不同生活环境下小熊猫皮质醇和肠道微生物的变化规律

赵星; 马锐; 吴蔚; 李明喜; 陈超; 周延山; 洪明生; 齐敦武

doi:10.16829/j.slxb.150869

兽类学报 >

2024 , Vol. 44 >Issue 4: 427 - 435

DOI: https://doi.org/10.16829/j.slxb.150869

研究论文

不同生活环境下小熊猫皮质醇和肠道微生物的变化规律

赵星 ,
马锐 ,
吴蔚 ,
李明喜 ,
陈超 ,
周延山 ,
洪明生 ,
齐敦武

展开

1 西华师范大学, 西南野生动植物资源保护教育部重点实验室, 南充 637002;
2 成都大熊猫繁育研究基地, 四川省濒危野生动物保护生物学重点实验室, 成都 610081

赵星(1998-)，男，硕士，主要从事动物生态学、保护生物学研究.E-mail:zukoxi98@163.com

收稿日期: 2023-10-17

修回日期: 2024-03-13

网络出版日期: 2024-08-03

基金资助

国家自然科学基金重点项目(U21A20193)；成都大熊猫繁育研究基地自立课题(2022CPB-C06)；第二次青藏高原综合科学考察(2019QZKK05010502)

收起

Changing patterns of cortisol and gut microbiota in Ailurus fulgens under different living environments

ZHAO Xing ,
MA Rui ,
WU Wei ,
LI Mingxi ,
CHEN Chao ,
ZHOU Yanshan ,
HONG Mingsheng ,
QI Dunwu

Expand

1 Southwest Wildlife Resources Conservation Key Laboratory (Ministry of Education), China West Normal University, Nanchong 637002, China;
2 Sichuan Key Laboratory of Conservation Biology for Endangered Wildlife, Chengdu Research Base of Giant Panda Breeding, Chengdu 610081, China

Received date: 2023-10-17

Revised date: 2024-03-13

Online published: 2024-08-03

Fold

摘要

肠道微生物群落易受环境压力的影响，其结构的相对稳定对维持动物机体健康至关重要。皮质醇作为一种应激激素不仅能反映动物应激状况还影响动物的肠道微生物结构，然而小熊猫肠道菌群和粪便皮质醇之间的共变机制尚未被研究。为此，我们通过比较不同生活环境下(圈养、散养和野生)小熊猫粪便皮质醇和肠道微生物结构的差异，以期阐明其皮质醇和肠道微生物的变化规律。结果发现：(1)圈养环境下皮质醇浓度最低(71.1 ±21.6) ng/g，散养环境下其浓度为(111.3 ± 5.6) ng/g，而野生环境下最高，为(5094.8 ± 5383.9) ng/g。同时，散养环境下的小熊猫肠道微生物Shannon指数最高(6.178)，其次是野生环境下(5.535)，圈养环境下最低(3.449)。(2)圈养小熊猫皮质醇浓度与大肠杆菌志贺氏菌属(EscherichiaShigella)呈显著负相关(P<0.001)，与难辨梭菌属(Clostridium_sensu_stricto_1)呈显著正相关(P<0.001)。综上所述，不同生活环境显著影响小熊猫的肠道微生物组成和粪便皮质醇浓度，减少环境的变化频率和强度能有效降低其应激性，维持肠道菌群的健康稳定，这将为小熊猫种群的健康管理提供技术支撑。

关键词： 小熊猫; 肠道微生物; 16S rRNA测序; 皮质醇; 应激

本文引用格式

赵星 , 马锐 , 吴蔚 , 李明喜 , 陈超 , 周延山 , 洪明生 , 齐敦武 . 不同生活环境下小熊猫皮质醇和肠道微生物的变化规律[J]. 兽类学报, 2024 , 44(4) : 427 -435 . DOI: 10.16829/j.slxb.150869

Abstract

Gut microbiota are susceptible to environmental stresses and the relative stability of their structure is essential for maintaining animal health. Cortisol, as a stress hormone, not only responds to the current stress condition of the animal but also affects the gut microbiota structure of the animal. However, the covariation mechanism between gut flora and faecal cortisol in Ailurus fulgens has not been investigated yet. We compared the fecal cortisol and gut microbiota structure of Ailurus fulgens in different living environments (captive, semi-free-ranging and wild) to elucidate the patterns of change in cortisol and gut microbiota organisms. The results revealed that among different living environments, the lowest cortisol concentration was found in captive condition (71. 1 ± 21. 6) ng/g, and its concentration was (111. 3 ± 5. 6) ng/g in semi-free-ranging environment, while the highest (5094. 8 ± 5383. 9) ng/g was found in wild environment. Meanwhile, the highest shannon index of gut microbiota of Ailurus fulgens was found in the semi-free-ranging environment (6. 178), followed by the wild condition (5. 535), and the lowest in captive environment (3. 449). Cortisol concentrations in captive Ailurus fulgens showed a significant negative correlation (P<0. 001) with Escherichia-Shigella and a significant positive correlation (P<0. 001) with Clostridium_sensu_stricto_1. In summary, different living environments significantly affect the gut microbiota composition and faecal cortisol concentration of Ailurus fulgens. Reducing the frequency and intensity of environmental changes can effectively reduce their stress and maintain the health and stability of the gut flora, which will provide technical support for the health management of Ailurus fulgens populations.

Key words： Ailurus fulgens; Gut microbiota; 16S rRNA sequencing; Cortisol; Stress

参考文献

Adams C E, Greenway F L, Brantley P J. 2011. Lifestyle factors and ghrelin:critical review and implications for weight loss mainte nance. Obesity Reviews, 12 (5):e211-e218.
Baudrand R, Vaidya A. 2015. Cortisol dysregulation in obesityrelated metabolic disorders. Current Opinion in Endocrinology, Diabetes and Obesity, 22 (3):143-149.
Bi W L, Hou R, Fei L S, Zhang Z H, Chen P, Luo L, Li M X, Xiang Z F, Gu X D, Qi D W. 2014. Variation of fecal steroid hormone level of giant panda between Chengdu Research Base of Giant Panda Breeding and Dujiangyan Research Center. Sichuan Jour nal of Zoology, 33 (1):8-12. (in Chinese)
Björntorp P, Rosmond R. 2000. Obesity and cortisol. Nutrition, 16(10):924-936.
Bokulich N A, Subramanian S, Faith J J, Gevers D, Gordon J I, Knight R, Mills D A, Caporaso J G. 2013. Quality-filtering vastly im proves diversity estimates from Illumina amplicon sequencing.Nature Methods, 10 (1):57-59.
Demori I, Grasselli E. 2023. The role of the stress response in meta bolic dysfunction-associated fatty liver disease:a psychoneuroen docrine immunology-based perspective. Nutrients, 15 (3):795.
Dinan T G, Cryan J F. 2017. The microbiome-gut-brain axis in health and disease. Gastroenterology Clinics of North America, 46 (1):77-89.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics, 27 (16):2194-2200.
Farzi A, Fröhlich E E, Holzer P. 2018. Gut microbiota and the neuro endocrine system. Neurotherapeutics, 15 (1):5-22.
Gao H M, Jiang F, Zhang J J, Chi X W, Song P F, Li B, Cai Z Y, Zhang T Z. 2023. Effects of ex situ conservation on diversity and func tion of the gut microbiota of the Tibetan wild ass (Equus kiang).Integrative Zoology, 18 (16):1089-1104.
Guo W, Mishra S, Wang C D, Zhang H M, Ning R H, Kong F L, Zeng B, Zhao J C, Li Y. 2019. Comparative study of gut microbiota in wild and captive giant pandas (Ailuropoda melanoleuca). Genes, 10 (10):827.
Hickmott A J, Boose K J, Wakefield M L, Brand C M, Snodgrass J J, Ting N, White F J. 2022. A comparison of faecal glucocorticoid metabolite concentration and gut microbiota diversity in bonobos(Pan paniscus). Microbiology, 168 (8):1465-2080.
Hsiao E Y, McBride S W, Hsien S, Sharon G, Hyde E R, McCue T, Codelli J A, Chow J, Reisman S E, Petrosino J F, Patterson P H, Mazmanian S K. 2013. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155 (7):1451-1463.
IUCN. 2023. The IUCN Red List of Threatened Species. Version 2022-2. https://www.iucnredlist.org
Jin L, Huang Y, Yang S Z, Wu D F, Li C W, Deng W W, Zhao K, He Y G, Li B, Zhang G Q, Xiong Y W, Wei R P, Li G, Wu H N, Zhang H M, Zou L K. 2021. Diet, habitat environment and lifestyle con version affect the gut microbiomes of giant pandas. Science of The Total Environment, 770:145316.
Kong F L, Zhao J C, Han S C, Zeng B, Yang J D, Si X H, Yang B Q, Yang M Y, Xu H L, Li Y. 2014. Characterization of the gut mi crobiota in the red panda (Ailurus fulgens). PLoS ONE, 9 (2):e87885.
Koskinen M K, Aatsinki A, Kortesluoma S, Mustonen P, Munukka E, Lukkarinen M, Perasto L, Keskitalo A, Karlsson H, Karlsson L. 2023. Hair cortisol, cortisone and DHEA concentrations and the composition of microbiota in toddlers. Psychoneuroendocrinol ogy, 154:106309.
Kumar A, Rai U, Roka B, Jha A K, Reddy P A. 2016. Genetic assess ment of captive red panda (Ailurus fulgens) population. Springer Plus, 5 (1):1750.
Lv Y L, Sun Y Z, Li S C, Xue Q. 1998. Aeromonas sobria infection in the red panda. Chinese Journal of Veterinary Medicine, (11):22.(in Chinese)
Magoč T, Salzberg S L. 2011. FLASH:fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27 (1367-4811 (Electronic)):2957-2963.
O'Mahony S M, Marchesi J R, Scully P, Codling C, Ceolho A M, Quigley E M M, Cryan J F, Dinan T G. 2009. Early life stress al ters behavior, immunity, and microbiota in rats:implications for ir ritable bowel syndrome and psychiatric illnesses. Biological Psy chiatry, 65 (3):263-267.
Palme R, Fischer P, Schildorfer H, Ismail M N. 1996. Excretion of in fused ¹⁴C-steroid hormones via faeces and urine in domestic live stock. Animal Reproduction Science, 43 (1):43-63.
Pellissier S, Dantzer C, Mondillon L, Trocme C, Gauchez A S, Ducros V, Mathieu N, Toussaint B, Fournier A, Canini F, Bonaz B. 2014.
Relationship between Vagal Tone, Cortisol, TNF-Alpha, Epineph rine and Negative Affects in Crohn's Disease and Irritable Bowel Syndrome. PLoS ONE, 9 (9):e105328.
Sandrini S, Aldriwesh M, Alruways M, Freestone P. 2015. Microbial endocrinology:host-bacteria communication within the gut micro biome. Journal of Endocrinology, 225 (2):R21-R34.
Snyder R J, Perdue B M, Powell D M, Forthman D L, Bloomsmith M A, Maple T L. 2012. Behavioral and hormonal consequences of transporting giant pandas from China to the United States. Jour nal of Applied Animal Welfare Science, 15 (1):1-20.
Sohel Khan A, Lea S E G, Chand P, Rai U, Baskaran N. 2022. Predic tors of psychological stress and behavioural diversity among cap tive red panda in Indian zoos and their implications for global cap tive management. Scientific Reports, 12 (1):14034.
Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu X N, Kubo C, Koga Y. 2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. The Journal of Physiology, 558 (1):263-275.
Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss C A, Maza O, Israeli D, Zmora N, Gilad S, Weinberger A, Kuperman Y, Harmelin A, Kolodkin-Gal I, Shapiro H, Halpern Z, Segal E, Elinav E. 2014. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature, 514 (7521):181-186.
Tiwari R V, Parajuli P, Sylvester P W. 2015. γ-Tocotrienol-induced en doplasmic reticulum stress and autophagy act concurrently to pro mote breast cancer cell death. Biochemistry and Cell Biology, 93(4):306-320.
Valdes A M, Walter J, Segal E, Spector T D. 2018. Role of the gut mi crobiota in nutrition and health. British Medical Journal, 361:k2179.
Vitali F, Tortora K, Di Paola M, Bartolucci G, Menicatti M, De Filippo C, Caderni G. 2022. Intestinal microbiota profiles in a genetic model of colon tumorigenesis correlates with colon cancer bio markers. Scientific Reports, 12 (1):1432.
Wang Y Y, Guo H, Gao X G, Wang J H. 2021. The intratumor micro biota signatures associate with subtype, tumor stage, and survival status of esophageal carcinoma. Frontiers in Oncology, 11:754788.
Wang L, Huang G P, Hou R, Qi D W, Wu Q, Nie Y G, Zuo Z Q, Ma R, Zhou W L, Ma Y J, Hu Y B, Yang Z S, Yan L, Wei F W. 2021.Multi-omics reveals the positive leverage of plant secondary me tabolites on the gut microbiota in a non-model mammal. Microbi ome, 9 (1):192.
Wang W, Chen M H, Zhao S Q, Jiang J, You Y Y, Sun D T, Huang T P, Wu F, Liu L G, Zhang Y G, Liu X F. 2023. Variations in cortisol and klotho hormone levels in golden snub-nosed monkeys under different environmental conditions. Chinese Journal of Wildlife, 44 (1):179-184. (in Chinese)
Yang K, Jian S, Wen C, Guo D, Liao P, Wen J, Kuang T, Han S, Liu Q, Deng B. 2022. Gallnut tannic acid exerts anti-stress effects on stress-induced inflammatory response, dysbiotic gut microbiota, and alterations of serum metabolicprofile in beagle dogs. Fron tiers in Nutrition, 9:847996.
Zhan M, Wang A, Yao Y, Zhou Y, Zhang S, Fu X, Zhou J, Pei E, Wang L. 2022. An amateur gut microbial configuration formed in giant panda for striving to digest cellulose in bamboo:Systematic evi dence from intestinal digestive enzymes, functional genes and mi crobial structures. Frontiers in Microbiology, 13:926515.
Zhang Q, Hu W M, Deng Y L, Wan J J, Wang Y J, Jin P. 2023. Dys biosis of gut microbiota and decreased propionic acid associated with metabolic abnormality in Cushing's syndrome. Frontiers in Endocrinology, 13:1664-2392.
Zhou X, Baumann R, Gao X, Mendoza M, Singh S, Katz S I, Xia Z, Cox L M, Chitnis T, Yoon H, Moles L, Caillier S J, Santaniello A, Ackermann G, Harroud A, Lincoln R, Gomez R, González P A, Digga E, Hakim D J, Vazquez-Baeza Y, Soman K, Warto S, Hum phrey G, Farez M, Gerdes L A, Oksenberg J R, Zamvil S S, Chan dran S, Connick P, Otaegui D, Castillo-Triviño T, Hauser S L, Gel fand J M, Weiner H L, Hohlfeld R, Wekerle H, Graves J, Bar-Or A, Cree B A C, Correale J, Knight R, Baranzini S E. 2022. Gut microbiome of multiple sclerosis patients and paired household healthy controls reveal associations with disease risk and course.Cell, 185 (19):3467-3486. e3416.
王伟, 程铭昊, 赵思棋, 蒋军, 由玉岩, 孙冬婷, 黄天鹏, 吴锋, 刘连贵, 张于光, 刘学锋. 2023. 不同环境条件下川金丝猴的皮质醇和Klotho 激素水平变化. 野生动物学报, 44 (1):179-184.
毕温磊, 侯蓉, 费立松, 张志和, 陈鹏, 罗娌, 李明喜, 向左甫, 古晓东, 齐敦武. 2014. 迁入都江堰野放中心的大熊猫野化放归个体皮质醇水平变化初步研究. 四川动物, 33 (1):8-12.
吕艳丽, 孙艳争, 李树春, 薛琴. 1998. 小熊猫温和气单孢菌感染.中国兽医杂志, (11):22.

Options

文章导航

模态框（Modal）标题

摘要

本文引用格式

Abstract

参考文献