非人灵长类肠道微生物研究进展与展望

doi:10.16829/j.slxb.150669

兽类学报 ›› 2023, Vol. 43 ›› Issue (1): 69-81.DOI: 10.16829/j.slxb.150669

非人灵长类肠道微生物研究进展与展望

郭秋艳¹, 韦晓², 陆媚静¹, 范鹏来¹(), 周岐海¹()

^1.珍稀濒危动植物生态与环境保护教育部重点实验室，广西珍稀濒危动物生态学重点实验室，广西师范大学，桂林 541006
^2.广西壮族自治区陆生野生动物救护研究与疫源疫病监测中心，南宁 530000

收稿日期:2022-03-20 接受日期:2022-07-05 出版日期:2023-01-30 发布日期:2023-01-10
通讯作者: 范鹏来,周岐海
作者简介:郭秋艳 (1995- )，女，硕士研究生，主要从事动物生态学研究
韦晓 (1987- )，男，硕士研究生，主要从事动物学研究.第一联系人：（郭秋艳、韦晓并列第一作者）
基金资助:
国家自然科学基金(32170492);广西自然科学基金(2019GXNSFDA245021);广西科技基地和人才专项(桂科AD21220028);广西林业科技推广示范项目

Advances and prospects of the gut microbiome in non-human primate

Qiuyan GUO¹, Xiao WEI², Meijing LU¹, Penglai FAN¹(), Qihai ZHOU¹()

^1.Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection, Monistry of Education, Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin 541006, China
^2.Terrestrial Wildlife Rescue and Epidemic Diseases Surveillance Center of Guangxi, Nanning 530000, China

Received:2022-03-20 Accepted:2022-07-05 Online:2023-01-30 Published:2023-01-10
Contact: Penglai FAN,Qihai ZHOU

摘要/Abstract

摘要：

肠道微生物组被誉为动物的“第二套基因组”，与动物的个体发育、营养获取、生理功能、免疫调节等重要活动密切相关。非人灵长类在生态位、社会结构、地理分布以及进化上与人类相近，开展其肠道微生物研究不仅有助于了解灵长类的生态、保护和进化，而且对深入了解肠道微生物在人类进化中所发挥的作用也具有重要的参考价值。本文总结了影响非人灵长类肠道微生物变化的因素，包括系统发育、觅食、栖息地破碎化、年龄和性别、圈养方式以及社群生活，并探讨了肠道微生物研究在非人灵长类生态、行为、保护以及适应性进化方面的应用。未来，非人灵长类肠道微生物研究将为灵长类生态、进化和人类健康的研究提供新的视角，为灵长类的保护提供新的理论基础和研究方法。

关键词: 非人灵长类, 肠道微生物, 适应, 协同进化, 保护

Abstract:

The gut microbiome is the second set of animal genomes and interacts with hosts in development, nutrition metabolism, physiological function, and immunity. Non-human primates (NHPs) are close to humans in terms of ecological niche, social structure, geographical distribution and evolution. The research of NHPs gut microbiome not only contributes to understanding primate ecology, conservation, and evolution but has also important reference value for in-depth understanding of the role of the gut microbiome in human evolution. This paper summarizes the factors influencing the composition of the gut microbiome in NHPs, including host species and phylogeny, diet, habitat fragmentation, age/sex, captivity, and community life. We also explore the application of gut microbiome research in NHPs ecology, behavior, conservation, and adaptive evolution. Future studies of the gut microbiome of NHPs will offer new insight into primate ecology and evolution as well as human health. They will also provide a new theoretical basis and means for primate conservation.

Key words: Non-human primates, Gut microbiome, Adaptation, Coevolution, Conservation

中图分类号:

郭秋艳, 韦晓, 陆媚静, 范鹏来, 周岐海. 非人灵长类肠道微生物研究进展与展望[J]. 兽类学报, 2023, 43(1): 69-81.

Qiuyan GUO, Xiao WEI, Meijing LU, Penglai FAN, Qihai ZHOU. Advances and prospects of the gut microbiome in non-human primate[J]. ACTA THERIOLOGICA SINICA, 2023, 43(1): 69-81.

参考文献 0

	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. The Journals of Gerontology: Series A, 75 (7): 1293-1298.
	Aiello L C, Wells J C K. 2002. Energetics and the evolution of the genus Homo . Annual Review of Anthropology, 31 (1): 323-338.
	Altmann J, Samuels A. 1992. Costs of maternal care: Infant‑carrying in baboons. Behavioral Ecology Sociobiology, 29 (6): 391-398.
	Amaral W Z, Lubach G R, Proctor A, Lyte M, Phillips G J, Coe C L. 2017. Social influences on Prevotella and the gut microbiome of young monkeys. Psychosomatic Medicine, 79 (8): 888-897.
	Amato K R, Belle S V, Fiore A D, Estrada A, Stumpf R, White B, Nelson K E, Knight R, Leigh S R. 2017. Patterns in gut microbiota similarity associated with degree of sociality among sex classes of a neotropical primate. Microbial Ecology, 74 (1): 250-258.
	Amato K R, Clayton J B, Hale V L. 2022. Colobine gut microbiota: new perspectives on the nutrition and health of a specialized subfamily of primates. In: Matsuda I, Grueter C C, Teichroeb J A eds. The Colobines: Nature History, Behavior and Ecological Diversity. Cambridge University Press, 78-93.
	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. 2015. 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, 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, 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.
	Amato K R, Sanders J G, Song S J, Nute M, Metcalf J L, Thompson L R, Morton J T, Amir A, Mckenzie V J, Humphrey G, Gogul G, Gaffney J, Baden A L, Britton G A O, Cuozzo F P, Fiore A D, Dominy N J, Goldberg T L, Gomez A, Kowalewski M M, Lewis R J, Link A, Sauther M L, Tecot S, White B A, Nelson K E, Stumpf R M, Knight R, Leigh S R. 2019. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. The ISME Journal, 13: 576-587.
	Amato K R, Yeoman C J, Kent A, Righini N, Carbonero F, Estrada A, Gaskins H R, Stumpf R M, Yildirim S, Torralba M, Gillis M, Wilson B A, Nelson K E, White B A, Leigh S R. 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal, 7 (7): 1344-1353.
	Antwis R E, Edwards K L, Unwin B, Walker S L, Shultz S. 2019. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome, 7 (1): 27.
	Baniel A, Amato K R, Beehner J C, Bergman T J, Mercer A, Perlman R F, Petrullo L, Reitsema L, Sams S, Lu A, Snyder‑Mackler N. 2020. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas. Microbiome, 9 (1): 26.
	Baranga D, Chapman C A, Mucunguzi P, Reyna‑Hurtabo R. 2013. Fragments and food: red‑tailed monkey abundance in privately owned forest fragments of central Uganda. Primates in Fragments, 15: 213-225.
	Barbican H J, Li Y Y, Ramirez M, Klase Z, Lipende I, Mjungu D, Moeller A H, Wilson M L, Pusey A E, Lonsdorf E V, Bushman F D, Hahn B H. 2018. Destabilization of the gut microbiome marks the end‑stage of simian immunodeficiency virus infection in wild Chimpanzees. American Journal of Primatology, 80 (1): e22515.
	Barelli C, Albanese D, Stumpf R M, Asangba A E, Donati C, Rovero F, Hauffe H C. 2020. The gut microbiota communities of wild arboreal and ground‑feeding tropical primates are affected differently by habitat disturbance. mSystems, 5 (3): e00061-20.
	Barton W, Cronin O, Garcia‑Perez I, Whiston R, Holmes E, Woods T, Molloy C B, Molloy M G, Shanahan F, Cotter P D, O’Sullivan O. 2020. The effects of sustained fitness improvement on the gut microbiome: a longitudinal, repeated measures case‑study approach. Translation Sports Medicine, 4 (2): 174-192.
	Bauchop T, Martucci R W. 1968. Ruminant-like digestion of the langur monkey. Science, 161 (3842): 698-700.
	Becker F, Gavins F N E, Fontenot J, Fontenot J, Jordan P, Yun J Y, Scott R, Polk P R, Friday R E, Boktor M, Musso M, Romero E, Boudreaux S, Simmons J, Hasselschwert D L, Goetzmann J E, Vanchiere J, Cvek U, Trutschl M, Kilgore P, Alexander J S. 2019. Dynamic gut microbiome changes following regional intestinal lymphatic obstruction in primates. Pathophysiology, 26 (3-4): 253-261.
	Benavidez K M, Iruri‑Tucker A, Steiniche T, Wasserman M D. 2019. Primate microbial endocrinology: an uncharted frontier. American Journal of Primatology, 81: e23053.
	Bennett G, Malone M, Sauther M L, Cuozzo F P, White B, Nelson K E, Stumpf R M, Knight R, Leigh S R, Amato K R ． 2016. Host age, social group, and habitat type influence the gut microbiota of wild ring‑tailed lemurs (Lemur catta)．American Journal of Primatology, 78 (8): 883-892．
	Björk J R, Dasari M, Grieneisen L, Archie E A. 2019. Primate microbiomes over time: longitudinal answers to standing questions in microbiome research. American Journal of Primatology, 81 (12): e22970.
	Bonaz B, Bazin T, Pellissier S. 2018. The vagus nerve at the interface of the microbiota-gut-brain axis. Frontiers in Neuroscience, 12: 49.
	Bronikowski A M, Cords M, Alberts S C, Altmann J, Brockman D K, Fedigan L M, Pusey A, Stoinski T, Strier K B, Morris W F. 2016. Female and male life tables for seven wild primate species. Scientific Data, 3 (1): 160006.
	Brooks A W, Kohl K D, Brucher R M, van Opstal E J, Bordenstein S R. 2016. Phylosymbiosis: relationships and functional effects of microbial commnunities across host evolutionary history. PLoS Biology, 14 (11): e2000225.
	Bublitz D C, Wright P C, Rasambainarivo F T, Arrigo‑Nelson S J, Bodager J R, Gillespie T G. 2015. Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance. American Journal of Primatology, 77 (3): 330-337.
	Chen L M, Wang D M, Garmaeva S, Kurilshikov A, Vila V A, Gacesa R, Sinha T, Study L C, Segal E, Weersma R K, Wijmenga C, Zhernakova A, Fu J Y. 2021. The long‑term genetic stability and individual specificity of the human gut microbiome. Cell, 184 (9): 2302-2315.
	Chi L D, Khan I, Lin Z B, Zhang J W, Lee M Y S, Leong W, Hsiao W L W, Zheng Y. 2020. Fructo-oligosaccharides from Morinda officinalis remodeled gut microbiota and alleviated depression features in a stress rat mode. Phytomedicine, 67: 153457.
	Clarke S F, Murphy E F, O’Sullivan O, Lucey A, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery I B, Wood‑Martin R, Kerins D M, Quigley E M, Ross R P, O’Toole P W, Molloy M G, Falvey E C, Shanahan F, Cotter P. 2014. Exercise and associated dietary extremes impact on gut microbial diversity. Gut, 63 (12): 1913-1920.
	Clayton J B, Al‑Ghalith G A, Long H T, Tuan B V, Cabana F, Huang H, Vangay P, Ward T, Minh V V, Tam N A, Dat N T, Travis D A, Murtaugh M P, Covert H, Glander K E, Nadler T, Toddes B, Sha J C M, Singer R, Knights D, Johnson T J. 2018a. Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Scientific Reports, 8 (1): 11159.
	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. 2018b. The gut microbiome of nonhuman primates: lessons in ecology and evolution. American Journal of Primatology, 80 (6): e22867.
	Clayton J B, Vangay P, Huang H, Ward T, Hillmann B M, Al‑Ghalith G A, Travis D A, Long H T, Tuan B V, Minh V V, Cabana F, Nadler T, Toddes B, Murphy T, Glander K E, Johnson T J, Knights D. 2016. Captivity humanizes the primate microbiome. Proceedings of the National Academy of Sciences, 113 (37): 10376-10381.
	Corlett R T. 2016. Plant diversity in a changing world: status, trends, and conservation needs. Plant Divers, 38 (1): 10-16.
	Cui Z W, Holmes A J, Zhang W J, Hu D L, Shao Q, Wang Z L, Lu J Q, Raubenheimer D. 2022. Seasonal diet and microbiome shifts in wild rhesus macaques are better correlated at the level of nutrient components than food items. Integrative Zoology, 17: 1147-1161.
	Dantzer R. 1991. Stress, stereotypies and welfare. Behavioural Processes, 25 (2-3): 95-102.
	Lugano S D, Nyerere K A, Kariuki W K, Samuel K, Joseph K, Apondi O J. 2018. Gastrointestinal microbial flora in wild and captive olive baboons (Papio anubis). American Journal of Infectious Diseases and Microbiology, 6 (1): 30-37.
	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. Biological Sciences, 109 (32): 13034-13039.
	den Besten G, van Eunen K, Groen A K, Venema K, Reijngoud D J, Bakker B M. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota and host energy metabolism. Journal of Lipid Research, 54 (9): 2325-2340.
	Dillon R J, Vennard C T, Buckling A, Charnley A K. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecology Letters, 8 (12): 1291-1298.
	Ding Y, Bu F, Chen T, Shi G P, Yuan X M, Feng Z Y, Duan Z L, Wang R, Zhang S M, Wang R, Zhang S M, Wang Q, Zhou J Y, Chen Y G. 2021. A next-generation probiotic: Akkermansia muciniphila ameliorates chronic stress-induced depressive-like behavior in mice by regulating gut microbiota and metabolites. Applied Microbiology and Biotechnology, 105 (21-22): 8411-8426.
	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 Sinaca, 37 (4): 399-406. (in Chinese)
	Donohue M E, Asangba A E, Ralainirina J, Weisrock D W, Stumpf R M, Wright P C. 2019. Extensive variability in the gut microbiome of a highly‑specialized and critically endangered lemur species across sites. American Journal of Primatology, 81 (10-11): e23046.
	Dunbar R, Fleagle J G. 1999. Primate adaptation and evolution. The Journal of the Royal Anthropological Institute, 5: 650.
	Eckermann H A, Ou Y, Lahti L, Weerth C. 2022. Can gut microbiota throughout the first 10 years of life predict executive functioning in childhood? Developmental Psychobiology, 64 (3): e22226.
	Ezenwa V O, Gerardo N M, Inouye D W, Medina M, Xavier J B. 2012. Animal behavior and the microbiome. Science, 338 (6140): 198-199.
	Ezenwa V O, Ghai R R, McKay A F, Williams A E. 2016. Group living and pathogen infection revisited. Current Opinion in Behavioral Sciences, 12: 66-72.
	Fackelmann G, Gillingham M A F, Schmid J, Heni A C, Wilhelm K, Schwensow N, Sommer S. 2021. Human encroachment into wildlife gut microbiomes. Communications Biology, 4 (1): 800.
	Farzi A, Fröhlich E E, Holzer P. 2018. Gut microbiota and the neuroendocrine system. Neurotherapeutics, 15: 5-22.
	Frankel J S, Mallott E K, Hopper L M, Ross S R, Amato K R. 2019. The effect of captivity on the primate gut microbiome varies with host dietary niche. American Journal of Primatology, 81 (12): e23061.
	Friswell M K, Gika H, Stratford I J, Theodoridis G, Telfer B, Wilson I D, Mcbain A J. 2010. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS ONE, 5 (1): e8584.
	Goldberg T L, Gillespie T R, Rwego I B, Estoff E L, Chapman C A. 2008. Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerging Infectious Diseases, 14 (9): 1375-1382.
	Gomez A, Petrzelkova K, Yeoman C J, Vlckova K, Mrázek J, Koppova I, Carbonero F, Ulanov A, Modry D, Todd A, Torralba M, Nelson K E, Gaskins H R, Wilson B, Stumpf R M, White B A, Leigh S R. 2015. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Molecular Ecology, 24 (10): 2551-2565.
	Gomez A, Rothman J M, Petrzelkova K, Yeoman C J, Vlckova K, Umaña J D, Carr M, Modry D, Todd A, Torralba M, Nelson K E, Stumpf R M, Wilson B A, Blekhman R, White B A, Leigh S R. 2016. Temporal variation selects for diet‑microbe co‑metabolic traits in the gut of Gorilla spp. The ISME Journal, 10: 514-526.
	Grassotti T T, Kothe C I, Prichula J, Mohellibi N, Mann M B, Wagner P G C, Campos F S, Campos A A S, Frazzon J, Frazzon A P G. 2021. Fecal bacterial communities of wild black capuchin monkeys (Sapajus nigritus) from the Atlantic Forest biome in Southern Brazil are divergent from those of other non‑human primates. Current Research in Microbial Sciences, 2: 100048.
	Grieneisen L E, Livermore J, Alberts S, Tung J, Archie E A. 2017. Group living and male dispersal predict the core gut microbiome in wild baboons. Integrative and Comparative Biology, 57 (4): 770-785.
	Guan Y, Yang H T, Han S Y, Feng L M, Wang T M, Ge J P. 2017. Comparison of the gut microbiota composition between wild and captive sika deer (Cervus nippon hortulorum) from feces by high‑throughput sequencing. AMB Express, 7 (1): 212.
	Hale V L, Tan C L, Niu K F, Yang Y Q, Knight R, Zhang Q K, Cui D Y, Amato K R. 2017. Diet versus phylogeny: a comparison of gut microbiota in captive colobine monkey species. Mirobial Ecology, 75: 515-527.
	Hale V L, Tan C L, Niu K F, Yang Y Q, Zhang Q K, Knight R, Amato K R. 2019. Gut microbiota in wild and captive Guizhou snub-nosed monkeys, Rhinopithecus brelichi . American Journal of Primatology, 81 (10-11): e22989.
	Hennessy M B, Mccowan B, Jiang J, Capitanio J P. 2014. Depressive-like behavioral response of adult male rhesus monkeys during routine animal husbandry procedure. Frontiers in Behavioral Neuroscience, 8 (8): 309.
	Hicks A L, Lee K J, Couto‑Rodriguez M, Patel J, Sinha R, Guo C, Olson S H, Seimon A, Seimon T A, Ondzie A U, Karesh W B, Reed P, Cameron K N, Lipkin W L, Williams B L. 2018. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nature Communications, 9 (1): 1789.
	Jašarević E, Morrison K E, Bale T L. 2016. Sex differences in the gut microbiome-brain axis across the lifespan. Philosophical Transactions of the Royal Society B, 371: 20150122.
	Kalkeri R, Walters K, Pol W V D, Mcfarland B C, Fisher N, Koide F, Morrow C D, Singh V K. 2021. Changes in the gut microbiome community of nonhuman primates following radiation injury. BMC Microbiology, 21 (1): 93.
	Kummrow M. 2021. Diagnostic and therapeutic guidelines to abnormal behavior in captive nonhuman primates. Veterinary Clinics of North America: Exotic Animal Practice, 24 (1): 253-266.
	Kuthyar S, Manus M B, Amato K R. 2019. Leveraging non‑human primates for exploring the social transmission of microbes. Current Opinion in Microbiology, 50: 8-14.
	Langille M G I, Zaneveld J, Caporaso J G, Mcdonald D, Knights D, Reyes J A, Clemente J C, Burkepile D E, Thurber R L V, Knight R, Beiko R G, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA maker gene sequences. Nature Biotechnology, 31: 814-821.
	Lee W, Hayakawa T, Kiyono M, Yamabata N, Hanya G. 2019. Gut microbiota composition of Japanese macaques associates with extent of human encroachment. American Journal of Primatology, 81 (12): e23072.
	Levy M, Thaiss C A, Elinav E. 2016. Metabolites: messengers between the microbiota and the immune system. Genes & Development, 30 (14): 1589-1597.
	Ley R E, Hamady M, Lozupone C, Turnbaugh P J, Ramey R R, Bircher S, Schlegel M L, Tucker T A, Schrenzel M D, Knight R, Gordon J I. 2008. Evolution of mammals and their gut microbes. Science, 320 (5883): 1647-1651.
	Li Y H, Chen T, Li Y B, Tang Y, Huang Z H. 2021. Gut microbiota are associated with sex and age of host: Evidence from semi‐provisioned rhesus macaques in southwest Guangxi, China. Ecology and Evolution, 11 (12): 8096-8122.
	Liu R, Amato K, Hou R, Gomez A, Dunn D W, Zhang J, Garber P A, Chapman C A, Righini N, He G, Fang G, Li Y H, Li B G, Guo S T. 2022. Specialized digestive adaptations within the hindgut of a colobine monkey. The Innovation, 2: 103-109.
	Liu S H, Guo R J, Liu F, Yuan Q J, Yu Y, Ren F F. 2020. Gut microbiota regulates depression-like behavior in rats through the neuroendocrine-immune-mitochondrial pathway. Neuropsychiatric Disease and Treatment, 16: 859-869.
	Ma J, Prince A L, Bader D, Hu M, Ganu R, Baquero K, Blundell P, Harris R A, Frias A E, Grove K L, Aagaard K M. 2014. High‑fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nature Communications, 5: 3889-3900.
	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.
	Marshall A R. 2008. Ecological report on Magombera forest. Worldwide Fund For Nature Tanzania Programme Office.
	Mckenney E A, Ashwell M, Lambert J E, Fellner V. 2014. Fecal microbial diversity and putative function in captive western lowland gorillas (Gorilla gorilla gorilla), common chimpanzees (Pan troglodytes), hamadryas baboons (Papio hamadryas) and binturongs (Arctictis binturong). Integrative Zoology, 9 (5): 557-569.
	Mckenney E A, O’Connell T M, Rodrigo A, Yoder A D. 2018a. Feeding strategy shapes gut metagenomic enrichment and functional specialization in captive lemurs, Gut Microbes, 9 (3): 202-217.
	Mckenney E A, Koelle K, Dunn R R, Yoder A D. 2018b. The ecosystem services of animal microbiomes. Molecular Ecology, 27 (8): 2164-2172.
	Moeller A H, Foerster S, Wilson M L, Pusey A E, Hahn B H, Ochman H.2016.Social behavior shapes the chimpanzee pan‑microbiome. Science Advances, 2: 372-379.
	Moreno‑Indias I, Sánchez‑Alcoholado L, Sánchez‑Garrido M Á, Martín‑Núñez G M, Pérez‑Jiménez F, Tena‑Sempere M, Tinahones F J, Queipo‑Ortuño M I. 2016. Neonatal androgen exposure causes persistent gut microbiota dysbiosis related to metabolic disease in adult female rats. Endocrinology, 157 (12): 4888-4898.
	Nagpal R, Shively C A, Register T C, Craft S, Yadav H. 2019. Gut microbiome Mediterranean diet interactions in improving host health. F1000Research, 8: 699.
	Nakamura N, Amato K R, Garber P, Estrada A, Mackie R I, Gaskins H R. 2011. Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico. American Journal of Primatology, 73 (9): 909-919.
	Namasivayam S, Kauffman K D, Mcculloch J A, Yuan W X, Thovarai V, Mittereder L R, Trinchieri G, Barber D L, Sher A. 2019. Correlation between disease severity and the intestinal microbiome in Mycobacterium tuberculosis‑Infected Rhesus Macaques. mBio, 10 (3): e01018-e01019.
	Neufeld K M, Kang N, Bienenstock J, Foster J A. 2011. Reduced anxiety-like behavior and central neurochemical change in germ‑free mice. Neurogastroenterology & Motility, 23 (3): 255-264.
	Noguera J C, Aira M, Pérez‑Losada M, Domínguez J, Velando A. 2018. Glucocorticoids modulate gastrointestinal microbiome in a wild bird. Royal Society Open Science, 5 (4): 171743.
	Ochman H, Worobey M, Kuo C H, Ndjango J B N, Peeters M, Hahn B H, Hugenholtz P. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8 (11): e1000546.
	Oftedal O T, Whiten A, Southgate D A T, Soest P V. 1991. The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philisophical Transaction of The Royal Sociey B: Biological Sciences, 334: 161-170.
	Orkin J D, Campos F A, Myers M S, Hernandez S E C, Guadamuz A, Melin A D. 2019a. Seasonality of the gut microbiota of free‑ranging white‑faced capuchins in a tropical dry forest. The ISME Journal, 13 (1): 183-196.
	Orkin J D, Webb S E, Melin A D. 2019b. Small to modest impact of social group on the gut microbiome of wild Costa Rican capuchins in a seasonal forest. American Journal of Primatology, 81(10-11): e22985.
	Perofsky A C, Lewis R J, Abondano L A, Fiore A D, Meyers L A. 2017. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. The Royal Society, 284 (1868): 20172274.
	Perofsky A C, Mayers L A, Abondano L A, Fiore A D, Lewis R J. 2021. Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes. Molecular Ecology, 30 (24): 6759-6775.
	Qi X Y, Yun C Y, Pang Y L, Qiao J. 2021. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes, 13 (1): 21.
	Reese A T, Phillips S R, Owens L A, Venable E M, Langergraber K E, Machanda Z P, Mitani J C, Muller M N, Watts D P, Wrangham R W, Goldberg T L, Thompson M E, Carmody R N. 2021. Age patterning in wild chimpanzee gut microbiota diversity reveals differences from humans in early life. Current Biology, 31 (3): 613-620.
	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.
	Rudolph K, Schneider D, Fichtel C, Daniel R, Heistermann M, Kappeler P M. 2022. Drivers of gut microbiome variation within and between groups of a wild Malagasy primate. Microbiome, 10 (1): 28.
	Sarkar A, Lehto S M, Harty S, Dinan T G, Cryan J F, Burnet P W J. 2016. Psychobiotics and the manipulation of bacteria‒gut‒brain signals. Trends in Neurosciences, 39: 763-781.
	Savage D C. 1977. Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology, 31 (1): 107-133.
	Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14 (8): e1002533.
	Shigeno Y, Toyama M, Nakamura M, Niimi K, Takahashi E, Benno Y. 2018. Comparison of gut microbiota composition between laboratory‑bred marmosets (Callithrix jacchus) with chronic diarrhea and healthy animals using terminal restriction fragment length polymorphism analysis. Microbiology and Immunology, 62(11): 702-710.
	Shively C A, Willard S L. 2012. Behavioral and neurobiological characteristics of social stress versus depression in nonhuman primates. Experimental Neurology, 233 (1): 87-94.
	Sun B H, Wang X, Bernstein S, Huffman M A, Xia D P, Gu Z Y, Chen R, Sheeran L K, Wagner R S, Li J H. 2016. Marked variation between winter and spring gut microbiota in free‑ranging Tibetan macaques (Macaca thibetana). Scientific Reports, 6: 26035.
	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. 2018a. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome, 6 (1): 84.
	Trosvik P, Rueness E K, de Muinck E J, Moges A, Mekonnen A. 2018b. Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys. Scientific Reports, 8 (1): 20.
	Tung J, Barreiro L B, Burns M B, Grenier J C, Lynch J, Grieneisen L E, Altmann J, Alberts S C, Blekhman R, Archie E A. 2015. Social networks predict gut microbiome composition in wild baboons. eLife, 4 (4): e05224.
	Uenishi G, Fujita S, Ohashi G, Kato A, Yamauchi S, Matsuzawa T, Ushida K. 2007. Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. American Journal of Primatology, 69 (4): 367-376.
	Unwin T, Smith A. 2010. Behavioral differences between provisioned and non‑provisioned Barbary macaques (Macaca sylvanus). Anthrozoös, 23 (2): 109-118.
	Wang L, Beier U H, Akimova T, Dahiya S, Han R, Samanta A, Levine M H, Hancock W W. 2018. Histone/protein deacet-ylase inhibitor therapy for enhancement of Foxp3⁺ T-regulatory cell function posttransplantation. American Journal of Transplantation, 18: 1596-1603.
	Wei F W, Shan L, Hu Y B, Nie Y G. 2019. Conservation evolutionary biology: a new branch of conservation biology. Science China life Sciences, 49 (4): 498-508. (in Chinese)
	Wei Z Y, Rao J H, Tang M T, Zhao G A, Li Q C, Wu L M, Liu S Q, Li B H, Xiao B Q, Liu X Y, Chen J H. 2022. Characterization of changes and driver microbes in gut microbiota during healthy aging using a captive monkey model. Genomics, Proteomics & Bioinformatics, 20 (2): 350-365.
	Wikberg E C, Christie D, Sicotte P, Ting N. 2020. Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes. Animal Behaviour, 163: 17-31.
	Wu X Y, Wei X B, Shang Y Q, Zhang H H. 2021. Evolutionary and dietary relationships of wild mammals based on the gut microbiome. Gene, 808: 145999.
	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: 685-699.
	Xie T Q, Wang Y C, Zou Z J, He J, Yu Y, Liu Y Q, Bai J B. 2020. Environmental tobacco smoke exposure and breastfeeding duration influence the composition and dynamics of gut microbiota in young children aged 0-2 years. Biological Research For Nursing, 23 (3): 1099800420975129.
	Yang S Z, Liu Y, Yang N, Lan Y, Lan Y, Feng J Y, Yue B S, He M, Zhang L, Zhang A Y, Price M, Li J, Fan Z X. 2022. The gut microbiome and antibiotic resistome of chronic diarrhea rhesus macaques (Macaca mulatta) and its similarity to the human gut microbiome. Microbiome, 10 (1): 29.
	Yang Y, Li Q H, Garber P A, Grueter C C, Ren G P, Wang X W, Huang Z P, Xiang Z F, Xiao W, Behie A. 2020. Cafeteria: style feeding trials provide new insights into the diet and nutritional strategies of the black snub‑nosed monkey (Rhinopithecus strykeri): implications for conservation. American Journal of Primatology, 82 (3): e23108.
	Yasuda K, Oh K, Ren B, Tickle T L, Franzosa E A, Wachtman L M, Miller A D, Westmoreland S V, Mansfield K G, Vallender E J, Miller G M, Rowlett J K, Gevers D, Huttenhower C, Morgan X C. 2015. Biogeography of the intestinal mucosal and luminal microbiome in the rhesus macaque. Cell Host & Microbe, 17 (3): 385-391.
	Yi L N. 2019. Gut microbiota of wild snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia: variation in relation to seasonality, age, and gender. Master thesis.Beijing: University of Chinses Academy of Sciences. (in Chinese)
	Yildirim S, Yeoman C J, Sipos M, Torralba M, Wilson B A, Goldberg T L, Stumpf R M, Leigh S R, White B A, Nelson K E. 2010. Characterization of the fecal microbiome from non‑human wild primates reveals species specific microbial communities. PLoS ONE, 5 (11): e13963.
	Zeng Y, Pu Y, Niu L L, Deng J B, Zeng D, Amato K R, Li Y, Zhou Y, Lin Y C, Wang J, Wu L Q, Chen B H, Pan K C, Jing B, Ni X Q. 2022. Comparison of gastrointestinal microbiota in golden snub-nosed monkey (Rhinopithecus roxellanae), green monkey (Chlorocebus aethiops sabaeus), and ring‑tailed lemur (Lemur catta) by high throughput sequencing. Global Ecology and Conservation, 33: e01946.
	Zhan J, Ma X R, Liu D H, Liang Y R, Li P Z, Cui J N, Zhou Z Q, Wang P. 2020. Gut microbiome alterations induced by tributyltin exposure are associated with increased body weight, impaired glucose and insulin homeostasis and endocrine disruption in mice. Environmental Pollution, 266 (Pt 3): 115276.
	Zhang Z G, Xu D M, Wang L, Hao J J, Wang J F, Zhou X, Wang W W, Qiu Q, Huang X D, Zhou J W, Long R J, Zhao F Q, Shi P. 2016. Convergent evolution of rumen microbiomes in high‑altitude mammals. Current Biology, 26 (14): 1873-1879.
	Zhao Q, Elson C O. 2018. Adaptive immune education by gut microbiota antigens. Immunology, 154 (1): 28-37.
	Zheng P, Wu J, Zhang H P, Perry S W, Yin B M, Tan X M, Chai T J, Liang W W, Huang Y, Li Y F, Duan J J, Wong M L, Licinio J, Xie P. 2020. The gut microbiome modulates gut-brain axis glycerophospholipid metabolism in a region-specific manner in a nonhuman primate model of depression. Molecular Psychiatry, 26 (6): 2380-2392.
	Zhu L F, Suhr Van Haute M J, Hassenstab H R, Smith C, Rose D J, Mustoe A C, Benson A K, French J A. 2020. Fecal short‑chain fatty acid concentrations increase in newly paired male marmosets (Callithrix jacchus). mSphere, 5 (5): e00794-20.
	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成研究进展与展望. 兽类学报, 37 (4): 399-406.
	伊丽娜. 2019. 神农架野生川金丝猴肠道菌群不同季节、年龄、性别差异的研究. 北京: 中国科学院大学硕士学位论文.
	魏辅文, 单磊, 胡义波, 聂永刚. 2019. 保护演化生物学—保护生物学的新分支. 中国科学: 生命科学, 49 (4): 498-508.

[1]	张鹏, 颜修刚, 石运, 杨德, 王彬, 李伟, 杨远露, 杨朝辉, 吴光阳, 蔡鸷, 李思尧, 邹浩, 张璠. 麻阳河国家级自然保护区黑叶猴野外投食群动态观察[J]. 兽类学报, 2023, 43(6): 753-759.
[2]	蒙秉顺, 黄小龙, 谢波, 王维熙, 黄继池, 张涛, 冉景丞, 张明明. 贵州梵净山国家级自然保护区有蹄类动物适宜栖息地分布[J]. 兽类学报, 2023, 43(6): 664-675.
[3]	钟俊杰, 钮冰, 陈沁, 陈翔, 王艳. 深度学习在野生动物保护中的应用[J]. 兽类学报, 2023, 43(6): 734-744.
[4]	刘思燚, 苏彦捷. 动物数量认知能力的演化[J]. 兽类学报, 2023, 43(4): 450-464.
[5]	邢宝瑞, 赵海平, 李光玉, 孙红梅, 马泽芳, 谭展清, 胡肖, 李晨莹, 吴建华, 刘振. 甾体类激素对梅花鹿鹿茸间充质干细胞骨保护素表达的影响[J]. 兽类学报, 2023, 43(4): 443-449.
[6]	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.
[7]	阮向东, 陈奕欣, 王博宇, 杨筱, 廖春林, 禹洋, 郭程. 湖南八大公山国家级自然保护区兽类和鸟类多样性及活动节律调查[J]. 兽类学报, 2023, 43(3): 342-351.
[8]	张同作, 江峰, 张婧捷, 蔡振媛, 高红梅, 顾海峰, 宋鹏飞. 三江源国家公园野生动物保护与管理对策[J]. 兽类学报, 2023, 43(2): 193-205.
[9]	谢博, 农秀萍, 黄国力, 黄蓉, 姚维, 林建忠, 周岐海. 广西恩城国家级自然保护区兽类和鸟类多样性红外相机监测初报[J]. 兽类学报, 2023, 43(2): 215-223.
[10]	江峰, 宋鹏飞, 张婧捷, 高红梅, 汪海静, 蔡振媛, 刘道鑫, 张同作. 不同养殖场林麝肠道微生物组成和功能的差异[J]. 兽类学报, 2023, 43(2): 129-140.
[11]	叶秀林, 郭克疾, 李欣蕊, 吴庆, 张梦斐, 李明, 赵序茅. 气候变化导致青藏高原马鹿种群适应性分布退缩：以类乌齐马鹿国家级自然保护区为例[J]. 兽类学报, 2023, 43(2): 149-156.
[12]	张清浩, 姚松, 徐恺, 刘统, 肖文宏, 白兵勇, 黄小群, 肖治术. 基于红外相机技术对河南内乡宝天曼国家级自然保护区鸟兽多样性的调查[J]. 兽类学报, 2023, 43(2): 206-214.
[13]	陈辉宝, 贾婷, 章迪, 张浩, 王政昆, 朱万龙. 外源瘦素注射对昆明和大理地区大绒鼠适应性产热的影响[J]. 兽类学报, 2023, 43(1): 21-32.
[14]	韩克国, 李凯, 孙婧, 饶静秋, 周佳, 杨云, 崔亮伟, 管振华. 基于红外相机技术对文山国家级自然保护区老君山片区地栖鸟兽多样性的调查[J]. 兽类学报, 2023, 43(1): 89-101.
[15]	周永祥, 薛亚东, 刘少创, 刘建泉, 周多良. 利用不同家域计算方法对野骆驼栖息地空间利用的比较[J]. 兽类学报, 2023, 43(1): 102-108.

非人灵长类肠道微生物研究进展与展望

Advances and prospects of the gut microbiome in non-human primate

RichHTML

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献 0

相关文章 15

编辑推荐

Metrics