引用本文
王斐, 徐树杰, 李响, 李卫芬. 益生菌在猪上的应用效果和作用机理研究进展[J]. 动物营养学报, 2021, 33(11): 6044-6056.
WANG Fei, XU Shujie, LI Xiang, LI Weifen. Research Progress on Application Effects and Mechanism of Probiotics in Pigs[J]. Chinese Journal of Animal Nutrition, 2021, 33(11): 6044-6056.
益生菌在猪上的应用效果和作用机理研究进展
1. 浙江大学动物科学学院饲料科学研究所, 教育部动物分子营养学重点实验室, 杭州 310058;
2. 浙江大学海南研究院, 三亚 572025
2. 浙江大学海南研究院, 三亚 572025
摘要: 益生菌通过改善宿主肠道菌群结构、提高营养物质消化吸收和增强机体免疫力等机理促进动物生长。本文总结了益生菌对猪生长和繁殖性能的影响，并阐述了益生菌的作用机理，以期为益生菌更好地应用于生猪养殖业提供参考。
关键词:
益生菌 养殖业 生猪 肠道健康
Research Progress on Application Effects and Mechanism of Probiotics in Pigs
1. Key Laboratory of Animal Molecular Nutrition of Ministry of Education, Institute of Feed Science, College of Animal Science, Zhejiang University, Hangzhou 310058, China;
2. Hainan Institute of Zhejiang University, Sanya 572025, China
2. Hainan Institute of Zhejiang University, Sanya 572025, China
Abstract: Probiotics can promote animal growth by improving the structure of host intestinal flora, enhancing nutrient digestion and absorption and enhancing body immunity. This paper summarized the effects of probiotics on growth and reproductive performance of pigs, and then elaborated the mechanism of probiotics, aiming to provide reference for better application of probiotics in the pig breeding industry.
Key words:
probiotics breeding industry pigs intestine health
我国是世界上生猪养殖规模和消费量最大的国家。2010—2018年，我国生猪存栏量和产量分别在4.5亿头左右和5 100万t以上；2019年，非洲猪瘟的传入对生猪养殖业造成了较大影响，生猪存栏量和猪肉产量分别降至3.1亿多头和4 200多万t[1]。随着2020年7月1日起饲料全面禁抗(中药类除外)的实施，生猪养殖业面临了更大的挑战，安全、绿色、促健康的饲料添加剂已成为当前研究的热点和市场急需产品。大量研究表明，益生菌、益生元、酸化剂、植物提取物和抗菌肽等在替代饲用抗生素方面均有一定的效果。其中，益生菌的应用较为广泛，当在动物饲粮中给予一定数量时，能够提高宿主肠道中有益微生物的数量，促进动物肠道健康[2]。饲用益生菌可分为乳酸菌类、芽孢杆菌类和酵母菌类三大类[3]。益生菌具有维持肠道菌群稳态、抑制病原菌定植、改善肠道黏膜结构、促进营养物质消化吸收、增强机体免疫机能和预防动物患病等功效[4-6]。本文就益生菌在生猪上的应用以及作用机理等方面进行综述，旨在为益生菌能更好地应用于生猪养殖业提供参考。
1 益生菌在猪上的应用效果总得来说，在饲粮中添加益生菌可以改善猪各个阶段的健康状况并提高生产性能。
1.1 益生菌在仔猪上的应用效果仔猪断奶后，消化道中的乳酸菌数量减少，胃中pH升高，导致消化酶活性下降，同时由于饲粮更换和环境改变所造成的应激，促使断奶仔猪肠道中的病原菌大量增殖，最终导致仔猪腹泻[7-8]。断奶仔猪腹泻是养猪业中最为突出的问题。益生菌在仔猪上的应用效果主要表现在降低腹泻和提高生长性能等。如鼠李糖乳杆菌能使仔猪腹泻率比对照组降低30.73%[9]，枯草芽孢杆菌能使仔猪平均日增重比对照组提高7.37%[10]。在仔猪饲粮中添加富硒益生菌或粪肠球菌可改善肠道微生物组成，增加乳酸杆菌数量，从而改善仔猪生长性能[11-12]。益生菌还可以提高仔猪的免疫功能和抗体水平，口服枯草芽孢杆菌可显著提高感染猪流行性腹泻病毒的仔猪血清中免疫球蛋白G(IgG)和回肠免疫球蛋白A(IgA)含量[13]；德氏乳杆菌可使仔猪肠黏膜分泌型免疫球蛋白A(sIgA)含量显著提高[14]。sIgA是调节肠黏膜防御能力的主要抗体，可保护肠上皮免受肠毒素和病原微生物的侵害，有助于维持肠内稳态[15]，从而改善仔猪的免疫应激。
此外，适量的益生菌可使仔猪肠道中挥发性脂肪酸的含量显著增加，抑制病原菌生长，促进营养物质消化吸收[16]。但过量添加益生菌会使其效果下降，如饲粮中添加6×1011 CFU/kg枯草芽孢杆菌组的仔猪生长性能低于最适添加量组，但优于不添加组[17]。近年来，益生菌在仔猪上的应用效果见表 1[10-11, 14, 18-40]，除改善生长性能外，益生菌还能改善仔猪肠道微生物的组成以及肠黏膜结构，增强肠道屏障、抗氧化和免疫功能，减少仔猪肠道炎症等。
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表 1 益生菌在仔猪上的应用效果 Table 1 Application effects of probiotics in piglets |
研究表明，饲粮中单独或复合使用益生菌可以维持生长育肥猪肠道的形态完整[41]，促进肠绒毛增长和消化酶的分泌[42]，提高其平均日增重，改善猪肉肉色、pH、眼肌面积和大理石花纹等指标[43]，提高生长育肥猪对干物质和氮的消化率，增加粪便中乳酸菌的数量，降低粪便的pH，减少总硫醇和氨的排放等[44]。肉质的嫩度和多汁性主要取决于猪肉肌间脂肪的含量，而在饲粮中添加乳酸球菌FT28不仅可以降低猪肉pH以及血清中的甘油三酯含量，增加肌内脂肪含量从而改善肉质风味, 而且可以通过阻止脂质氧化来改善肌肉内的氧化稳定性，但对猪腰肌的水分和粗蛋白质含量没有影响[45]。总而言之，益生菌可影响生长育肥猪的生长性能、肠道健康、胴体品质和肉品质等，其在生长育肥猪上的应用效果见表 2[41-42, 44-49]。
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表 2 益生菌在生长育肥猪上的应用效果 Table 2 Application effects of probiotics in growing-finishing pigs |
目前种猪繁殖性能低下仍然是我国养猪业面临的严峻问题，种猪的繁殖能力改善不仅需要提高母猪的受胎率和产仔数，还要改善出生仔猪免疫力从而提高仔猪的存活率。研究表明，饲粮中单独或复合使用益生菌可有效提高母猪采食量[50]、妊娠期母猪体重[51]、哺乳中期母猪血清中胆固醇和脂质含量[52]、胎次数[53]、乳汁分泌量及其IgA和IgG含量，增加仔猪出生体重和免疫力，降低出生仔猪腹泻率和死亡率[54]。另外，益生菌对种公猪精液品质也有很好的改善作用，如用含有0.3 mg/kg富硒益生菌的饲粮饲喂种公猪，能增加其精液中健康精子的数量，提高精子形态和功能的完整性以及谷胱甘肽过氧化物酶的活性[55]。总得来说，益生菌对种猪繁殖性能具有显著的积极作用，益生菌在种猪上的应用效果见表 3[50-51, 54-60]。
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表 3 益生菌在种猪上的应用效果 Table 3 Application effects of probiotics in breeding pigs |
肠道微生物由100多万亿个细菌组成，与肠道发育密切相关，不同的菌群通过各自新陈代谢的过程使得动物肠道内环境维持在相对稳定的状态[61]。猪肠道微生物主要由真菌、链球菌属、乳杆菌属、梭菌属以及拟杆菌属等组成[62]。
益生菌可以调节肠道菌群的结构和功能。益生菌通过争夺营养抑制有害菌附植，并且产生代谢物质，如乳酸菌在代谢过程中可以产生细菌素、有机酸、过氧化氢和短链脂肪酸等，抑制病原菌增殖[63-65]。此外，益生菌还可以通过占位效应抢占肠道中的附植位点，抑制或阻断病原菌的吸附和定植，调节肠道菌群的结构和功能，控制肠道内毒素和其他有害代谢产物的产生量，从而促进动物肠道的发育[66]。饲粮中添加0.1%的含芽孢杆菌的复合益生菌能显著增加断奶仔猪粪便中乳酸杆菌的数量，并减少大肠杆菌的数量，提高养分消化率[67]，而粪肠球菌对大肠杆菌具有特定的预防作用，可以显著降低仔猪肠道黏膜上黏附的致病性大肠杆菌的数量[68]。
猪肠道微生物大部分属于厚壁菌门和拟杆菌门[69]。肠道内菌群不同其功能则不同，代谢产物也不同。贝莱斯芽孢杆菌B13能显著提高猪肠道中瘤胃球菌属和毛螺菌科的相对丰度，使肠道中短链脂肪酸产生增多，对抵抗炎症有促进作用[70]。Wang等[71]研究表明，地衣芽孢杆菌和枯草芽孢杆菌复合益生菌不仅能提高拟杆菌科和瘤胃球菌属的相对丰度，还能降低梭状芽孢杆菌的相对丰度，并加快肠道菌群的成熟。益生菌通过影响猪肠道菌群结构、功能以及肠道菌群的代谢产物，从而影响猪肠道健康和生长性能。
当致病菌在猪肠道中大量定植后，产生的细菌毒素进入肠腔内，分解细胞间紧密连接蛋白来破坏肠道屏障，再进入体内循环，导致动物机体患病[72]。细菌素是某些细菌在代谢过程中由核糖体合成的一类抗菌肽，不仅可以对目标致病菌产生抑制效果，同时还对肠道菌群的结构和代谢产物产生影响[73]。通过对艰难梭菌CD4菌株的遗传修饰，得到的R型细菌素能有针对性地预防艰难梭菌在动物肠道中定植，并能将其有效地消灭[74]。
2.2 提高机体对营养物质的消化吸收以及肝脏的代谢功能益生菌本身不仅能分泌消化相关的酶类，还能影响宿主消化道淀粉酶、脂肪酶、蛋白酶、二糖酶和肽酶等酶的分泌和活性，从而促进营养物质的消化吸收，提高饲粮利用率[75]。益生菌还通过调节肠道菌群影响肠道微生物酶的合成和分泌。有研究发现，干酪乳杆菌和粪肠球菌能刺激猪肠道中可分泌蛋白酶和淀粉酶的微生物生长繁殖，从而提高猪消化道中相关酶活性[76]。而丁酸梭菌可以通过抑制大肠杆菌K88和脂多糖的毒性保障肠道的完整性，提高受大肠杆菌K88感染的动物消化道中消化酶的活性，丁酸梭菌组或抗生素组动物在试验第3、7和14天蛋白酶和淀粉酶活性更高，在试验后第3和7天脂肪酶活性更高[77]。
益生菌可通过提高肠上皮细胞的吸收能力和转运载体的表达，促进小肽和氨基酸等小分子物质的吸收和转运[78]。此外，益生菌对糖类的转运也有积极作用，葡萄糖转运蛋白(GLUT)家族蛋白是介导葡萄糖摄取的膜载体蛋白，它通过协同扩散方式帮助细胞转运糖类[79]。钠/葡萄糖转运蛋白1(SGLT1)介导的葡萄糖摄取增加了小肠抗凋亡蛋白，并保护了肠上皮细胞免受凋亡和屏障缺陷的影响[80]；肽转运蛋白1(PEPT1)在机体中大量表达，介导小肽的吸收[81]。有研究表明，益生菌可以上调GLUT2和PEPT1基因的表达[82-83]。
肝脏在营养物质代谢中有着非常重要的作用，包括糖原储存、蛋白质和脂质的合成以及解毒作用等[84-85]。在肝脏中，葡萄糖和脂质代谢的异常能导致肝脂肪变性和全身胰岛素抵抗等有关疾病，胰岛素受体底物2(IRS2)/磷脂酰肌醇3-激酶(PI3K)/RAC-β丝氨酸/苏氨酸蛋白激酶2(Akt2)信号传导能调节葡萄糖转运和脂质与糖原合成，而腺苷酸活化蛋白激酶(AMPK)是脂质和蛋白质合成与葡萄糖转运的主要调节剂[86]。益生菌能有效调节体内相关因子的水平，提高肝脏对营养物质代谢的功能，如植物乳杆菌Ln4能提高肝脏中与葡萄糖和脂质代谢相关的代谢因子的水平，包括IRS2、Akt2、AMPK以及脂蛋白脂酶的mRNA水平[87]，而枯草芽孢杆菌能下调肝脏中脂肪酸合成酶和乙酰辅酶A羧化酶α的mRNA水平[88]。
高脂饮食能改变肠道菌群，使肠道内脂多糖含量增多，从而诱发肠道炎症，机体产生胰岛素抵抗[89]，而发酵乳杆菌CECT5716可预防肝脂肪变性，减轻胰岛素抵抗，并显著改善营养不良[90]。还有研究表明，嗜酸乳杆菌和干酪乳杆菌能通过降低肝脏葡萄糖的积累，以及血浆总胆固醇、低密度脂蛋白和极低密度脂蛋白的含量，从而减少胰岛素抵抗的发生[91]。当动物机体的肝功能受损时将会影响动物对营养物质的吸收利用，而长双歧杆菌BB536可以显著降低大鼠血浆总胆固醇含量，减少肝脏脂质沉积，缩小脂肪细胞大小，并改善其肝肾功能[92]。
2.3 改善肠道黏膜结构和物理屏障功能动物机体对营养物质的消化吸收主要在小肠中完成，肠绒毛能增加肠腔吸收营养物质的表面积。肠绒毛是由小肠上皮和固有层向肠腔形成的突起组成，肠绒毛脱落在动物肠道中时刻发生，为了维持肠绒毛的平衡，隐窝基部的细胞能分化形成肠上皮细胞以促进肠绒毛更新[93]。小肠绒毛高度和隐窝深度影响动物消化道对营养物质的消化吸收[94]。绒毛高度增加，隐窝深度变浅，可以增加小肠与营养物质的接触面积，使得小肠对营养物质的消化吸收能力提高[95]。丁酸梭菌能增加十二指肠和空肠中的绒毛高度和绒毛高度/隐窝深度，提高仔猪对营养物质的消化吸收能力[96]。
肠上皮细胞由分泌抗菌肽的潘氏细胞、分泌黏液的杯状细胞和肠内分泌细胞组成，是外部环境与宿主免疫系统之间的物理屏障，由紧密连接的多蛋白结构调节[97]。细胞间紧密连接蛋白调节着各种物质的跨细胞旁路的被动转运，当其紧密连接蛋白相关分子基因和蛋白表达下降，会引起紧密连接结构和功能的改变，进而损害肠道黏膜机械屏障功能[98]，肠道通透性增加，导致动物胃肠功能紊乱[99-100]。罗伊氏乳杆菌LR1能通过激活Toll样受体2增加断奶仔猪肠道中紧密连接蛋白表达和抗菌肽表达[25]，还能促进细胞迁移来改善肠上皮屏障的功能[101]；植物乳杆菌MB452能上调紧密连接蛋白-1(ZO-1)、紧密连接蛋白-2(ZO-2)和闭合蛋白(occludin)的基因和蛋白质表达[102]。
肠上皮的杯状细胞分泌黏液素可以增强肠道屏障功能来缓解应激，但长期的慢性应激会使得杯状细胞的数量减少[103]。有研究发现，嗜黏蛋白-艾克曼菌(Akkermansia muciniphila)能与培养的结肠上皮细胞系Caco-2和HT-29牢固结合以影响黏液层的厚度，并在肠道损伤部位竞争性排斥病原菌，从而保护新生的肠道上皮，维持肠道屏障的完整性和消化吸收功能[104]。
2.4 改善动物肠黏膜免疫屏障和机体免疫功能益生菌对改善动物肠黏膜屏障和机体免疫功能具有积极的作用。肠黏膜免疫屏障由肠道内浆细胞sIgA和肠黏膜淋巴组织构成[105]。sIgA的分泌需要Th1和Th2这2种辅助性T细胞的参与，Th2细胞分泌的转化生长因子-β(TGF-β)、白细胞介素(IL)-4、IL-5、IL-6及IL-10等细胞因子对sIgA分泌有重要的作用[106]；而益生菌和中草药复合制剂能提高猪血清中丙氨酸氨基转移酶活性以及白蛋白、免疫球蛋白M(IgM)、IL-4、IL-6和β-干扰素的含量[107]。上皮内淋巴细胞分布于肠道上皮细胞之间，益生菌能促进其增殖，维持上皮内淋巴细胞数量稳定，如腊状芽孢杆菌饲喂母猪和仔猪能促进肠道内淋巴细胞的增殖以及减少其凋亡，同时增加肠道中吞噬细胞的数量来清除病原菌[108]。
此外，派尔集合淋巴结是小肠黏膜内由B细胞和以CD4+为主的T细胞组成的淋巴滤泡，其表面覆盖的一层M细胞，能识别抗原参与肠道免疫过程，是肠黏膜免疫系统的重要组成部分[109]。益生菌能通过促进肠道中T细胞增殖和血清中免疫因子的含量来保护动物健康，如酿酒酵母能显著增加仔猪血清IgA、IL-2和IL-6的含量和CD4+/CD8+值，促进T淋巴细胞的增殖，从而改善断奶仔猪的免疫功能[110]。饲粮添加发酵乳杆菌I5007可提高仔猪外周血CD4+ T淋巴细胞的百分比，增强胃肠道黏膜肿瘤坏死因子-α(TNF-α)和干扰素-γ(IFN-γ)mRNA的表达，并最终在肠道中发挥免疫调节作用[111]。
2.5 提高抗应激能力，降低细胞凋亡，促进肠黏膜修复应激，包括仔猪早产应激、断奶应激、氧化应激和冷热应激等，是猪养殖中常见的问题，制约着养殖业的发展。应激会导致细胞凋亡，损伤肠道结构，诱导与高通透性和肠道黏膜炎症有关的肠道屏障功能问题，严重影响消化吸收功能[112]。除此之外，应激还会影响猪机体内分泌系统和免疫功能等，降低其抗病力[113]。
益生菌能影响细胞凋亡，修复损伤的肠黏膜。双歧杆菌、嗜酸乳杆菌和干酪乳杆菌等复合益生菌可以改善肠绒毛形态，减少肠道黏膜萎缩、功能障碍和病原体的定植，促进肠黏膜的损伤修复，预防和治疗坏死性小肠结肠炎，从而缓解仔猪的早产应激[114]。罗伊氏乳杆菌和唾液乳杆菌的复合益生菌可以增加仔猪的回肠黏膜和盲肠腔中双歧杆菌的数量和免疫分子的含量，降低皮质醇和内毒素的含量，血浆中生长激素的类胰岛素生长因子含量也有所改善，从而能够缓解仔猪的断奶应激[115]。约翰逊乳杆菌BS15k可以缓解高脂饮食诱导的小鼠氧化应激，同时也可改变小鼠的肠道菌群结构[116]。富硒益生菌通过影响机体内硒的含量和谷胱甘肽过氧化物酶的活性来增强血液抗氧化能力，下调热应激仔猪热休克蛋白的mRNA水平，缓解高温引起的热应激[117]；并通过影响脱碘酶的活性来增强甲状腺功能，降低丙二醛含量和热应激引起的自由基增加，使得生产性能得到提高[12]。将双歧杆菌与致病菌共培养后可降低细胞凋亡，显著缓解致病菌对细胞膜的损伤[118]。此外，益生菌还可以调节黏蛋白的产生，同时通过影响肠道黏蛋白单糖的组成、黏液层的厚度和肠道形态等来促进肠黏膜修复，从而维持肠道屏障的完整性[119-120]。
3 小结益生菌具有改善肠道菌群和黏膜结构，提高肠黏膜屏障功能、机体免疫功能和抗氧化应激能力，以及促进肠黏膜修复和营养物质消化吸收代谢等诸多生物学功能，因此可以提高生猪各个阶段生产性能。但有关益生菌深入的作用机制还需作进一步的研究，以使其在生猪养殖业中发挥更大的作用。
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