兽类学报 ›› 2022, Vol. 42 ›› Issue (4): 420-431.DOI: 10.16829/j.slxb.150622
收稿日期:
2021-10-17
接受日期:
2022-04-06
出版日期:
2022-07-30
发布日期:
2022-07-22
通讯作者:
刘新宇
作者简介:
毛敏 (1997- ),女,硕士研究生,主要从事动物生理生态学研究.
基金资助:
Min MAO, Ming YANG, Xinyu LIU()
Received:
2021-10-17
Accepted:
2022-04-06
Online:
2022-07-30
Published:
2022-07-22
Contact:
Xinyu LIU
摘要:
冬眠哺乳动物的肠道微生物会发生季节性变化,同时在冬眠期间动物处于禁食状态,对肠道微生物的多样性和组成也产生影响。本研究通过16S rRNA基因高通量测序分析达乌尔黄鼠育肥阶段 (起始育肥期、快速育肥期、育肥完成期) 和冬眠阶段 (冬眠早期、冬眠晚期、出眠期) 共6个时期盲肠菌群的多样性、组成和功能,并通过冗余分析 (RDA) 探究其生理特征与菌群组成和功能之间的关系,揭示达乌尔黄鼠盲肠菌群的季节性变化。菌群组成的分析显示达乌尔黄鼠盲肠菌群主要由厚壁菌门 (Firmicutes)、拟杆菌门 (Bacteroidetes) 和疣微菌门 (Verrucomicrobia) 组成。与其他时期相比,冬眠早期厚壁菌门的相对丰度减少,拟杆菌门和疣微菌门的相对丰度增加。在Alpha多样性中,起始育肥期、快速育肥期和冬眠早期的Chao1和ACE指数显著低于出眠期,育肥完成期的Simpson指数显著低于快速育肥期 (P < 0.05) 。通过加权和非加权的UniFrac距离矩阵的主坐标分析发现盲肠菌群均显示出了明显的季节性聚类。PICRUSt分析中,丁酸代谢等代谢通路在育肥阶段富集,冬眠阶段集中在氮代谢等相关通路中。RDA分析显示达乌尔黄鼠不同时期的生理特征与其盲肠菌群的组成和功能显著相关。本研究表明,冬眠使达乌尔黄鼠盲肠菌群的多样性和相对丰度发生改变,盲肠菌群组成和功能的变化调节了达乌尔黄鼠的生理代谢,使达乌尔黄鼠适应季节性的环境变化。
中图分类号:
毛敏, 杨明, 刘新宇. 冬眠对达乌尔黄鼠盲肠菌群的影响[J]. 兽类学报, 2022, 42(4): 420-431.
Min MAO, Ming YANG, Xinyu LIU. Effects of hibernation on cecal microbiota in Daurian ground squirrel[J]. ACTA THERIOLOGICA SINICA, 2022, 42(4): 420-431.
分组 Group | 观察到的OTU数 Observed species | Chao1指数 Chao1 index | ACE指数 ACE index | Shannon指数 Shannon index | Simpson指数 Simpson index |
---|---|---|---|---|---|
起始育肥期组IF | 533.13 ± 23.42a | 588.65 ± 26.17b | 584.73 ± 27.29b | 6.22 ± 0.29a | 0.94 ± 0.02ab |
快速育肥期组RF | 531.00 ± 41.45a | 591.35 ± 42.94b | 583.64 ± 42.94b | 6.19 ± 0.29a | 0.93 ± 0.02b |
育肥完成期组FF | 585.29 ± 15.33a | 665.68 ± 12.83ab | 647.96 ± 15.07ab | 6.87 ± 0.10a | 0.98 ± 0.00a |
冬眠早期组EH | 527.13 ± 35.05a | 603.06 ± 42.69b | 588.95 ± 42.09b | 6.56 ± 0.13a | 0.97 ± 0.00ab |
冬眠晚期组LH | 577.00 ± 23.35a | 666.01 ± 29.67ab | 654.41 ± 28.10ab | 6.83 ± 0.11a | 0.98 ± 0.00ab |
出眠期组A | 640.38 ± 29.84a | 762.99 ± 37.36a | 752.93 ± 34.15a | 6.78 ± 0.13a | 0.97 ± 0.00ab |
表1 不同时期达乌尔黄鼠盲肠菌群的Alpha多样性指数表
Table 1 Index table of Alpha diversity of cecal microbiota of Daurian ground squirrel in different periods
分组 Group | 观察到的OTU数 Observed species | Chao1指数 Chao1 index | ACE指数 ACE index | Shannon指数 Shannon index | Simpson指数 Simpson index |
---|---|---|---|---|---|
起始育肥期组IF | 533.13 ± 23.42a | 588.65 ± 26.17b | 584.73 ± 27.29b | 6.22 ± 0.29a | 0.94 ± 0.02ab |
快速育肥期组RF | 531.00 ± 41.45a | 591.35 ± 42.94b | 583.64 ± 42.94b | 6.19 ± 0.29a | 0.93 ± 0.02b |
育肥完成期组FF | 585.29 ± 15.33a | 665.68 ± 12.83ab | 647.96 ± 15.07ab | 6.87 ± 0.10a | 0.98 ± 0.00a |
冬眠早期组EH | 527.13 ± 35.05a | 603.06 ± 42.69b | 588.95 ± 42.09b | 6.56 ± 0.13a | 0.97 ± 0.00ab |
冬眠晚期组LH | 577.00 ± 23.35a | 666.01 ± 29.67ab | 654.41 ± 28.10ab | 6.83 ± 0.11a | 0.98 ± 0.00ab |
出眠期组A | 640.38 ± 29.84a | 762.99 ± 37.36a | 752.93 ± 34.15a | 6.78 ± 0.13a | 0.97 ± 0.00ab |
图1 不同时期达乌尔黄鼠观察到的OTU数的稀释曲线. 图中的每一个样本用不同的曲线代表,不同的颜色表示不同的分组;随着样本序列数的增加,OTU的数量也在增加;最终,曲线开始趋于平缓,说明所有样品的测序数量合理,能够涵盖样品中绝大多数微生物物种信息. IF:起始育肥期组;RF:快速育肥期组;FF:育肥完成期组;EH:冬眠早期组;LH:冬眠晚期组;A:出眠期组;图2 ~ 5同
Fig. 1 The rarefaction curves of observed species of Daurian ground squirrel in different periods. Each sample in the figure is represented by a different curve, and different colors indicate different groupings. With the increase of sequence per sample, the observed species also increases. Finally, the curve began to plateau, indicating that the sequencing quantity of all samples was reasonable, and could cover the information of the vast majority of microbial species in the samples. IF: Initial fattening group; RF: Rapid fattening group; FF: Finished fattening group; EH: Early hibernation group; LH: Late hibernation group; A: Arousal group; the same to figure 2 - 5
图2 不同时期达乌尔黄鼠盲肠菌群基于加权 (A) 和非加权 (B) UniFrac距离矩阵的主坐标分析 (PCoA). 横坐标和纵坐标表示选定的两个主坐标轴;百分比表示主坐标轴对样本组成差异的解释度;刻度是相对距离,无实际意义;不同颜色的置信椭圆代表不同的分组;不同颜色或形状的点代表不同分组的样本,两样本的点越接近,表明两样本盲肠菌群结构组成越相似
Fig. 2 Principal coordinate analysis (PCoA) of the weighted (A) and unweighted (B) UniFrac distance matrix compared with the cecal microbiota of Daurian ground squirrel in different periods. The abscissa and ordinate represent are the two selected main axes, and the percentage represents the contribution of the main axis to explain the difference in sample composition. The scale is relative distance has no practical significance. Confidence ellipses of different colors represent different groups and the dots of different colors and shapes represent samples of different groups. The closer the points of the two samples are, the more similar the cecal microbiota of the two samples is proved
图3 达乌尔黄鼠盲肠菌群在门 (A)、科 (B) 和属 (C) 水平的相对丰度组成. 不同的物种用不同颜色表示,柱子的长短代表该物种所占比例的大小;Others代表其他细菌分类以及未注释出来的细菌分类;星号表示科水平中未分类的属
Fig. 3 Composition of relative abundance of cecal microbiota in Daurian ground squirrel at phylum (A), family (B) and genus (C) levels. Different species are indicated in different colors, and the length of the column represents the proportion. Others represent other bacterial taxa and undefined bacterial taxa. Asterisks indicate unclassified genera at the family level
类群 Taxa | 起始育肥期组IF | 快速育肥期组RF | 育肥完成期组FF | 冬眠早期组EH | 冬眠晚期组LH | 出眠期组 A | |
---|---|---|---|---|---|---|---|
门Phylum | 厚壁菌门 Firmicutes | 0.7794 ± 0.0236a | 0.7448 ± 0.0291ab | 0.7629 ± 0.0180ab | 0.5783 ± 0.0347b | 0.7519 ± 0.0287a | 0.8225 ± 0.0232a |
拟杆菌门 Bacteroidetes | 0.1863 ± 0.0242b | 0.2207 ± 0.0289ab | 0.2049 ± 0.0167b | 0.3357 ± 0.0255a | 0.1810 ± 0.0300b | 0.1512 ± 0.0254b | |
疣微菌门 Verrucomicrobia | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
Epsilonbacteraeota | 0.0000 ± 0.0000ab | 0.0001 ± 0.0001a | 0.0004 ± 0.0003ab | 0.0001 ± 0.0000ab | 0.0000 ± 0.0000b | 0.0000 ± 0.0000ab | |
科Family | 瘤胃菌科 Ruminococcaceae | 0.2395 ± 0.0276ab | 0.1799 ± 0.0217ab | 0.3185 ± 0.0303a | 0.1711 ± 0.0209b | 0.1982 ± 0.0312ab | 0.2261 ± 0.0263ab |
乳杆菌科 Lactobacillaceae | 0.1923 ± 0.0686a | 0.1052 ± 0.0405a | 0.0283 ± 0.0121ab | 0.0009 ± 0.0003b | 0.0009 ± 0.0003b | 0.0471 ± 0.0277ab | |
拟杆菌科 Bacteroidaceae | 0.0361 ± 0.0110b | 0.0544 ± 0.0133ab | 0.0477 ± 0.0112ab | 0.1126 ± 0.0144a | 0.0395 ± 0.0156b | 0.0226 ± 0.0053b | |
艾克曼氏菌科 Akkermansiaceae | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
Family | 0.0242 ± 0.0036ab | 0.0232 ± 0.0019ab | 0.0317 ± 0.0038a | 0.0165 ± 0.0033b | 0.0282 ± 0.0046ab | 0.0271 ± 0.0066ab | |
消化球菌科 Peptococcaceae | 0.0047 ± 0.0015b | 0.0019 ± 0.0004b | 0.0052 ± 0.0013ab | 0.0126 ± 0.0040ab | 0.0187 ± 0.0031a | 0.0111 ± 0.0028ab | |
韦荣球菌科 Erysipelotrichaceae | 0.0035 ± 0.0009b | 0.0049 ± 0.0013ab | 0.0054 ± 0.0018ab | 0.0093 ± 0.0017ab | 0.0098 ± 0.0009a | 0.0198 ± 0.0072a | |
氨基酸球菌科 Acidaminococcaceae | 0.0014 ± 0.0013ab | 0.0205 ± 0.0072a | 0.0078 ± 0.0049ab | 0.0028 ± 0.0028ab | 0.0007 ± 0.0007b | 0.0024 ± 0.0017ab | |
属Genus | 乳杆菌属 Lactobacillus | 0.1923 ± 0.0686a | 0.1052 ± 0.0405a | 0.0283 ± 0.0121ab | 0.0009 ± 0.0003b | 0.0009 ± 0.0003b | 0.0471 ± 0.0277ab |
拟杆菌属 Bacteroides | 0.0361 ± 0.0110b | 0.0544 ± 0.0133ab | 0.0477 ± 0.0112ab | 0.1126 ± 0.0144a | 0.0395 ± 0.0156b | 0.0226 ± 0.0053b | |
Marvinbryantia | 0.0137 ± 0.0043b | 0.0159 ± 0.0045b | 0.0203 ± 0.0115b | 0.0583 ± 0.0151ab | 0.0917 ± 0.0132a | 0.0341 ± 0.0082ab | |
[Eubacterium] coprostanoligenes group | 0.0391 ± 0.0103ab | 0.0086 ± 0.0053b | 0.0453 ± 0.0120a | 0.0212 ± 0.0041ab | 0.0252 ± 0.0049ab | 0.0369 ± 0.0108ab | |
艾克曼菌属 Akkermansia | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
瘤胃球菌属1 Ruminococcus 1 | 0.0321 ± 0.0133ab | 0.0191 ± 0.0073ab | 0.0430 ± 0.0135a | 0.0096 ±0.0052ab | 0.0027 ± 0.0006b | 0.0321 ± 0.0123a | |
脱硫弧菌属 Desulfovibrio | 0.0037 ± 0.0016b | 0.0036 ± 0.0010ab | 0.0054 ± 0.0024ab | 0.0105 ±0.0014a | 0.0101 ± 0.0027ab | 0.0053 ± 0.0011ab |
表2 在门、科和属水平中达乌尔黄鼠优势菌群相对丰度的差异比较
Table 2 Comparison of relative abundance of dominant microbiota of Daurian ground squirrel at phylum, family and genus levels
类群 Taxa | 起始育肥期组IF | 快速育肥期组RF | 育肥完成期组FF | 冬眠早期组EH | 冬眠晚期组LH | 出眠期组 A | |
---|---|---|---|---|---|---|---|
门Phylum | 厚壁菌门 Firmicutes | 0.7794 ± 0.0236a | 0.7448 ± 0.0291ab | 0.7629 ± 0.0180ab | 0.5783 ± 0.0347b | 0.7519 ± 0.0287a | 0.8225 ± 0.0232a |
拟杆菌门 Bacteroidetes | 0.1863 ± 0.0242b | 0.2207 ± 0.0289ab | 0.2049 ± 0.0167b | 0.3357 ± 0.0255a | 0.1810 ± 0.0300b | 0.1512 ± 0.0254b | |
疣微菌门 Verrucomicrobia | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
Epsilonbacteraeota | 0.0000 ± 0.0000ab | 0.0001 ± 0.0001a | 0.0004 ± 0.0003ab | 0.0001 ± 0.0000ab | 0.0000 ± 0.0000b | 0.0000 ± 0.0000ab | |
科Family | 瘤胃菌科 Ruminococcaceae | 0.2395 ± 0.0276ab | 0.1799 ± 0.0217ab | 0.3185 ± 0.0303a | 0.1711 ± 0.0209b | 0.1982 ± 0.0312ab | 0.2261 ± 0.0263ab |
乳杆菌科 Lactobacillaceae | 0.1923 ± 0.0686a | 0.1052 ± 0.0405a | 0.0283 ± 0.0121ab | 0.0009 ± 0.0003b | 0.0009 ± 0.0003b | 0.0471 ± 0.0277ab | |
拟杆菌科 Bacteroidaceae | 0.0361 ± 0.0110b | 0.0544 ± 0.0133ab | 0.0477 ± 0.0112ab | 0.1126 ± 0.0144a | 0.0395 ± 0.0156b | 0.0226 ± 0.0053b | |
艾克曼氏菌科 Akkermansiaceae | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
Family | 0.0242 ± 0.0036ab | 0.0232 ± 0.0019ab | 0.0317 ± 0.0038a | 0.0165 ± 0.0033b | 0.0282 ± 0.0046ab | 0.0271 ± 0.0066ab | |
消化球菌科 Peptococcaceae | 0.0047 ± 0.0015b | 0.0019 ± 0.0004b | 0.0052 ± 0.0013ab | 0.0126 ± 0.0040ab | 0.0187 ± 0.0031a | 0.0111 ± 0.0028ab | |
韦荣球菌科 Erysipelotrichaceae | 0.0035 ± 0.0009b | 0.0049 ± 0.0013ab | 0.0054 ± 0.0018ab | 0.0093 ± 0.0017ab | 0.0098 ± 0.0009a | 0.0198 ± 0.0072a | |
氨基酸球菌科 Acidaminococcaceae | 0.0014 ± 0.0013ab | 0.0205 ± 0.0072a | 0.0078 ± 0.0049ab | 0.0028 ± 0.0028ab | 0.0007 ± 0.0007b | 0.0024 ± 0.0017ab | |
属Genus | 乳杆菌属 Lactobacillus | 0.1923 ± 0.0686a | 0.1052 ± 0.0405a | 0.0283 ± 0.0121ab | 0.0009 ± 0.0003b | 0.0009 ± 0.0003b | 0.0471 ± 0.0277ab |
拟杆菌属 Bacteroides | 0.0361 ± 0.0110b | 0.0544 ± 0.0133ab | 0.0477 ± 0.0112ab | 0.1126 ± 0.0144a | 0.0395 ± 0.0156b | 0.0226 ± 0.0053b | |
Marvinbryantia | 0.0137 ± 0.0043b | 0.0159 ± 0.0045b | 0.0203 ± 0.0115b | 0.0583 ± 0.0151ab | 0.0917 ± 0.0132a | 0.0341 ± 0.0082ab | |
[Eubacterium] coprostanoligenes group | 0.0391 ± 0.0103ab | 0.0086 ± 0.0053b | 0.0453 ± 0.0120a | 0.0212 ± 0.0041ab | 0.0252 ± 0.0049ab | 0.0369 ± 0.0108ab | |
艾克曼菌属 Akkermansia | 0.0142 ± 0.0042abc | 0.0090 ± 0.0051bc | 0.0079 ± 0.0019abc | 0.0658 ± 0.0274a | 0.0474 ± 0.0126ab | 0.0048 ± 0.0012c | |
瘤胃球菌属1 Ruminococcus 1 | 0.0321 ± 0.0133ab | 0.0191 ± 0.0073ab | 0.0430 ± 0.0135a | 0.0096 ±0.0052ab | 0.0027 ± 0.0006b | 0.0321 ± 0.0123a | |
脱硫弧菌属 Desulfovibrio | 0.0037 ± 0.0016b | 0.0036 ± 0.0010ab | 0.0054 ± 0.0024ab | 0.0105 ±0.0014a | 0.0101 ± 0.0027ab | 0.0053 ± 0.0011ab |
图4 LEfSe分析KEGG三个层级中达乌尔黄鼠盲肠菌群显著富集的功能. LDA > 2认为有差异. IF:起始育肥期组;RF:快速育肥期组;FF:育肥完成期组;EH:冬眠早期组;LH:冬眠晚期组
Fig. 4 LEfSe analysis of the function of significant enrichment of cecal microbiota of Daurian ground squirrel at three KEGG levels. LDA > 2 is considered to be different. IF: Initial fattening group; RF: Rapid fattening group; FF: Finished fattening group; EH: Early hibernation group; LH: Late hibernation group
图5 达乌尔黄鼠不同时期的生理特征与其盲肠菌群组成 (A) 和功能 (B) 的冗余分析. 红色箭头射线代表不同时期达乌尔黄鼠的生理特征;蓝色箭头射线分别代表盲肠菌群的组成和功能;不同颜色的点代表不同的分组;射线与射线之间的关系由夹角表示,锐角代表正相关,钝角代表负相关
Fig. 5 RDA analysis of physiological characteristics of Daurian ground squirrel in different periods and the composition (A) and function (B) of cecal microbiota. The red arrow rays represent the physiological characteristics of Daurian ground squirrel in different periods. The blue arrow rays represent the composition and function of cecal microbiota. Dots of different colors represent samples of different groups. The relationship between rays is indicated by the included angle, with acute angle representing positive correlation and obtuse angle representing negative correlation
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