同一笼养生境下金头狮面狨猴、赤掌柽柳猴和棉顶狨猴肠道菌群比较

doi:10.16829/j.slxb.150739

摘要/Abstract

摘要： 动物的肠道菌群组成与宿主种类及其生存环境直接相关，研究同一生境下不同物种的肠道菌群组成对于物种多样性保护具有积极意义。本研究采用非损伤取样和16S rDNA高通量测序等方法，以南京市红山森林动物园笼养的金头狮面狨猴(Leontopithecus chrysomelas)、赤掌柽柳猴(Saguinus midas)和棉顶狨猴(Saguinus oedipus)三种新大陆猴为研究对象，比较分析其肠道菌群结构组成差异，并进行功能预测。结果发现：3个物种的肠道菌群合计14门20纲50目101科231属356种。优势菌门均为厚壁菌门(Firmicutes)、放线菌门(Actinobacteria)、变形菌门(Proteobacteria)和拟杆菌门(Bacteroidetes)，共有优势菌属为链球菌属(Streptococcus)和双歧杆菌属(Bifidobacterium)。3个物种间肠道菌群在门水平和属水平均存在显著差异，其中金头狮面狨猴的肠道菌群丰富度显著高于另外两个物种。本研究结果为灵长类肠道菌群多样性与生存适应研究提供基础数据，同时为相关物种的易地保护管理提供参考依据。

关键词: 新大陆猴, 肠道菌群, 高通量测序技术, 16S rDNA

Abstract: The composition of intestinal microbiota in animals is directly related to the host species and their living environment. Studies on intestinal microbiota composition of various species living in the same habitat is important for the conservation of species diversity. Both non-damage sampling and 16S rDNA high-throughput sequencing were used to investigate the structure, diversity, and functional prediction of intestinal microbiota across three species of New World monkeys (golden-headed lion tamarin Leontopithecus chrysomelas, golden-handed tamarin Saguinus midas, and cottonheaded tamarin Saguinus oedipus) from Nanjing Hongshan Forest Zoo. The results showed that a total of 14 phyla, 20 classes, 50 orders, 101 families, 231 genera, and 356 species of intestinal flora were obtained from 18 fecal samples collected from the three species. At the phylum level, the common dominant phyla across the three species were Firmicutes, Actinobacteria, Proteobacteria, and Bacteroidetes. At the genus level, the common dominant bacterial genera included Streptococcus and Bifidobacterium. There were significant differences in intestinal microbiota at both the phylum level and the genus level among species, in which the richness of intestinal microbiota in golden-headed lion tamarin was significantly higher than that in the others. This study provides basic data for further investigation on the intestinal microbiota diversity and survival adaptation, and also serves as reference for ex situ management for species conservation.

Key words: New world monkeys, Intestinal microbiota, High-throughput sequencing, 16S rDNA

中图分类号:

Q939

张泽明, 姚红玉, 吴楠, 赵玲玲, 顾逸如, 王宇, 吴弘, 赵大鹏. 同一笼养生境下金头狮面狨猴、赤掌柽柳猴和棉顶狨猴肠道菌群比较[J]. 兽类学报, 2023, 43(5): 580-592.

ZHANG Zeming, YAO Hongyu, WU Nan, ZHAO Lingling, GU Yiru, WANG Yu, WU Hong, ZHAO Dapeng. Comparison of intestinal microbiota of golden-headed lion tamarins, golden-handed tamarins and cotton-headed tamarins under the same captive environment[J]. ACTA THERIOLOGICA SINICA, 2023, 43(5): 580-592.

参考文献

Adriansjach J, Baum S T, Lefkowitz E J, Van Der Pol W J, Buford T W, Colman R J. 2020. Age-related differences in the gut microbiome of rhesus macaques. Journals of Gerontology Series ABiological Sciences and Medical Sciences, 75 (7):1293-1298.
Amato K R, Leigh S R, Kent A, Mackie R I, Yeoman C J, Stumpf R M, Wilson B A, Nelson K E, White B A, Garber P A. 2014. The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra). American Journal of Physical Anthropology, 155 (4):652-664.
Amato K R, Leigh S R, Kent A, Mackie R I, Yeoman C J, Stumpf R M, Wilson B A, Nelson K E, White B A, Garber P A. 2014. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69 (2):434-443.
Amato K R, Martinez-Mota R, Righini N, Raguet-Schofield M, Corcione F P, Marini E, Humphrey G, Gogul G, Gaffney J, Lovelace E, Williams L, Luong A, Dominguez-Bello M G, Stumpf R M, White B, Nelson K E, Knight R, Leigh S R. 2016. Phylogenetic and ecological factors impact the gut microbiota of two neotropical primate species. Oecologia, 180 (3):717-733.
Bolton D J. 2015. Campylobacter virulence and survival factors. Food Microbiology, 48:99-108.
Clayton J B, Gomez A, Amato K, Knights D, Travis D A, Blekhman R, Knight R, Leigh S, Stumpf R, Wolf T, Glander K E, Cabana F, Johnson T J. 2018. The gut microbiome of nonhuman primates:Lessons in ecology and evolution. American Journal of Primatology, 80 (6):e22867.
Dale C, Moran N A. 2006. Molecular interactions between bacterial symbionts and their hosts. Cell, 126 (3):453-465.
Degnan P H, Pusey A E, Lonsdorf E V, Goodall J, Wroblewski E E, Wilson M L, Rudicell R S, Hahn B H, Ochman H. 2012. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences of the United States of America, 109 (32):13034-13039.
Ding Y, Wu Q, Hu Y B, Wang X, Nie Y G, Wu X P, Wei F W. 2017. Advances and prospects of gut microbiome in wild mammals. Acta Theriologica Sinica, 37 (4):399-406. (in Chinese)
Firrman J, Liu L S, Tanes C, Bittinger K, Mahalak K, Rinaldi W. 2019. Metagenomic assessment of the Cebus apella gut microbiota. American Journal of Primatology, 81 (10-11):e23023.
Goldberg T L, Gillespie T R, Rwego I B, Wheeler E, Estoff E L, Chapman C A. 2017. Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation, 135 (4):511-517.
Guo S H, Yu Y T, Wan J H, Mao Y N, Zhang H D, Zhang J S, Tian X Y, Zhao Q M. 2022. Progress in research on the relationship between Proteobacteria and the imbalance of mammalian colonic intestinal flora. Chinese Journal of Microecology, 34 (4):479-484.(in Chinese)
Hale V L, Tan C L, Niu K, Yang Y, Knight R, Zhang Q, Knight R, Zhang Q K, Cui D Y, Amato K R. 2018. Diet versus phylogeny:a comparison of gut microbiota in captive colobine monkey species. Microbial Ecology, 75 (2):515-527.
Huan Z J, Chen H W, Zhao B, Liu X Z, Mao J. 2022. Research advances on influencing factors of gut microbiota. Bulletin of Biology, 57 (2):1-4. (in Chinese)
Jian P, Wang Q, Wang J, Niu L L, Zhu H, Zeng Y, Ni X Q, Zeng D. 2015. Difference analysis of gut microbiome of Rhinopithecus roxellana in different ages. Chinese Journal of Animal Nutrition, 27 (4):1302-1309. (in Chinese)
Li H, Li H Z, Wang J J, Guo L, Fan H T, Zheng H W, Yang Z N, Huang X, Chu M M, Yang F M, He Z H, Li N, Yang J X, Wu Q W, Shi H J, Liu L D. 2019. The altered gut virome community in rhesus monkeys is correlated with the gut bacterial microbiome and associated metabolites. Virology Journal, 16:105.
Lynch J B, Hsiao E Y. 2019. Microbiomes as sources of emergent host phenotypes. Science, 365 (6460):1405-1409.
Mallott E K, Amato K R, Garber P A, Malhi R S. 2018. Influence of fruit and invertebrate consumption on the gut microbiota of wild white-faced capuchins (Cebus capucinus). American Journal of Physical Anthropology, 165 (3):576-588.
Malukiewicz J, Cartwright R A, Dergam J A, Igayara C S, Kessler S E, Moreira S B, Nash L T, Nicola P A, Pereira L C M, Pissinatti A, Ruiz-Miranda C R, Ozga A T, Quirino A A, Roos C, Silva D L, Stone A C, Grativol A D. 2022. The gut microbiome of exudivorous marmosets in the wild and captivity. Scientific Reports, 12:5049.
Mao M, Yang M, Liu X Y. 2022. Effects of hibernation on cecal microbiota in Daurian ground squirrel. Acta Theriologica Sinica, 42(4):420-431. (in Chinese)
Martínez-Mota R, Righini N, Mallott E K, Gillespie T R, Amato K R. 2021. The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra). American Journal of Primatology, 83 (12):e23330.
Mazmanian S K, Liu C, Tzianabos A O, Kasper D L. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell, 122 (1):107-118.
McCord A I, Chapman C A, Weny G, Tumukunde A, Hyeroba D, Klotz K, Koblings A S, Mbora D N M, Cregger M, White B A, Leigh S R, Goldberg T L. 2014. Fecal microbiomes of non-human primates in western Uganda reveal species-specific communities largely resistant to habitat perturbation. American Journal of Primatology, 76 (4):347-354.
Mittermeier R A, Urbani B, Rylands A B, Régis T. 2021. Saguinus midas. The IUCN Red List of Threatened Species 2021:e. T41525A192552538. https://dx.doi.org/10.2305/IUCN.UK.2021-1.RLTS.41525A192552538.en.
Moeller A H, Peeters M, Ndjango J, Li Y Y, Hahn B H, Ochman H. 2013. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Research, 23 (10):1715-1720.
Ni Q Y, He X, Zeng B, Meng X Y, Xu H L, Li Y, Yang M Y, Li D Y, Yao Y F, Zhang M W, Li Y, Fan X L, Yang D Y, Xie M. 2020. Variation in gut microbiota of captive Bengal slow lorises. Current Microbiology, 77 (10):2623-2632.
Oliveira L C, Neves L G, Kierulff M C M, Jerusalinsky L, Mittermeier R A, Rylands A B. 2021. Leontopithecus chrysomelas. The IUCN Red List of Threatened Species 2021:e. T40643A192329573.https://dx. doi. org/10. 2305/IUCN. UK. 2021-11. RLTS.T40643A192327593. en.
Orkin J D, Campos F A, Myers M S, Cheves Hernandez S E, Guadamuz A, Melin A D. 2019. Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest. The ISME Journal, 13 (1):183-196.
Qu C, Zhao L N, Cheng K, Yu S P, Zhang J Y. 2019. Time budget and activity rhythm of captive black-capped capuchin. Chinese Journal of Wildlife, 40 (2):279-284. (in Chinese)
Que T C, Pang X W, Huang H L, Chen P Y, Wei Y F, Hua Y M, Liao H J, Wu J B, Li S S, Wu A Q, He M H, Ruan X D, Hu Y L. 2022. Comparative gut microbiome in Trachypithecus leucocephalus and other primates in Guangxi, China, based on metagenome sequencing. Frontiers in Cellular and Infection Microbiology, 12(485):872841.
Raulo A, Ruokolainen L, Lane A, Amato K, Knight R, Leigh S, Stumpf R, White B, Nelson K E, Baden A L, Tecot S R. 2018. Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer):In search of the role of immunity in the evolution of sociality. Journal of Animal Ecology, 87 (2):388-399.
Reveles K R, Patel S, Forney L, Ross C N. 2019. Age-related changes in the marmoset gut microbiome. American Journal of Primatology, 81 (2):e22960.
Rhoades N S, Cinco I R, Hendrickson S M, Slifka M K, Messaoudi I. 2022. Taxonomic and functional shifts in the perinatal gut microbiome of Rhesus macaques. Microbiology Spectrum, 10 (4):e00814-22.
Rodríguez V, Link A, Guzman-Caro D, Defler T R, Palacios E, Stevenson P R, Mittermeier R A. 2021. Saguinus oedipus. The IUCN Red List of Threatened Species 2021:e. T19823A19255106 7. https://dx.doi.org/10.2305/IUCN.UK.2021-1.RLTS.T19823A192551067.en.
Sheh A. 2020. The gastrointestinal microbiota of the common marmoset (Callithrix jacchus). ILAR Journal, 61 (2-3):188-198.
Sheh A, Artim S C, Burns M A, Molina-Mora J A, Lee M A, Dzink-Fox J, Muthupalani S, Fox J G. 2022. Analysis of gut microbiome profiles in common marmosets (Callithrix jacchus) in health and intestinal disease. Scientific Reports, 12 (1):4430.
Sun B H, Gu Z, Wang X, Huffman M A, Garber P A, Sheeran L K, Zhang D, Zhu Y, Xia D P, Li J H. 2018. Season, age, and sex affect the fecal mycobiota of free-ranging Tibetan macaques (Macaca thibetana). American Journal of Primatology, 80 (7):e22880.
Trosvik P, de Muinck E J, Rueness E K, Fashing P J, Beierschmitt E C, Callingham K R, Kraus J B, Trew T H, Moges A, Mekonnen A, Venkataraman V V, Nguyen N. 2018. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome, 6 (1):84.
Turnbaugh P J, Hamady M, Yatsunenko T, Cantarel B L, Duncan A, Ley R E, Sogin M L, Jones W J, Roe B A, Affourtit J P, Egholm M, Henrissat B, Heath A C, Knight R, Gordon J I. 2009. A core gut microbiome in obese and lean twins. Nature, 457 (7228):480-484.
Wang W, Gao J, Li J R, Yang F, Li Z, Li L X. 2016. Comparative analysis of the gastrointestinal microbial communities of bar-headed goose (Anser indicus) in different breeding patterns by high-throughput sequencing. Microbiological Research, 182:59-67.
Yang X W, Peng C C, Guo Q Y, Ran J C, Wang Y Y, Zhang M M, Hu C S, Li S Z, Su H J. 2021. Diversity and functional characteristics of intestinal microflora of free-living wild boars in the Miaoling Mountain area in Guizhou Province, China. Acta Theriologica Sinica, 41 (4):365-376. (in Chinese)
Yang Z Q. 2021. Comparative study on the intestinal bacterial communities of hooded crane (Grus monacha) and bean goose (Anser fabalis) at Shengjin Lake. Master thesis. Hefei:Anhui University, 26-30. (in Chinese)
Yao L J. 2015. Age-based compositions and differences in the gut microbiome of the Shennongjia golden snub-nosed monkey (Rhinopithecus roxellana). Master thesis. Wuhan:Huazhong Agricultural University, 27-38. (in Chinese)
Yeoman C J, Chia N, Yildirim S, Miller M E B, Kent A, Stumpf R, Leigh S R, Nelson N E, White B A, Wilson B A. 2011. Towards an evolutionary model of animal-associated microbiomes. Entropy, 13 (3):570-594.
Yi L N, Liu X P, Jiang Z G. 2018. Gut bacterial composition and its influencing factors of non-human primates. Chinese Journal of Zoology, 53 (3):479-494. (in Chinese)
Zhu L F, Yang Q N, Suhr Van Haute M J, Kok C R, Gomes-Neto J C, Pavlovikj N, Pillai R, Sinha R, Hassenstab H, Mustoe A, Moriyama E N, Hutkins R, French J, Benson A K. 2021. Captive common marmosets (Callithrix jacchus) are colonized throughout their lives by a community of Bifidobacterium species with species-specific genomic content that can support adaptation to distinct metabolic niches. mBio, 12 (4):e0115321.
丁赟, 吴琦, 胡义波, 王潇, 聂永刚, 吴小平, 魏辅文. 2017. 野生哺乳动物肠道微生物组研究进展与展望. 兽类学报, 37(4):399-406.
毛敏, 杨明, 刘新宇. 2022. 冬眠对达乌尔黄鼠盲肠菌群的影响. 兽类学报, 42 (4):420-431.
伊丽娜, 刘学聪, 蒋志刚. 2018. 非人灵长类肠道菌群组成及影响因素. 动物学杂志, 53 (3):479-494.
杨竹青. 2021. 升金湖越冬白头鹤与豆雁肠道细菌群落的比较研究. 合肥:安徽大学硕士学位论文, 26-30.
杨雄威, 彭彩淳, 郭群毅, 冉景丞, 王野影, 张明明, 胡灿实, 李仕泽, 粟海军. 2021. 贵州苗岭地区野猪肠道菌群结构与功能分析.兽类学报, 41 (4):365-376.
姚丽娟. 2015. 不同年龄段神农架金丝猴肠道菌群组成和差异的研究. 武汉:华中农业大学硕士学位论文, 27-38.
桓宗锦, 陈红卫, 赵波, 刘选珍, 毛杰. 2022. 肠道菌群影响因素的研究进展. 生物学通报, 57 (2):1-4.
郭仕辉, 余永涛, 万佳宏, 毛彦妮, 张浩东, 张津慎, 田新岳, 赵清梅. 2022. 变形菌门与哺乳动物结肠肠道菌群失调相关研究进展.中国微生态学杂志, 34 (4):479-484.
渠畅, 赵丽娜, 程鲲, 余树培, 张敬旸. 2019. 圈养环境下黑帽悬猴行为时间分配和活动节律. 野生动物学报, 40 (2):279-284.
简平, 王强, 王剑, 牛李丽, 祝辉, 曾燕, 倪学勤, 曾东. 2015. 不同年龄段川金丝猴肠道菌群结构差异分析. 动物营养学报, 27 (4):1302-1309.

[1]	操康琳, 陶梦凡, 任月, 侯玉, 贾变桃, 杨新根. 人工饲喂对长尾仓鼠肠道菌群组成的影响[J]. 兽类学报, 2024, 44(2): 195-208.
[2]	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.
[3]	王德华, 赵志军, 张学英, 张志强, 徐德立, 邢昕, 杨生妹, 王政昆, 高云芳, 杨明. 中国哺乳动物生理生态学研究进展与展望[J]. 兽类学报, 2021, 41(5): 537-555.
[4]	杨雄威, 彭彩淳, 郭群毅, 冉景丞, 王野影, 张明明, 胡灿实, 李仕泽, 粟海军. 贵州苗岭地区野猪肠道菌群结构与功能分析[J]. 兽类学报, 2021, 41(4): 365-376.
[5]	丁赟吴琦胡义波王潇聂永刚吴小平魏辅文. 野生哺乳动物肠道微生物组研究进展与展望[J]. 兽类学报, 2017, 37(4): 399-406.