滇金丝猴肠道微生物四环素抗性基因和肠道环境特征

doi:10.16829/j.slxb.150671

摘要/Abstract

摘要：

野生动物肠道是微生物抗生素抗性基因 (Antibiotic resistance genes, ARGs) 的储存库，滇金丝猴 (Rhinopithecus bieti) 在动物展示区存在ARGs暴露的风险。本研究基于16S rRNA技术，测定展示区不同性别滇金丝猴的肠道微生物组成，利用定量聚合酶链反应 (quantitative polymerase chain reaction, qPCR) 技术检测其肠道微生物四环素类抗生素抗性基因 (Tetracycline antibiotic resistance genes, T-ARGs) 和可移动遗传元件 (Mobile genetic elements, MGEs) 丰度，并分析其肠道酶活性和营养物质含量特征；利用网络模型 (NetWork) 分析T-ARGs和MGEs的潜在宿主菌，简单相关关系分析肠道微生物T-ARGs和 MGEs的丰度与滇金丝猴肠道的微生态环境特征的关系。结果表明，滇金丝猴雌性和雄性肠道微生物T-ARGs和MGEs的绝对丰度差异不显著；雌性肠道中疣微菌门 (Verrucomicrobia) 和纤维杆菌门 (Fibrobacteres) 相对丰度显著低于雄性，而纤维素酶和蛋白酶活力显著高于雄性。滇金丝猴肠道微生物的T-ARGs可作为其展示区健康风险的指示因子，展示区的滇金丝猴可能存在3个风险：(1) 条件致病菌是T-ARGs的潜在宿主菌，利用四环素类抗生素对展示区的滇金丝猴进行疾病治疗时，该致病菌可能具有产生耐药性的风险；(2) 脂肪酶活力、蛋白酶活力和纤维素酶活力能够提高MGEs的转移能力，说明维持展示区滇金丝猴的肠道消化能力的管理方式可能与降低T-ARGs转移能力的目标相悖；(3) T-ARGs抑制滇金丝猴对蛋白质的消化和氨基酸的吸收。建议对展示区滇金丝猴的ARGs污染源加以控制，以保障滇金丝猴肠道微生态环境的稳定和降低致病菌的耐药性，与雌性滇金丝猴相比，雄性滇金丝猴个体的健康状况更应该重视。

关键词: 干扰, 滇金丝猴, 肠道微生物, 抗生素抗性基因, 转移风险

Abstract:

The gut of wild animals has been shown to be a reservoir for microorganisms that contain antibiotic resistance genes (ARGs). Yunnan snub-nosed monkeys (Rhinopithecus bieti) are at particular risk for ARGs. The intestinal microbial composition of female and male Yunnan snub-nosed monkeys was determined using 16S rRNA gene sequencing. Tetracycline antibiotic resistance genes (T-ARGs) and mobile genetic elements (MGEs) were detected by quantitative polymerase chain reaction (qPCR), and intestinal enzyme activities and nutrient contents of the monkeys intestinal microorganisms were analyzed. A network model was used to analyze the potential host bacteria of T-ARGs and MGEs. A simple correlative relationship was used to analyze the relationship between the abundances of T-ARGs and MGEs and the intestinal micro?ecological environment. The results showed no significant difference in the absolute abundance of T-ARGs and MGEs between female and male monkey groups. The relative abundance of Verrucomicrobia and Fibrobacteres in the intestines of the female group were significantly lower than those of the male group, while the activities of cellulase and protease content were significantly higher than those of the male group. T-ARGs could be used as an indicator of management risks of Yunnan snub-nosed monkeys in the exhibition area, who may face three potential risks. First, opportunistic pathogens in Yunnan snub-nosed monkeys are potential hosts of T-ARGs and there may be a risk of drug resistance in Yunnan snub-nosed monkeys treated with tetracycline antibiotics. Second, lipase activity, protease activity, and cellulase activity can improve the transfer ability of MGEs, which suggests that the method of maintaining intestinal digestive ability of Yunnan snub-nosed monkeys in the exhibition area may be contrary to the goal of reducing the transfer ability of T-ARGs. Third, T-ARGs may inhibit proteins being digested and amino acids being absorbed. It is suggested to control the sources of T-ARGs exposure in the exhibition area, in order to ensure the stability of the intestinal micro-ecological environment and to reduce the drug resistance of pathogenic bacteria. Furthermore, extra attention should be paid to the individual health of male Yunnan snub-nosed monkeys.

Key words: Interference, Yunnan snub-nosed monkey, Intestinal microorganism, Antibiotic resistance gene, Transfer risk

中图分类号:

Q931

邹书珍, 罗亚, 程鸣, 王凡, 黎大勇, 康迪, 唐贇. 滇金丝猴肠道微生物四环素抗性基因和肠道环境特征[J]. 兽类学报, 2023, 43(3): 304-314.

Shuzhen ZOU, Ya LUO, Ming CHENG, Fan WANG, Dayong LI, Di KANG, Yun TANG. Characteristics of tetracycline antibiotic resistance genes in intestinal microorganisms and intestinal environment of Yunnan snub-nosed monkeys[J]. ACTA THERIOLOGICA SINICA, 2023, 43(3): 304-314.

图/表 6

表 1 本研究中使用的引物列表

Table 1 Primer list used in this study

基因名称 Gene name	上游引物 Forward primer	下游引物 Reverse primer
tet （B）	AGTGCGCTTTGGATGCTGTA	AGCCCCAGTAGCTCCTGTGA
tet （C）	CATATCGCAATACATGCGAAAAA	AAAGCCGCGGTAAATAGCAA
tet （O）	ATGTGGATACTACAACGCATGAGATT	TGCCTCCACATGATATTTTTCCT
tet （X）	AAATTTGTTACCGACACGGAAGTT	CATAGCTGAAAAAATCCAGGACAGTT
tet （A）	GCTGTTTGTTCTGCCGGAAA	GGTTAAGTTCCTTGAACGCAAACT
tet （D）	TGCCGCGTTTGATTACACA	CACCAGTGATCCCGGAGATAA
tet （E）	TTGGCGCTGTATGCAATGAT	CGACGACCTATGCGATCTGA
tet （M）	CATCATAGACACGCCAGGACATAT	CGCCATCTTTTGCAGAAATCA
intI	GGCATCCAAGCAGCAAG	AAGCAGACTTGACCTGA
intI2	CAC GGA TAT GCG ACA AAA AGG T	GTA GCA AAC GAG TGA CGA AAT G
intI1	CGAACGAGTGGCGGAGGGTG	TACCCGAGAGCTTGGCACCCA
IS613	AGGTTCGGACTCAATGCAACA	TTCAGCACATACCGCCTTGAT
tnpA-01	CATCATCGGACGGACAGAATT	GTCGGAGATGTGGGTGTAGAAAGT
tnpA-02	GGGCGGGTCGATTGAAA	GTGGGCGGGATCTGCTT
tnpA-03	AATTGATGCGGACGGCTTAA	TCACCAAACTGTTTATGGAGTCGTT

图1 滇金丝猴肠道微生物T-ARGs和MGEs的绝对丰度. A：基因修饰机制的T-ARGs；B：核糖体保护机制的T-ARGs；C：外泵机制的T-ARGs；D：MGEs基因. 相同小写字母表示雌性和雄性间差异不显著 (P ≥ 0. 05). F1 ~ F4表示4只雌性个体；M1 ~ M4表示4只雄性个体

Fig.1 Absolute abundances of T-ARGs and MGEs in intestinal microorganisms of R.bieti. A: T-ARGs of modification mechanism; B: T-ARGs of ribosomal protection mechanism; C: T-ARGs of expump mechanism; D: MGEs. The same lowercase indicates there are no significant difference between female and male (P ≥ 0. 05). F1 to F4 are the 4 female R.bieti individuals and M1 to M4 are the 4 males R.bieti individuals

图2 滇金丝猴肠道微生物的相对丰度.A：门水平微生物；B：属水平微生物. *表示雌性和雄性间差异显著 (P < 0.05). F1 ~ F4表示4只雌性个体；M1 ~ M4表示4只雄性个体

Fig. 2 Relative abundances of intestinal microorganisms of R.bieti. A: intestinal microorganisms in phylum level; B: intestinal microorganisms ingenus level. * indicates there are significant difference between female and male (P < 0. 05). F1 to F4 are the 4 female R.bieti individuals and M1 to M4 are the 4 males R.bieti individuals

图3 滇金丝猴肠道的酶活力和营养物质含量. 图中不同小写字母表示雌性和雄性间差异显著 (P < 0.05). F1 ~ F4表示4只雌性个体；M1 ~ M4表示4只雄性个体

Fig. 3 Enzyme activity and nutrient content in intestine of R.bieti. The different lowercase indicates there are significant difference between female and male (P < 0.05). F1 to F4 are the 4 female R.bieti individuals and M1 to M4 are the 4 males R.bieti individuals

图4 滇金丝猴肠道中T-ARGs和MGEs与微生物的Network网络分析. 红色线段表示显著正相关 (P < 0.05)，绿色线段表示显著负相关 (P < 0.05)，蓝色节点表示微生物种类，黄色节点表示T-ARGs，绿色节点表示MGEs，节点的大小表示与其他物种的关联关系的多少，相关的因素数量越多，点的半径越大

Fig. 4 Network analysis on T-ARGs, MGEs and microorganisms in the intestine of R.bieti. The red line segments indicate significant positive correlation (P < 0.05), while the green line segments indicate significant negative correlation (P < 0.05). The blue nodes represent microbial species, the yellow nodes represent the T-ARGs and the green nodes represent the MGEs. The size of the dot indicates the number of associations with other species, and the larger the number of related factors, the larger the radius of the dots

表2 滇金丝猴肠道T-ARGS和MGEs与环境特征之间的相关系数

Table 2 Correlation coefficients between T-ARGs and MGEs in intestinal microorganisms and environmental characteristics in R.bieti

指标 Indices	核糖体保护机制的T-ARGs T-ARGs of protecting ribosomes	外泵机制的T-ARGs T-ARGs of efflux pump	MGEs	淀粉酶活力 Amylase activity	脂肪酶活力 Lipase activity	蛋白酶活力 Protease activity	纤维素酶活力 Cellulose activity	蛋白质含量 Protein content	氨基酸含量 amino acids contents
基因修饰机制的T-ARGs T-ARGs of gene modification	-0.180	0.151	0.212	0.111	0.327	0.482	0.379	0.064	0.162
核糖体保护机制的T-ARGs T-ARGs of protecting ribosomes		0.336	-0.149	-0.079	-0.215	-0.101	-0.092	-0.452	-0.574
外泵机制的T-ARGs T-ARGs of efflux pump			-0.439	0.461	-0.445	-0.323	-0.378	-0.641^*	-0.710^*
MGEs				0.210	0.895^**	0.917^**	0.976^**	0.637^*	0.646^*
淀粉酶活力 Amylase activity					0.395	0.201	0.147	-0.374	-0.251
脂肪酶活力 Lipase activity						0.899^**	0.871^**	0.474	0.612
蛋白酶活力 Protease activity							0.966^**	0.512	0.577
纤维素酶活力 Cellulose activity								0.600	0.608
蛋白质含量 Protein content									0.953^**

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