Characteristics of tetracycline antibiotic resistance genes in intestinal microorganisms and intestinal environment of Yunnan snub-nosed monkeys
Received date: 2022-03-24
Accepted date: 2022-10-19
Online published: 2023-05-18
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.
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 . DOI: 10.16829/j.slxb.150671
| null | Bao S D. 2000. Soil Agrochemical Analysis. Beijing: China Agriculture Press. (in Chinese) |
| null | Cai K K, Huang Z W, Ye D J, Sun C T. 2011. Regulation of intestinal flora of probiotics and its immune function. China Feed, 18: 34-37. (in Chinese) |
| null | Cheng M. 2021. Study on intestinal microbial diversity of Yunnan snub?nosed monkey and Sichuan snub?nosed monkey. Master thesis. Nanchong: China West Normal University. (in Chinese) |
| null | Chopra I. 2001. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistanc. Microbiology & Molecular Biology Reviews, 65 (2): 232-260. |
| null | Cristina M, Lin C, Marina C, Massimo M, Luisa M H, Louise K, Mohney R P, Steves C J, Spector T D, Kuo C F. 2018. Gut microbial diversity is associated with lower arterial stiffness in women. European Heart Journal, 39 (25): 2390-2397. |
| null | Ding J R, Zhang Q X, Liu X M, Wang G, Tian W F, Zhang H, Chen W. 2012. Quantity of desulfovibrios and analysis of intestinal microbiota diversity in health and intestinal disease people in Wuxi, Jiangsu Province. Acta Microbiologica Sinica, 8 (52): 1033-1039. (in Chinese) |
| null | Fahad S M, Zhu C X, Geng B, Raza A H, Song T T, Li H. 2021. The fate of antibiotic resistance genes in cow manure composting: shaped by temperature-controlled composting stages. Bioresource Technology, 320 (PB): 124403. |
| null | Fan X T, Li H, Chen Q L, Zhang Y S, Ye J, Zhu Y G, Su J Q. 2019. Fate of antibiotic resistant pseudomonas putida and broad host range plasmid in natural soil microcosms. Frontiers in Microbiology, 1 (10): 294. |
| null | Gou C L, Wang Y Q, Zhang X Q, Lou Y J, Gao Y H. 2017. Effects of high?temperature composting on tetracyclines and tetracycline resistance genes in swine manure. Acta Scientiae Circumstantiae, 37 (4): 1454-1460. (in Chinese) |
| null | Grigor’Eva I N. 2021. Personalized medicine review gallstone disease, obesity and the firmicutes/bacteroidetes ratio as a possible biomarker of gut dysbiosis. Journal of Personalized Medicine, 11 (1): 13. |
| null | Guo A Y, Gu J, Wang X J, Zhang R R, Yin Y N, Sun W, Tuo X X, Zhang L. 2017. Effects of superabsorbent polymers on the abundances of antibiotic resistance genes, mobile genetic elements, and the bacterial community during swine manure composting. Bioresource Technology, 244 (1): 658-663. |
| null | Guo C, Xiang Z F, Ren B P, Li M. 2011. All-male unit’s spatial structure and its function of a moving troop in Rhinopithecus bieti . Journal of Central South University of Forestry & Technology, 31 (7): 136-139. (in Chinese) |
| null | Guo S T. 2004. Studies on foraging behaviorand of home range of the Sichuan golden monkey(Rhinopithecus roxellana). Master thesis. Xi’an: North West China University. (in Chinese) |
| null | Kintses B, Méhi O, Ari E, Számel M, ádám G, Jangir P K, Nagy I, Pál F, Fekete G, Teng?lics R, Nyergesá, Likó I, Bálint A, Molnár T, Bálint B, Vásárhelyi B M, Bustamante M, Papp B, Pál C. 2019. Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota. Nature Microbiology, 4: 447-458. |
| null | Li W W, Li L, Wu G S, Zhang Y, Dai Y C, Zhou Y. 2016. Impact evaluation on the Yunnan snub?nosed monkey’s habitat in terms of landscape connectivity by agricultural land with consideration at different scale scenarios. Acta Ecologica Sinica, 36 (24): 8136-8144. (in Chinese) |
| null | Li Z. 2021. Effect of standardized grape powder consumption on the gut microbiome of healthy subjects: a pilot study. Nutrients, 13 (11): 3965. |
| null | Liu H X, Clarissa A R, Dandekar S. 2016. Functional analysis of the relationship between intestinal microbiota and the expression of hepatic genes and pathways during the course of liver regeneration. Journal of Hepatology, 64 (3): 641-650. |
| null | Luo Y, Tang Y, Zhang D, Cheng M, Zou S Z, Zhang J D, Kang D. 2020. Research on microbiota and enzyme activity characteristics in the feces of giant pandas of different ages. Acta Veterinaria et Zootechnica Sinica, 51 (4): 763-771. (in Chinese) |
| null | Maynard C, Fairbrother J M, Bekal S, Sanschagrin F, Levesque R C, Brousseau R, Masson L, Larivière S, Harel J. 2003. Antimicrobial resistance genes in enterotoxigenic Escherichia coliO 149: K91 isolates obtained overa 23-year period from pigs. Antimicrob. Agents Chemother, 47: 3214-3221. |
| null | Mazhar S H, Li X, Rashid A, Su J, Rensing C. 2021. Co?selection of antibiotic resistance genes, and mobile genetic elements in the presence of heavy metals in poultry farm environments. Science of the Total Environment, 755: 142702. |
| null | Pei R, Kim S C, Carlson K H, Pruden A. 2006. Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Research, 40 (12): 2427-2435. |
| null | Penczek P, Grassucci R A, Trieber C A, Connell S R, Taylor D E, Nierhaus K H, Frank J. 2001. Localization of the ribosomal protection protein Tet (O) on the ribosome and the mechanism of tetracycline resistance. Molecular Cell, 7 (5): 1037-1045. |
| null | Raubenheimer D, Righini N, Ji W H, Jay O, He S J, Wu F, Li F F, Li B G. 2018. Nutrient-specific compensation for seasonal cold stress in a free?ranging temperate colobine monkey. Functional Ecology, 32 (9): 2170-2180. |
| null | Su J Q, Bei W, Ouyang W Y, Huang F Y, Zhao Y, Xu H J, Zhu Y G. 2015. Antibiotic resistome and its association with bacterial communities during Sewage Sludge composting. Environmental Science & Technology, 49 (12): 7356-7363. |
| null | Tian Z, Zhang Y, Yang M. 2014. The origin,environmental distribution and potential application of tetracycline resistance gene-tet(X). Environmental Chemistry, 12: 2027-2037. |
| null | Tommi V, Aleksandar D K, Eva H, Heli S, Eric A F, Moran Y, Raivo K, Hera V, Timothy D A, H?m?l?inen A M, Aleksandr P, Vallo T, Raivo U, Sergei M, Natalya D, Jorma I, Suvi M V, Susanne J S, Jeffrey A P, Harri L, Curtis H, Dirk G, Thomas W C, Mikael K, Ramnik J X. 2016. Variation in microbiome lps immunogenicity contributes to autoimmunity in humans. Cell, 165 (4): 842-853. |
| null | Wang J, Ma Z B, Zeng Z L, Yang X W, Huang Y, Liu J H. 2017. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zoological Research, 38 (2): 55-80. |
| null | Waters J L, Ley R E. 2019. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biology, 17 (1): 1-11. |
| null | Wei F W. 2016. Research progress in conservation biology of endangered mammals in China. Acta Theriologica Sinica, 36 (3): 255-269. |
| null | Wen W, Xu X L, Ou W G. 2013. Study on the carrying status of antibiotic resistance genes in children intestinal flora. Journal of Zunyi Medical University, 36 (2): 113-115. (in Chinese) |
| null | Wo H H. 2014. Identification and screening of intestinal probiotics from golden monkey in Shennongjia. Master thesis. Wuhan: Huazhong Agricultural University. (in Chinese) |
| null | Xia W C, Liu G Q, Wang D L, Chen H, Zhu L F, Li D Y. 2022. Functional convergence of Yunnan snub?nosed monkey and bamboo-eating panda gut microbiomes revealing the driving by dietary flexibility on mammal gut microbiome. Computational and Structural Biotechnology Journal, 20: 695-699. |
| null | Xu C Y, Lv Z Q, Shen Y B, Liu D J, Fu Y L, Zhou L, Liu W W, Chen K, Ye H L, Xia X, Xia J J, Wang Y, Ke Y B, Shen J Z. 2020. Metagenomic insights into differences in environmental resistome profiles between integrated and monoculture aquaculture farms in China. Environment International, 144: 106005. |
| null | Yang B. 2017. Mechanism in grouth and rumen development alteration by early alfalfa supplementation in Hu Lambs.Ph.D thesis. Hangzhou: Zhejiang University. (in Chinese) |
| null | Yang W, Moore I F, Koteva K P, Bareich D C, Hughes D W, Wright G D.2004. TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. Journal of Biological Chemistry, 279 (50): 52346-52352. |
| null | Yu L, Huang Y M, Zhang Z G, Zhu X C, Li Y T, Li N, Li C B, Xu Z R, Yao X Q, Hu J Y, Wu H, Kuang W M. 2021. Regulation for data acquisition of gut microbiota for Rhinopithecus bieti . DB 53/T1057-2021.(in Chinese) |
| null | Yu X L. 2020. Study on differences in intestinal microbial community between male and female Yunnan snub?nosed monkeys (Rhinopithecus bieti) in different seasons. Master thesis. Nanchong: China West Normal University.(in Chinese) |
| null | Zang K L, Jiang Y, Sun Y, Chen Q L, Zhao L S, Zhao P, Cui W J, Ma X Y, Yan Y L. 2018. Relationship between microecologics and the expression of short chain fatty acids synthesis genes in key bacterial genera in the regulation of intestinal flora structure in populations with constipation and diarrhea. Food Science, 39 (5): 155-165. (in Chinese) |
| null | Zeng X Q. 2018. Research on glucocorticoid and behavior adaptation strategies of Yunnan snub?nosed monkey under Human behaviors. Master thesis. Nanchong: China West Normal University. (in Chinese) |
| null | Zhan J, Wei S. 2015. The distribution and eco-toxicology of tetracycfine in soil and water environment and its degradation: a review. Acta Ecologica Sinica, 35 (9): 2819-2825. (in Chinese) |
| null | Zhang H, Zhang Q, Song J, Zhang Z, Fang H. 2020. Tracking resistomes, virulence genes, and bacterial pathogens in long?term manure?amended greenhouse soils. Journal of Hazardous Materials, 396 (122618): 1-12. |
| null | Zhang Q, Wu Y, Wang J, Wu G, Long W, Xue Z, Wang L, Zhang X, Pang X, Zhao Y. 2016. Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium. Scientific Reports, 6 (27572): 1-11. |
| null | Zhao H, Sun R, Yu P, Alvarez P J. 2020. High levels of antibiotic resistance genes and opportunistic pathogenic bacteria indicators in urban wild bird feces. Environmental Pollution, 266 (2): 115200. |
| null | Zhou W R, Wang H N, Zhang A Y, Wu Q, Huang Y, Liu P, Tian L, Yang X, Liu L, Xia Q Q. 2007. Detection of sulfonamides-resistant genes in Salmonella and Escherichia coli isolated from pigs and wild animals. Veterinary Science in China, 37 (4): 287-290. (in Chinese) |
| null | Zhu D, Chen Q L, Ding J, Wang Y F, Cui H L, Zhu Y G. 2019. Antibiotic resistance genes in the soil ecosystem and planetary health:progress and prospect. Scientia Sinica (Vitae), 49 (12): 1652-1663. (in Chinese) |
| null | 丁俊荣, 张秋香, 刘小鸣, 王刚, 田丰伟, 张灏, 陈卫. 2012. 江苏无锡健康与肠病人群肠道脱硫弧菌数量及肠道菌群多样性. 微生物学报, 8 (52): 1033-1039. |
| null | 于黎, 黄艳梅, 张志刚, 朱勋程, 李依恬, 李宁, 李纯兵, 徐志茹, 姚雪沁, 胡靖扬, 吴宏, 匡卫民. 2021. 滇金丝猴肠道微生物组数据获取技术规程. DB 53/T1057-2021. |
| null | 勾长龙, 王雨琼, 张喜庆, 娄玉杰, 高云航. 2017. 高温堆肥对猪粪中四环素类抗生素及抗性基因的影响. 环境科学学报, 37 (4): 1454-1460. |
| null | 文雯, 徐先林, 欧刚卫. 2013. 多种抗生素抗性基因在儿童肠道菌群的携带状况. 遵义医学院学报, 36 (2): 113-115. |
| null | 田哲, 张昱, 杨敏. 2014. 四环素类药物酶修饰基因-tet (X) 的起源、分布及在环境中的作用. 环境化学, 12: 2027-2037. |
| null | 朱冬, 陈青林, 丁晶, 王一飞, 崔慧灵, 朱永官. 2019. 土壤生态系统中抗生素抗性基因与星球健康: 进展与展望. 中国科学: 生命科学, 49 (12): 1652-1663. |
| null | 李雯雯, 李丽, 吴巩胜, 张宇, 代云川, 周跃 ．2016. 评估不同尺度下农牧地对滇金丝猴景观连接度的影响．生态学报, 36 (24): 8136-8144. |
| null | 杨斌. 2017. 早期补饲苜蓿调节幼龄湖羊生长和瘤胃发育的机制研究. 杭州: 浙江大学博士学位论文. |
| null | 呙会会. 2014. 神农架金丝猴源益肠道益生菌的筛选和鉴定. 武汉: 华中农业大学硕士学位论文. |
| null | 余小丽. 2020. 雌雄滇金丝猴不同季节肠道微生物群落结构差异的研究. 南充: 西华师范大学硕士学位论文. |
| null | 罗亚, 唐贇, 张丁, 程鸣, 邹书珍, 张晋东, 康迪. 2020. 不同年龄大熊猫肠道菌群及其酶活特征分析. 畜牧兽医学报, 51 (4): 763-771. |
| null | 周万蓉, 王红宁, 张安云, 吴琦, 黄勇, 柳萍, 田浪, 杨鑫, 刘立, 夏青青. 2007. 猪和野生动物源大肠杆菌及沙门菌中磺胺类药物耐药基因的检测. 中国兽医科学, 37 (4): 287-290. |
| null | 郭松涛. 2004. 秦岭金丝猴 (Rhinopithecus roxellana) 的采食和家域行为的研究. 西安: 西北大学硕士学位论文. |
| null | 郭程, 向左甫, 任保平, 李明. 2011. 滇金丝猴群中全雄单元在移动时的空间结构与功能. 中南林业科技大学学报, 31 (7): 136-139. |
| null | 程鸣. 2021. 滇金丝猴和川金丝猴肠道微生物多样性研究. 南充: 西华师范大学硕士学位论文. |
| null | 曾小琴. 2018. 人为干扰下滇金丝猴 (Rhinopithecus bieti) 皮质醇激素变化与行为适应策略研究. 南充: 西华师范大学硕士学位论文. |
| null | 詹杰, 魏树. 2015. 四环素在土壤和水环境中的分布及其生态毒性与降解. 生态学报, 35 (9): 2819-2825. |
| null | 鲍士旦. 2000. 土壤农化分析. 北京中国农业出版社. |
| null | 蔡凯凯, 黄占旺, 叶德军, 孙长涛. 2011. 益生菌调节肠道菌群及免疫调节作用机理. 中国饲料, 18: 34-37 |
| null | 臧凯丽, 江岩, 孙勇, 陈庆森, 赵林森, 赵培, 崔文静, 马新颖, 闫亚丽. 2018. 微生态制剂调节便秘, 腹泻人群肠道菌群结构与产短链脂肪酸关键菌属的相关性. 食品科学, 39 (5): 155-165. |
| null | 魏辅文. 2016. 我国濒危哺乳动物保护生物学研究进展. 兽类学报, 36 (3): 255-269. |
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