{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T01:43:00Z","timestamp":1790905380167,"version":"4.1.0"},"reference-count":45,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T00:00:00Z","timestamp":1761868800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Qinghai Provincial Key Laboratory of Animal Ecological Genomics","award":["QHEG-2024-04"],"award-info":[{"award-number":["QHEG-2024-04"]}]},{"name":"Independent Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University"},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"crossref","award":["2024T170992"],"award-info":[{"award-number":["2024T170992"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Przewalski\u2019s gazelle (Procapra przewalskii) is an endangered ungulate endemic to the Qinghai\u2013Tibet Plateau, with a small population size and exposure to multiple ecological pressures. Its gut microbiota may play a crucial role in host environmental adaptation. To investigate the functional divergence of gut microbial communities, we performed high-throughput metagenomic sequencing on 105 wild fecal samples collected from 10 geographic regions around Qinghai Lake. The results revealed significant regional differentiation in key functional modules related to metabolism, antibiotic resistance mechanisms, and virulence-associated pathways. All populations showed enrichment in core metabolic pathways such as carbohydrate and amino acid metabolism, with carbohydrate-active enzymes dominated by glycoside hydrolases (GHs) and glycosyltransferases (GTs), exhibiting overall functional conservation. Although populations shared many antibiotic- and virulence-related reference genetic markers, the marker composition associated with distinct resistance mechanisms and pathogenic processes exhibited clear population-specific patterns, suggesting differential microbial responses to local environmental pressures. Correlation network analysis further identified core taxa (e.g., Arthrobacter and Oscillospiraceae\/Bacteroidales lineages) as key genera linking community structure with core metabolic, resistance-related, and virulence-associated marker functions. Overall, the gut microbiota of Przewalski\u2019s gazelle exhibits a complex spatially structured functional differentiation, reflecting host\u2013microbiome co-adaptation under region-specific ecological pressures. These findings provide critical methodological and theoretical support for microecological health assessment and regionally informed conservation management of this endangered species.<\/jats:p>","DOI":"10.3390\/microorganisms13112513","type":"journal-article","created":{"date-parts":[[2025,11,3]],"date-time":"2025-11-03T13:55:22Z","timestamp":1762178122000},"page":"2513","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Metagenome-Based Functional Differentiation of Gut Microbiota and Ecological Adaptation Among Geographically Distinct Populations of Przewalski\u2019s Gazelle (Procapra przewalskii)"],"prefix":"10.3390","volume":"13","author":[{"given":"Jingjie","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Animal Ecological Genomics, Xining 810001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feng","family":"Jiang","sequence":"additional","affiliation":[{"name":"Qinghai Provincial Key Laboratory of Animal Ecological Genomics, Xining 810001, China"},{"name":"Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohuan","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6964-8273","authenticated-orcid":false,"given":"Pengfei","family":"Song","sequence":"additional","affiliation":[{"name":"Qinghai Provincial Key Laboratory of Animal Ecological Genomics, Xining 810001, China"},{"name":"Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tongzuo","family":"Zhang","sequence":"additional","affiliation":[{"name":"Qinghai Provincial Key Laboratory of Animal Ecological Genomics, Xining 810001, China"},{"name":"Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1017\/S0030605310001134","article-title":"Current status and conservation of the Endangered Przewalski\u2019s gazelle Procapra przewalskii, endemic to the Qinghai\u2013Tibetan Plateau, China","volume":"46","author":"Li","year":"2012","journal-title":"Oryx"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Zhang, J., Jiang, F., Cai, Z., Dai, Y., Liu, D., Song, P., Hou, Y., Gao, H., and Zhang, T. (2021). Resistance-based connectivity model to construct corridors of the Przewalski\u2019s gazelle (Procapra przewalskii) in fragmented landscape. Sustainability, 13.","DOI":"10.3390\/su13041656"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/nrgastro.2012.156","article-title":"The role of the gut microbiota in nutrition and health","volume":"9","author":"Flint","year":"2012","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Levin, D., Raab, N., Pinto, Y., Rothschild, D., Zanir, G., Godneva, A., Mellul, N., Futorian, D., Gal, D., and Leviatan, S. (2021). Diversity and functional landscapes in the microbiota of animals in the wild. Science, 372.","DOI":"10.1126\/science.abb5352"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Su, Q., Zhuang, D.H., Li, Y.C., Chen, Y., Wang, X.Y., Ge, M.X., Xue, T.Y., Zhang, Q.Y., Liu, X.Y., and Yin, F.Q. (2024). Gut microbiota contributes to high-altitude hypoxia acclimatization of human populations. Genome Biol., 25.","DOI":"10.1186\/s13059-024-03373-w"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Deng, F., Wang, C., Li, D., Peng, Y., Deng, L., Zhao, Y., Zhang, Z., Wei, M., Wu, K., and Zhao, J. (2023). The unique gut microbiome of giant pandas involved in protein metabolism contributes to the host\u2019s dietary adaption to bamboo. Microbiome, 11.","DOI":"10.1186\/s40168-023-01603-0"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Yao, X.Q., Bao, H., La, N.T., Jiang, G.S., Zhai, P.H., Liu, C.B., and Yu, L. (2025). Gut microbiota contribute to cold adaptation in mammals-primates and ungulates. iScience, 28.","DOI":"10.1016\/j.isci.2025.112245"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Zhang, J., Gao, H., Jiang, F., Liu, D., Hou, Y., Chi, X., Qin, W., Song, P., Cai, Z., and Zhang, T. (2022). Comparative Analysis of Gut Microbial Composition and Functions in Przewalski\u2019s Gazelle (Procapra przewalskii) From Various Habitats. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.913358"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zhang, J., Song, P., Jiang, F., and Zhang, T. (2024). Exploring the population interaction of Przewalski\u2019s gazelle (Procapra przewalskii) based on the variations in gut microbiota across diverse geographic populations. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1439554"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"fastp: An ultra-fast all-in-one FASTQ preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010). Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform., 11.","DOI":"10.1186\/1471-2105-11-119"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","article-title":"CD-HIT: Accelerated for clustering the next-generation sequencing data","volume":"28","author":"Fu","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1093\/bioinformatics\/btn025","article-title":"SOAP: Short oligonucleotide alignment program","volume":"24","author":"Li","year":"2008","journal-title":"Bioinformatics"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_16","first-page":"3215","article-title":"Analysis of the gut bacterial communities in beef cattle and their association with feed intake, growth, and efficiency","volume":"95","author":"Myer","year":"2016","journal-title":"J. Anim. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Auffret, M.D., Stewart, R.D., Dewhurst, R.J., Duthie, C.A., Watson, M., and Roehe, R. (2020). Identification of microbial genetic capacities and potential mechanisms within the rumen microbiome explaining differences in beef cattle feed efficiency. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.01229"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1038\/s41564-020-00861-0","article-title":"Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes","volume":"6","author":"Peng","year":"2021","journal-title":"Nat. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Xu, B., Song, P., Jiang, F., Cai, Z., Gu, H., Gao, H., Li, B., Liang, C., Qin, W., and Zhang, J. (2024). Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates. NPJ Biofilms Microbiomes, 10.","DOI":"10.1038\/s41522-024-00597-3"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Villasante, A., Ram\u00edrez, C., Rodr\u00edguez, H., Catal\u00e1n, N., D\u00edaz, O., Rojas, R., Opazo, R., and Romero, J. (2019). In-depth analysis of swim bladder-associated microbiota in rainbow trout (Oncorhynchus mykiss). Sci. Rep., 9.","DOI":"10.1038\/s41598-019-45451-1"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Song, J., Li, Q., Everaert, N., Liu, R., Zheng, M., Zhao, G., and Wen, J. (2020). Dietary Inulin Supplementation Modulates Short-Chain Fatty Acid Levels and Cecum Microbiota Composition and Function in Chickens Infected with Salmonella. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.584380"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1111\/1749-4877.12699","article-title":"Gut microbial community structure and function of Przewalski\u2019s horses varied across reintroduced sites in China","volume":"18","author":"Tang","year":"2023","journal-title":"Integr. Zool."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"17714","DOI":"10.1073\/pnas.1017956108","article-title":"Evidence of cellulose metabolism by the giant panda gut microbiome","volume":"108","author":"Zhu","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Yan, Z., He, X., Ayala, J., Xu, Q., Yu, X., Hou, R., Yao, Y., Huang, H., and Wang, H. (2023). The Impact of Bamboo Consumption on the Spread of Antibiotic Resistance Genes in Giant Pandas. Vet. Sci., 10.","DOI":"10.3390\/vetsci10110630"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1007\/s12602-023-10072-8","article-title":"Understanding the Effect of Compound Probiotics on the Health of Rabbits and Its Mechanisms Through Metagenomics","volume":"16","author":"Hou","year":"2024","journal-title":"Probiotics Antimicrob Proteins"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Jin, L., Wu, H., Li, G., Yang, S., Wei, R., Huang, Y., Penttinen, P., Deng, W., Chen, J., and Han, X. (2023). Gastrointestinal microbiome, resistance genes, and risk assessment of heavy metals in wild giant pandas. Sci. Total Environ., 15.","DOI":"10.1016\/j.scitotenv.2023.165671"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Huang, G., Qu, Q., Wang, M., Huang, M., Zhou, W., and Wei, F. (2022). Global landscape of gut microbiome diversity and antibiotic resistomes across vertebrates. Sci. Total Environ., 838.","DOI":"10.1016\/j.scitotenv.2022.156178"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Huang, H., Pang, X., Que, T., Chen, P., Li, S., Wu, A., He, M., Qiu, H., and Hu, Y. (2023). Antibiotic resistance profiles of gut microbiota across various primate species in Guangxi. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1309709"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Huang, R., Ji, X., Zhu, L., Zhang, C., Luo, T., Liang, B., Jiang, B., Zhou, A., Du, C., and Sun, Y. (2024). Metagenomic and Antibiotic Resistance Analysis of the Gut Microbiota in Larus relictus and Anatidae Species Inhabiting the Honghaizi Wetland of Ordos, Inner Mongolia, from 2021 to 2023. Microorganisms, 12.","DOI":"10.3390\/microorganisms12050978"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Li, D.H., Li, Z.W., Sun, Q., Wang, L., and Ning, S.B. (2024). Lower fecal microbiota transplantation ameliorates ulcerative colitis by eliminating oral-derived Fusobacterium nucleatum and virulence factor. Gut Pathog., 16.","DOI":"10.1186\/s13099-024-00633-9"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Wang, X., Shang, Y., Xing, Y., Chen, Y., Wu, X., and Zhang, H. (2025). Captive environments reshape the compositions of carbohydrate active enzymes and virulence factors in wolf gut microbiome. BMC Microbiol., 25.","DOI":"10.1186\/s12866-025-03863-2"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Ma, X., Hu, X., Liu, K., Wang, W., Jia, W., Gao, H., Lu, M., Liu, J., Chen, Y., and Ma, Y. (2024). Spatiotemporal differences induced changes in the structure and function of the gut microbiota in an endangered ungulate. Anim. Microbiome, 6.","DOI":"10.1186\/s42523-024-00362-z"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Karmacharya, D., Manandhar, P., Manandhar, S., Sherchan, A.M., Sharma, A.N., Joshi, J., Bista, M., Bajracharya, S., Awasthi, N.P., and Sharma, N. (2019). Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0221868"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/j.chom.2024.04.004","article-title":"Microbiota metabolism of intestinal amino acids impacts host nutrient homeostasis and physiology","volume":"32","author":"Li","year":"2024","journal-title":"Cell Host Microbe"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Sun, Y., Yu, Y., Wu, A., Zhang, C., Liu, X., Qian, C., Li, J., and Ran, J. (2023). The composition and function of the gut microbiota of Francois\u2019 langurs (Trachypithecus francoisi) depend on the environment and diet. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1269492"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1016\/j.jgg.2021.07.009","article-title":"Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins","volume":"48","author":"Liu","year":"2021","journal-title":"J. Genet. Genom."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Guo, W., Mishra, S., Wang, C., Zhang, H., Ning, R., Kong, F., Zeng, B., Zhao, J., and Li, Y. (2019). Comparative Study of Gut Microbiota in Wild and Captive Giant Pandas (Ailuropoda melanoleuca). Genes, 10.","DOI":"10.3390\/genes10100827"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2350785","DOI":"10.1080\/19490976.2024.2350785","article-title":"Diet-microbiota associations in gastrointestinal research: A systematic review","volume":"16","author":"Duncanson","year":"2024","journal-title":"Gut Microbes"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1038\/ismej.2009.112","article-title":"Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice","volume":"4","author":"Zhang","year":"2010","journal-title":"ISME J."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Ayayee, P.A., Kinney, G., Yarnes, C., Larsen, T., Custer, G.F., van Diepen, L.T.A., and Mu\u00f1oz-Garcia, A. (2020). Role of the gut microbiome in mediating standard metabolic rate after dietary shifts in the viviparous cockroach, Diploptera punctata. J. Exp. Biol., 223.","DOI":"10.1242\/jeb.218271"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1849","DOI":"10.1002\/art.41018","article-title":"Novel Inter-omic Analysis Reveals Relationships Between Diverse Gut Microbiota and Host Immune Dysregulation in HLA-B27-Induced Experimental Spondyloarthritis","volume":"71","author":"Gill","year":"2019","journal-title":"Arthritis Rheumatol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Wang, Y., Yang, X., Zhang, M., and Pan, H. (2023). Comparative Analysis of Gut Microbiota between Wild and Captive Golden Snub-Nosed Monkeys. Animals, 13.","DOI":"10.3390\/ani13101625"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"117186","DOI":"10.1016\/j.ecoenv.2024.117186","article-title":"Metagenomic profiling of cecal microbiota and antibiotic resistome in rodents","volume":"286","author":"Shang","year":"2024","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e0025223","DOI":"10.1128\/msystems.00252-23","article-title":"Age-related alterations in metabolome and microbiome provide insights in dietary transition in giant pandas","volume":"8","author":"Liu","year":"2023","journal-title":"mSystems"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Rohrer, S.D., Jim\u00e9nez-Uzc\u00e1tegui, G., Parker, P.G., and Chubiz, L.M. (2023). Composition and function of the Galapagos penguin gut microbiome vary with age, location, and a putative bacterial pathogen. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-31826-y"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/11\/2513\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,5]],"date-time":"2025-11-05T05:18:42Z","timestamp":1762319922000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/11\/2513"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,31]]},"references-count":45,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["microorganisms13112513"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13112513","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,31]]}}}