoccus:丁酸梭菌属;Campylobacter:弯曲杆菌属;unclassified_f_Veillonellaceae:未分类韦荣氏球菌科。

Fig.3 Effects of kelp enzymatic hydrolysate on composition of gut microbiota of weaned piglets (genus level heatmap)

3 讨论

3.1 海带酶解液对断奶仔猪生长性能的影响

海带酶解液的主要有效成分包括海藻多糖和海藻寡糖。有研究表明,通过糖苷键将单糖相互连接而形成的植物多糖具有改善动物生长性能的作用[22]。Heim等[23]研究发现,昆布多糖可显著提高仔猪ADG,同时降低F/G。此外,海藻寡糖也具有多种生物学功能,包括改善生长性能、促进肠道健康、抗菌抗病毒和增强机体免疫力等[24]。本研究结果表明,在饲粮中添加高剂量海带酶解液可降低F/G,这种功效可能与海带酶解液的浓度有关。与本研究结果相似,在断奶仔猪饲粮中添加海藻寡糖提高了营养物质的消化率,并改善了生长性能[25-26]。另外,张丽等[27]的研究中发现,随着饲粮中添加的褐藻寡糖浓度逐渐增加,断奶仔猪的ADG和ADFI随之提高。

3.2 海带酶解液对断奶仔猪腹泻频率的影响

断奶仔猪由于肠道功能尚未发育完善,因此很有可能会因断奶应激等导致微生物平衡遭到破坏,有害菌繁殖,进而引发严重的腹泻甚至死亡事件[28-29]。有研究发现,在断奶仔猪饲粮中添加植物提取多糖,可修复仔猪肠道功能,同时缓减断奶后的腹泻[30-31]。海藻多糖可以激活Toll样受体(TLRs)信号通路和调节核因子-κB(NF-κB)信号通路,上调猪小肠上皮细胞(IPEC-J2)紧密连接蛋白闭合蛋白(occludin)、紧密连接蛋白-1(claudin-1)和闭锁小带蛋白-1(ZO-1)的mRNA表达量,同时通过降低IPEC-J2细胞的相关基因的表达以改善小肠上皮细胞的屏障功能[32]。海藻多糖和海藻寡糖可通过激活黏蛋白的合成和分泌,增加黏蛋白层的厚度,形成肠道黏膜的保护屏障。此外,海藻多糖和海藻寡糖还能够减少炎症反应,抑制炎症因子的产生,防止黏膜损伤和炎症的发生,从而减少腹泻的发生率[33]。而本研究未发现饲粮中添加海带酶解液对断奶仔猪腹泻频率有明显影响,这可能与仔猪健康状况与受应激程度有关。

3.3 海带酶解液对断奶仔猪血清免疫球蛋白含量的影响

机体免疫球蛋白含量的高低,决定了断奶仔猪在面对外界入侵的细菌、真菌或病毒时,机体能否迅速识别和结合抗原,产生足够的免疫力并减少对机体的损伤[34]。而本研究结果表明,饲粮中添加海带酶解液对血清免疫球蛋白含量无显著影响。杨晋[31]和刘永童[35]在断奶仔猪饲粮中添加海藻多糖的研究结果也都发现海藻多糖对断奶仔猪血清中的免疫球蛋白含量无显著影响。

3.4 海带酶解液对断奶仔猪肠道形态的影响

饲粮中的抗营养因子可能会刺激断奶仔猪的肠道绒毛萎缩及CD增加,因此常导致对蛋白质的消化吸收功能减弱[36]。此外,断奶后因摄入的营养物质改变,为了适应营养变化,机体自身结构也发生改变,通常表现为肠道上皮细胞增殖、分化以及凋亡机制发生变化,最终影响肠绒毛形态,导致绒毛萎缩和隐窝增生而降低肠道的消化吸收功能[37]。与叶仕斌等[38]的研究结果一致,本研究在添加高剂量海带酶解液后发现可显著提高断奶仔猪空肠和回肠的V/C,说明海带酶解液可以通过改善断奶仔猪的肠道形态,维持肠道健康,进而增强肠道对营养物质的吸收和利用能力。究其原因,可能与海带酶解液促进了肠道内有益菌的生长,同时抑制有害菌的繁殖,改变了肠道内环境并最终维持肠道结构和功能有关[39⇓⇓-42]。此外,海带酶解液也可通过调节免疫反应、抗炎作用以及促进肠黏膜修复等机制对肠道形态产生影响[35,43]。这也可能是本试验发现高剂量海带酶解液可提高断奶仔猪饲料转化效率这一结果的原因。相比之下,在饲粮中添加海带酶解液对断奶仔猪十二指肠肠道形态未产生显著影响,可能的原因是海带酶解液的主要活性成分无法在十二指肠的部位发挥作用,或者在此部位的生理功能不受寡糖和多糖成分的影响。而在其他肠道部位显现出的效果可能是因为空肠与回肠部位对海带酶解液中的生物活性物质有更大的敏感度或易受性。以上结果对海带酶解液在断奶仔猪饲粮中的应用提供新的研究启示。

3.5 海带酶解液对断奶仔猪肠道食糜VFA含量的影响

VFA是肠道发酵代谢产物,主要是乙酸、丙酸和丁酸,对肠道健康和养分吸收非常重要[44]。丁酸作为肠上皮细胞的燃料来源,可以改善肠黏膜屏障的功能并减轻结肠炎[45-46]。据报道,乙酸和丙酸可增强大鼠结肠和培养的肠细胞中紧密连接屏障的完整性[47]。本研究结果表明,海带酶解液对断奶仔猪盲肠和结肠食糜中的VFA含量无显著影响。海带酶解液中的海藻多糖和海藻寡糖主要是多糖类物质,而不是纤维素类物质。肠道微生物通常通过发酵纤维素来产生VFA,而海藻多糖和寡糖并不是它们的首选糖源。因此,海带酶解液中的成分可能无法提供足够的底物来促进VFA的产生。此外,微生物群落中的不同菌种对底物的利用能力和效率有所不同。因此,肠道微生物的变化也和VFA的产生息息相关。研究表明,浒苔多糖刺激肠道乳酸杆菌种群的生长发酵过程[48]。补充海藻多糖可显著增加盲肠消化物中乙酸、丁酸含量和乳酸杆菌的数量,为海藻多糖改善肠道屏障功能的潜在机制[49]。由于本研究中海带酶解液对断奶仔猪的肠道微生物产生了一定的改变,但这些变化可能主要发生在空肠和回肠中,而对盲肠和结肠的微生物组成影响较小。不同肠道部位的微生物群落具有不同的功能和代谢特点,对底物的利用和VFA的产生存在差异,从而可能导致不同组仔猪肠道VFA含量无显著差异。

3.6 海带酶解液对断奶仔猪肠道微生物组成的影响

肠道中同时存在有益菌和有害菌,其中有益菌对维持肠道的保护屏障功能、调节肠道黏膜免疫等方面具有重要的作用。正常情况下,仔猪肠道内的有益菌和有害菌数量保持平衡,但是在突然断奶后,肠道微生物可能发生变化而导致严重的腹泻[50-51]。在α多样性方面, Shannon指数描述种的多寡性,Shannon指数越大,生物多样性越高。Shannon指数来源于信息熵,Shannon指数越大,表示不确定性大。不确定性越大,表示这个群落中未知的因素越多,也就是多样性高[52]。Simpson指数描述从1个群落种连续2次抽样所得到的个体数属于同一种的概率[53]。本研究发现,高剂量海带酶解液对断奶仔猪肠道微生物α多样性有影响。在回肠样本中,对照组的α多样性较高;在盲肠样本中,仍然是无抗对照组的α多样性较高;而在结肠中,抗生素组的α多样性较高。此外,相比于盲肠和结肠,回肠中的微生物多样性较低。其中,在回肠中,无抗对照组的α多样性较高,表明可能海带酶解液在回肠中的作用较为有限,因为回肠是离胃较远的肠段,而海带酶解液可能在较早的消化过程中被分解或失去活性。在盲肠中,海带酶解液可能通过提供海藻多糖和海藻寡糖等有益的营养物质,促进了盲肠内微生物的生长和多样性。这些营养物质可能为有益微生物提供了理想的生存环境,从而增加了多样性。而在结肠中,抗生素组的α多样性较高,提示抗生素组的断奶仔猪结肠内微生物种类较多,可能说明抗生素的使用因导致微生物失衡,减少部分微生物的竞争压力,从而使其他微生物有机会增加多样性。
本研究发现, Streptococcus和Lactobacillus在不同组中显示出差异,其中,相比于无抗对照组,高剂量海带酶解液组断奶仔猪回肠中的Streptococcus相对丰度显著增加,与抗生素组相近。这说明海带酶解液对回肠微生物具有与抗生素相似的调节作用,存在着替代抗生素达到稳定肠道微生物组成的潜在优势。若通过添加海带酶解液能够改变肠道微生物组成,并达到与抗生素类似的作用效果,则可在仔猪饲养过程中推广应用替代抗生素。另外,海带酶解液可能通过影响微生物的代谢途径和生态功能来调节微生物群落结构。海藻多糖和海藻寡糖作为益生元,可以提供有益菌的生长环境,如乳酸菌和双歧杆菌等;通过有益菌产生有机酸降低肠道内pH继而抑制病原菌的生长,维持肠道微生物的稳定性,减少潜在的致病菌的侵袭和感染[54-55]。

4 结论

断奶仔猪饲粮中添加高剂量海带酶解液[75 g/(头·d)]可改善断奶仔猪的肠道形态和肠道微生物组成,具有替代抗生素的潜力。

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