解淀粉芽孢杆菌SC06介导猪肠道免疫机理的研究
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摘要
芽孢杆菌制剂是目前畜牧养殖业中应用较为广泛的益生菌制剂。本实验室前期从土壤中分离得到一株解淀粉芽孢杆菌SC06(简称Ba,保藏于中国典型培养物保藏中心,保藏号为CCTCC No:M2012280)。通过前期试验发现,益生菌Ba替代50%抗生素用量后,可有效降低断奶仔猪腹泻率,同时提高动物生长性能。基于上述试验结果,本论文拟进一步研究益生菌Ba调节动物肠道免疫功能的机理。同时探讨益生菌Ba替代抗生素(吉他霉素)对育肥阶段猪的饲喂效果研究。本研究分以下四部分试验：
(1)研究益生菌Ba对病原菌Escherichia coli K88(ETEC)介导IPEC-1细胞引起的炎症反应及其MAPKs信号通路的影响：IPEC-1细胞培养12天后可观察到致密的细胞单层和肠绒毛的形成,表明其在体外培养条件下可分化成熟。通过优化ETEC不同菌量,表明108cfu/ml剂量可有效引起IPEC-1细胞发生炎症反应。益生菌Ba预处理成熟分化的IPEC-1细胞,可有效抑制ETEC引起的IL-6、IL-1α和TNF-α炎症基因表达量的提高,表明益生菌Ba可有效抑制ETEC诱导的炎症反应。Western blot分析发现,益生菌Ba预处理IPEC-1细胞24h后,可显著降低ETEC引起的ERK、JNK和p38蛋白质磷酸化水平。上述结果说明益生菌Ba有可能通过MAPKs减轻ETEC诱导的IPEC-1细胞炎症反应。
(2)益生菌Ba对原代巨噬细胞分型的影响：为进一步探讨益生菌Ba对其它免疫细胞种类及其功能的影响,本试验以幼龄C57BL/6小鼠为研究模型,通过益生菌灌胃试验,运用流式细胞术发现脾脏中巨噬细胞比例由3.35%增加到8.55%(P<0.05),而T细胞和B细胞数量无显著变化(P>0.05),且抗体IgG和IgM含量无显著变化(P>0.05),提示益生菌Ba可能通过巨噬细胞发挥其免疫调节功能。同时发现,益生菌Ba可以有效降低小鼠断奶应激所造成的细菌移位。体外原代巨噬细胞试验发现,益生菌Ba处理M0型细胞后,其M1型相关基因TNF-α、IL-6、iNOS和IL-1β表达量显著上调,细胞上清NO含量显著提高(P<0.05)。相反,M2型基因Fizz1、Arg1、MR和Ym1相对表达量显著下(P<0.05),说明益生菌Ba可有效介导原代巨噬细胞(M0)向M1型巨噬细胞分化。FITC-dextran吞噬试验表明,益生菌Ba介导原代巨噬细胞(M0)向M1型分化后,其细胞吞噬活性显著提高(P<0.05)。本试验从分子免疫学角度发现了益生菌Ba可有效介导巨噬细胞分型,从而发挥相关免疫功能,进而解释益生菌清除病原菌的可能机制。
(3)益生菌Ba替代抗生素(吉他霉素)后对育肥猪生长性能及其肠道菌群的影响：通过育肥猪饲养试验发现,与抗生素吉他霉素组相比,抗生素+Ba和Ba试验组的平均日米食量(ADFI)(P<0.05)和平均日增重(ADG)显著提高(P<0.05)。试验表明日粮中添加益生菌Ba替代抗生素(吉他霉素)后,可有效提高动物的生长性能。通过肠道HE染色试验发现,与对照抗生素组相比,抗生素+Ba和Ba试验组中回肠绒毛高度显著提高(P<0.05),隐窝深度无显著变化(P>0.05),但绒毛高度与隐窝深度的比例(V：C)有一定提高的趋势,但统计无显著变化(P>0.05)。经ROCHE454测序试验表明,育肥猪肠道优势菌主要包括厚壁菌(Firmicutes)和拟杆菌(Bacteroidetes)。与抗生素对照组相比,益生菌添加组中的厚壁菌比例显著提高(P<0.05),同时拟杆菌和变形菌比例显著降低(P<0.05)。其中,拟杆菌纲在拟杆菌门中占有绝大多数比例。拟杆菌纲在抗生素组、抗生素+Ba和Ba试验组中分别占有71.09%、83.50%和67.66%。进一步分析发现,拟杆菌目占拟杆菌纲中绝大多数,梭杆菌门数量比例极少。育肥猪盲肠中厚壁菌门主要有芽孢杆菌纲、梭状芽胞杆菌纲和放线菌纲。芽孢杆菌纲在抗生素组、抗生素+Ba和Ba处理组中占厚壁菌门比例分别为67.98%、82.13%和84.48%。Erysipelotrichi菌分别占有13.9%、6.77%和6.15%。上述试验表明,益生菌Ba替代抗生素后,能有效改善猪肠道菌群结构,从而维持肠道健康。
(4)益生菌Ba替代抗生素(吉他霉素)后对育肥猪肝脏保护功能及其机理研究：通过血清生化指标测定发现,大多数指标胆固醇、氨、尿素氮、淀粉酶等均无显著变化(P>0.05)。有趣的是,实验结果表明抗生素组谷丙转氨酶和谷草转氨酶含量显著高于益生菌Ba处理组(P<0.05),其中谷丙转氨酶含量达到43.86IU/L,超出正常的生理范围。通过透射电镜技术观察,尽管肝细胞整体形态无明显变化,但进一步研究发现抗生素组线粒体发生明显肿胀(P<0.05),而添加益生菌Ba后肿胀现象明显缓解(P<0.05)。同时,抗生素组内质网发生较为明显的损伤,形成大量空泡,抗生素+Ba和Ba处理组中的内质网空泡数量显著减少(P<0.05)。本试验结果提示,益生菌Ba可有效缓解或预防抗生素(吉他霉素)引起育肥猪的肝脏损伤,而这一现象可能是通过介导内质网应激发挥其调节作用。
综合上述研究结果,初步揭示了益生菌Ba介导猪肠道免疫的机理,为养猪生产中科学合理使用益生菌Ba替代抗生素的可能性提供科学依据和理论基础。
Bacillus is widely used in the livestock industry. The probiotic Bacillus amyloliquefaciens SC06(Ba) was isolated from soil and kept at China Center for Type Culture Collection (CCTCC No:M2012280), In previous study, we found that dietary supplementation with the probiotic Ba could improve the growth performance and decrease the diarrhea incidence in the weaned piglets. Based on the study above, the mechanism of the probiotc Ba regulating the gut immunity will be further explored. In addition, this study was designed to evaluate the effect of fattening pig diets containing the probiotic Ba as alternative antibiotic (kitasamycin), main contents as follows:
(1) The probiotc Ba mediated enterotoxigenic Escherichia coli (ETEC)-induced pro-inflammatory responses and MAPKs:Porcine intestinal epithelial cell line (IPEC-1) formed an epithelial monolayer and the microvillus structures after12days incubation, These results have indicated that IPEC-1cells have successfully differentiated. We introduced the differentiated IPEC-1cells and observed the significant up-regulation expression of pro-inflammatory mediators after ETEC treatment (108cfu/ml), The probiotic Ba could effectively down-regulate IL-6, IL-la and TNF-a production in the differentiated IPEC-1cells with ETEC treatment, These data indicated that Ba inhibited ETEC-induced pro-inflammatory responses in the differentiated IPEC-1cells. Furthermore, the probiotic Ba attenuated ETEC-induced activation of the MAPKs pathways in differentiated IPEC-1cells. The activation level of the ERK1/2, JNK and p38was significantly decreased in the differentiated IPEC-1cells pre-incubated with Ba for24h. In sum, the probiotic Ba could inhibit ETEC-induced pro-inflammatory responses by suppression of MAPKs signaling pathways in intestinal epithelial cells.
(2) Probiotic Bacillus amyloliquefaciens SC06mediated M1macrophage polarization in bone marrow-derived macrophages:Oral administration of Bacillus amyloliquefaciens SC06could decrease bacterial translocation in C57BL/6mice. Furthermore, dramatically increase in the percentage and number of macrophages were observed in the spleen of Ba-treated mice compared with the control and0.85%NaCl group (P<0.05). In contrast, there have been no statistically changes in the splenic CD4+T CD8+T and B cells. Meanwhile, no dramatically changes of IgG and IgM levels were found in intestinal mucosa among the groups. We were interested to know whether probiotic Ba could induce macrophages polarization. Real-time fluorescence PCR analysis demonstrated that the expression of IL-1β, iNOS, TNF-α and IL-6genes for M1macrophages was significantly increased at1.5h after probiotic Ba treatments compared to the probiotic Ba-free treatment (P<0.01), whereas the expression of M2macrophage marker genes (Arg1, Fizz1, MR, Ym1) was decreased (P<0.05). Furthermore, the phagocytic activity was dramatically increased in the Ba-treated BMDMs using a FITC-dextran endocytosis assay. These data indicated that probiotic Ba facilitated polarization of M1macrophages and enhanced its phagocytic capacity. Moreover, the Ba also mediated the autophagy in bone marrow-derived macrophages. The results provided the new insight that how probiotic Ba reduce the diarrhea and clear intracellular pathogens in weaned piglets.
(3) The effects of dietary supplemented Ba replacement with kitasamycin on growth performance and gut flora in the fattening pigs:Adding Ba to swine diets increased ADG (P<0.05) and ADFI (P<0.05) compared to control fed pigs. Compared with the control fed pigs, villus height was significantly increased (P<0.05), crypt depth ratio (V:C) have no significant change (P<0.05). Roche454sequencing data showed that the dominant bacteria of the cecum were the Firmicutes and Bacteroides in fattening pigs. Bacteroides dominated a large portion in the cecum and the Fusobacterium accounted for a small proportion. Cecum of the fattening pigs main contained the Firmicutes, Bacillus, Clostridium and Actinobacteria. Bacillus accounted for the major proportion of Firmicutes in the antibiotic group, antibiotics+Ba and Ba treatment group were67.98%,82.13%and84.48%and the proportion of the Erysipelotrichi holded13.9%,6.77%and6.15%, respectively. Taken together, the Ba could promote growth performance and improve the intestine health, as well as regulate microbial ecological balance in the fattening pigs.
(4) Dietary supplemented Ba alleviated fed diets containing kitasamycin inducing liver injury in fattening pigs:Most of serum biochemical parameters were not different in the three dietary treatments and were within the normal physiologic concentrations. Interestingly, pigs fed diets containing kitasamycon with no Ba had higher glutamic pyruvic transaminase (ALT) and glutamic oxalacetic transaminease (AST) content than the other two treatments (P<0.05), especially the ALT43.8IU/L which was over the normal physiological range. Therefore, these data indicated that the Ba might prevent fed diets containing kitasamycin inducing liver damage. The most abnormality seen was damage to mitochondria and endoplasmic reticulum (ER) including the endoplasmic reticulum dilated and vesiculated, mitochondria swell, cristae vague in fed diets containing antibiotic kitasamycin. Dramatically increase in mitochondrial diameter was found in fed diets containing antibiotic kitasamycin compared with fed diets containing Ba (P<0.05). The average number of ER vacuoles per field in fed diets containing antibiotic kitasamycin was notably higher than that fed diet containing Ba groups (P<0.05). These results suggested that normal ER and mitochondria were restored when fattening pigs were fed with probiotic Ba-supplemented diet. Probiotic Ba may prevent fed diets containing kitasamycin induced-liver injury by attenuated ER and mitochondria damage.
The results provide the implications for elucidating the mechanism that the probiotic Ba regulates the immune response, and also supplying the technological and theoretical guidance for application of the probiotic Ba in livestock and feed industry.
(1)研究益生菌Ba对病原菌Escherichia coli K88(ETEC)介导IPEC-1细胞引起的炎症反应及其MAPKs信号通路的影响：IPEC-1细胞培养12天后可观察到致密的细胞单层和肠绒毛的形成,表明其在体外培养条件下可分化成熟。通过优化ETEC不同菌量,表明108cfu/ml剂量可有效引起IPEC-1细胞发生炎症反应。益生菌Ba预处理成熟分化的IPEC-1细胞,可有效抑制ETEC引起的IL-6、IL-1α和TNF-α炎症基因表达量的提高,表明益生菌Ba可有效抑制ETEC诱导的炎症反应。Western blot分析发现,益生菌Ba预处理IPEC-1细胞24h后,可显著降低ETEC引起的ERK、JNK和p38蛋白质磷酸化水平。上述结果说明益生菌Ba有可能通过MAPKs减轻ETEC诱导的IPEC-1细胞炎症反应。
(2)益生菌Ba对原代巨噬细胞分型的影响：为进一步探讨益生菌Ba对其它免疫细胞种类及其功能的影响,本试验以幼龄C57BL/6小鼠为研究模型,通过益生菌灌胃试验,运用流式细胞术发现脾脏中巨噬细胞比例由3.35%增加到8.55%(P<0.05),而T细胞和B细胞数量无显著变化(P>0.05),且抗体IgG和IgM含量无显著变化(P>0.05),提示益生菌Ba可能通过巨噬细胞发挥其免疫调节功能。同时发现,益生菌Ba可以有效降低小鼠断奶应激所造成的细菌移位。体外原代巨噬细胞试验发现,益生菌Ba处理M0型细胞后,其M1型相关基因TNF-α、IL-6、iNOS和IL-1β表达量显著上调,细胞上清NO含量显著提高(P<0.05)。相反,M2型基因Fizz1、Arg1、MR和Ym1相对表达量显著下(P<0.05),说明益生菌Ba可有效介导原代巨噬细胞(M0)向M1型巨噬细胞分化。FITC-dextran吞噬试验表明,益生菌Ba介导原代巨噬细胞(M0)向M1型分化后,其细胞吞噬活性显著提高(P<0.05)。本试验从分子免疫学角度发现了益生菌Ba可有效介导巨噬细胞分型,从而发挥相关免疫功能,进而解释益生菌清除病原菌的可能机制。
(3)益生菌Ba替代抗生素(吉他霉素)后对育肥猪生长性能及其肠道菌群的影响：通过育肥猪饲养试验发现,与抗生素吉他霉素组相比,抗生素+Ba和Ba试验组的平均日米食量(ADFI)(P<0.05)和平均日增重(ADG)显著提高(P<0.05)。试验表明日粮中添加益生菌Ba替代抗生素(吉他霉素)后,可有效提高动物的生长性能。通过肠道HE染色试验发现,与对照抗生素组相比,抗生素+Ba和Ba试验组中回肠绒毛高度显著提高(P<0.05),隐窝深度无显著变化(P>0.05),但绒毛高度与隐窝深度的比例(V：C)有一定提高的趋势,但统计无显著变化(P>0.05)。经ROCHE454测序试验表明,育肥猪肠道优势菌主要包括厚壁菌(Firmicutes)和拟杆菌(Bacteroidetes)。与抗生素对照组相比,益生菌添加组中的厚壁菌比例显著提高(P<0.05),同时拟杆菌和变形菌比例显著降低(P<0.05)。其中,拟杆菌纲在拟杆菌门中占有绝大多数比例。拟杆菌纲在抗生素组、抗生素+Ba和Ba试验组中分别占有71.09%、83.50%和67.66%。进一步分析发现,拟杆菌目占拟杆菌纲中绝大多数,梭杆菌门数量比例极少。育肥猪盲肠中厚壁菌门主要有芽孢杆菌纲、梭状芽胞杆菌纲和放线菌纲。芽孢杆菌纲在抗生素组、抗生素+Ba和Ba处理组中占厚壁菌门比例分别为67.98%、82.13%和84.48%。Erysipelotrichi菌分别占有13.9%、6.77%和6.15%。上述试验表明,益生菌Ba替代抗生素后,能有效改善猪肠道菌群结构,从而维持肠道健康。
(4)益生菌Ba替代抗生素(吉他霉素)后对育肥猪肝脏保护功能及其机理研究：通过血清生化指标测定发现,大多数指标胆固醇、氨、尿素氮、淀粉酶等均无显著变化(P>0.05)。有趣的是,实验结果表明抗生素组谷丙转氨酶和谷草转氨酶含量显著高于益生菌Ba处理组(P<0.05),其中谷丙转氨酶含量达到43.86IU/L,超出正常的生理范围。通过透射电镜技术观察,尽管肝细胞整体形态无明显变化,但进一步研究发现抗生素组线粒体发生明显肿胀(P<0.05),而添加益生菌Ba后肿胀现象明显缓解(P<0.05)。同时,抗生素组内质网发生较为明显的损伤,形成大量空泡,抗生素+Ba和Ba处理组中的内质网空泡数量显著减少(P<0.05)。本试验结果提示,益生菌Ba可有效缓解或预防抗生素(吉他霉素)引起育肥猪的肝脏损伤,而这一现象可能是通过介导内质网应激发挥其调节作用。
综合上述研究结果,初步揭示了益生菌Ba介导猪肠道免疫的机理,为养猪生产中科学合理使用益生菌Ba替代抗生素的可能性提供科学依据和理论基础。
Bacillus is widely used in the livestock industry. The probiotic Bacillus amyloliquefaciens SC06(Ba) was isolated from soil and kept at China Center for Type Culture Collection (CCTCC No:M2012280), In previous study, we found that dietary supplementation with the probiotic Ba could improve the growth performance and decrease the diarrhea incidence in the weaned piglets. Based on the study above, the mechanism of the probiotc Ba regulating the gut immunity will be further explored. In addition, this study was designed to evaluate the effect of fattening pig diets containing the probiotic Ba as alternative antibiotic (kitasamycin), main contents as follows:
(1) The probiotc Ba mediated enterotoxigenic Escherichia coli (ETEC)-induced pro-inflammatory responses and MAPKs:Porcine intestinal epithelial cell line (IPEC-1) formed an epithelial monolayer and the microvillus structures after12days incubation, These results have indicated that IPEC-1cells have successfully differentiated. We introduced the differentiated IPEC-1cells and observed the significant up-regulation expression of pro-inflammatory mediators after ETEC treatment (108cfu/ml), The probiotic Ba could effectively down-regulate IL-6, IL-la and TNF-a production in the differentiated IPEC-1cells with ETEC treatment, These data indicated that Ba inhibited ETEC-induced pro-inflammatory responses in the differentiated IPEC-1cells. Furthermore, the probiotic Ba attenuated ETEC-induced activation of the MAPKs pathways in differentiated IPEC-1cells. The activation level of the ERK1/2, JNK and p38was significantly decreased in the differentiated IPEC-1cells pre-incubated with Ba for24h. In sum, the probiotic Ba could inhibit ETEC-induced pro-inflammatory responses by suppression of MAPKs signaling pathways in intestinal epithelial cells.
(2) Probiotic Bacillus amyloliquefaciens SC06mediated M1macrophage polarization in bone marrow-derived macrophages:Oral administration of Bacillus amyloliquefaciens SC06could decrease bacterial translocation in C57BL/6mice. Furthermore, dramatically increase in the percentage and number of macrophages were observed in the spleen of Ba-treated mice compared with the control and0.85%NaCl group (P<0.05). In contrast, there have been no statistically changes in the splenic CD4+T CD8+T and B cells. Meanwhile, no dramatically changes of IgG and IgM levels were found in intestinal mucosa among the groups. We were interested to know whether probiotic Ba could induce macrophages polarization. Real-time fluorescence PCR analysis demonstrated that the expression of IL-1β, iNOS, TNF-α and IL-6genes for M1macrophages was significantly increased at1.5h after probiotic Ba treatments compared to the probiotic Ba-free treatment (P<0.01), whereas the expression of M2macrophage marker genes (Arg1, Fizz1, MR, Ym1) was decreased (P<0.05). Furthermore, the phagocytic activity was dramatically increased in the Ba-treated BMDMs using a FITC-dextran endocytosis assay. These data indicated that probiotic Ba facilitated polarization of M1macrophages and enhanced its phagocytic capacity. Moreover, the Ba also mediated the autophagy in bone marrow-derived macrophages. The results provided the new insight that how probiotic Ba reduce the diarrhea and clear intracellular pathogens in weaned piglets.
(3) The effects of dietary supplemented Ba replacement with kitasamycin on growth performance and gut flora in the fattening pigs:Adding Ba to swine diets increased ADG (P<0.05) and ADFI (P<0.05) compared to control fed pigs. Compared with the control fed pigs, villus height was significantly increased (P<0.05), crypt depth ratio (V:C) have no significant change (P<0.05). Roche454sequencing data showed that the dominant bacteria of the cecum were the Firmicutes and Bacteroides in fattening pigs. Bacteroides dominated a large portion in the cecum and the Fusobacterium accounted for a small proportion. Cecum of the fattening pigs main contained the Firmicutes, Bacillus, Clostridium and Actinobacteria. Bacillus accounted for the major proportion of Firmicutes in the antibiotic group, antibiotics+Ba and Ba treatment group were67.98%,82.13%and84.48%and the proportion of the Erysipelotrichi holded13.9%,6.77%and6.15%, respectively. Taken together, the Ba could promote growth performance and improve the intestine health, as well as regulate microbial ecological balance in the fattening pigs.
(4) Dietary supplemented Ba alleviated fed diets containing kitasamycin inducing liver injury in fattening pigs:Most of serum biochemical parameters were not different in the three dietary treatments and were within the normal physiologic concentrations. Interestingly, pigs fed diets containing kitasamycon with no Ba had higher glutamic pyruvic transaminase (ALT) and glutamic oxalacetic transaminease (AST) content than the other two treatments (P<0.05), especially the ALT43.8IU/L which was over the normal physiological range. Therefore, these data indicated that the Ba might prevent fed diets containing kitasamycin inducing liver damage. The most abnormality seen was damage to mitochondria and endoplasmic reticulum (ER) including the endoplasmic reticulum dilated and vesiculated, mitochondria swell, cristae vague in fed diets containing antibiotic kitasamycin. Dramatically increase in mitochondrial diameter was found in fed diets containing antibiotic kitasamycin compared with fed diets containing Ba (P<0.05). The average number of ER vacuoles per field in fed diets containing antibiotic kitasamycin was notably higher than that fed diet containing Ba groups (P<0.05). These results suggested that normal ER and mitochondria were restored when fattening pigs were fed with probiotic Ba-supplemented diet. Probiotic Ba may prevent fed diets containing kitasamycin induced-liver injury by attenuated ER and mitochondria damage.
The results provide the implications for elucidating the mechanism that the probiotic Ba regulates the immune response, and also supplying the technological and theoretical guidance for application of the probiotic Ba in livestock and feed industry.
引文
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