{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T15:48:50Z","timestamp":1753890530268,"version":"3.41.2"},"reference-count":51,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,5,28]],"date-time":"2024-05-28T00:00:00Z","timestamp":1716854400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Microbial community composition is closely associated with host disease onset and progression, underscoring the importance of understanding host\u2013microbiota dynamics in various health contexts.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>In this study, we utilized full-length 16S rRNA gene sequencing to conduct species-level identification of the microorganisms in the oral cavity of a giant panda (<jats:italic>Ailuropoda melanoleuca<\/jats:italic>) with oral malignant fibroma.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We observed a significant difference between the microbial community of the tumor side and non-tumor side of the oral cavity of the giant panda, with the latter exhibiting higher microbial diversity. The tumor side was dominated by specific microorganisms, such as <jats:italic>Fusobacterium simiae<\/jats:italic>, <jats:italic>Porphyromonas<\/jats:italic> sp. feline oral taxon 110, <jats:italic>Campylobacter<\/jats:italic> sp. feline oral taxon 100, and <jats:italic>Neisseria<\/jats:italic> sp. feline oral taxon 078, that have been reported to be associated with tumorigenic processes and periodontal diseases in other organisms. According to the linear discriminant analysis effect size analysis, more than 9 distinct biomarkers were obtained between the tumor side and non-tumor side samples. Furthermore, the Kyoto Encyclopedia of Genes and Genomes analysis revealed that the oral microbiota of the giant panda was significantly associated with genetic information processing and metabolism, particularly cofactor and vitamin, amino acid, and carbohydrate metabolism. Furthermore, a significant bacterial invasion of epithelial cells was predicted in the tumor side.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>This study provides crucial insights into the association between oral microbiota and oral tumors in giant pandas and offers potential biomarkers that may guide future health assessments and preventive strategies for captive and aging giant pandas.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fcimb.2024.1356907","type":"journal-article","created":{"date-parts":[[2024,5,28]],"date-time":"2024-05-28T05:29:36Z","timestamp":1716874176000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Oral microbiome sequencing revealed the enrichment of Fusobacterium sp., Porphyromonas sp., Campylobacter sp., and Neisseria sp. on the oral malignant fibroma surface of giant panda"],"prefix":"10.3389","volume":"14","author":[{"given":"Xiaowan","family":"Wang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Meiling","family":"Jing","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qizhao","family":"Ma","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yongwang","family":"Lin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ting","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiangchuan","family":"Yan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Libing","family":"Yun","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chengdong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuqing","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2024,5,28]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1186\/s40168-016-0169-y","article-title":"Diet may influence the oral microbiome composition in cats","volume":"4","author":"Adler","year":"2016","journal-title":"Microbiome"},{"key":"B2","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1111\/j.1461-0248.2006.00926.x","article-title":"Multivariate dispersion as a measure of beta diversity","volume":"9","author":"Anderson","year":"2006","journal-title":"Ecol. Lett."},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.1029","article-title":"Compact graphical representation of phylogenetic data and metadata with GraPhlAn","volume":"3","author":"Asnicar","year":"2015","journal-title":"Peerj"},{"key":"B4","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.jfms.2006.05.007","article-title":"Successful treatment of a localised CDC Group EF-4a infection in a cat","volume":"9","author":"Baral","year":"2007","journal-title":"J. Feline Med. Surg."},{"key":"B5","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1186\/s40168-018-0470-z","article-title":"Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2 \u2018 s q2-feature-classifier plugin","volume":"6","author":"Bokulich","year":"2018","journal-title":"Microbiome"},{"key":"B6","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","article-title":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"326","DOI":"10.2307\/1942268","article-title":"An ordination of the upland forest communities of southern wisconsin","volume":"27","author":"Bray","year":"1957","journal-title":"Ecol. Monogr."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1443","DOI":"10.1126\/science.aal5240","article-title":"Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer","volume":"358","author":"Bullman","year":"2017","journal-title":"Science"},{"key":"B9","first-page":"265","article-title":"Nonparametric-estimation of the number of classes in a population","volume":"11","author":"Chao","year":"1984","journal-title":"Scandinavian J. Stat"},{"key":"B10","doi-asserted-by":"publisher","first-page":"2252","DOI":"10.3390\/ijms22052252","article-title":"New insights into oral squamous cell carcinoma: from clinical aspects to molecular tumorigenesis","volume":"22","author":"Chen","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1111\/j.1442-9993.1993.tb00438.x","article-title":"Nonparametric multivariate analyses of changes in community structure","volume":"18","author":"Clarke","year":"1993","journal-title":"Aust. J. Ecol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.cvsm.2021.08.004","article-title":"Oral microbiome in dogs and cats: dysbiosis and the utility of antimicrobial therapy in the treatment of periodontal disease","volume":"52","author":"Davis","year":"2022","journal-title":"Vet. Clin. North Am. Small Anim. Pract."},{"key":"B13","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1038\/s41587-020-0548-6","article-title":"PICRUSt2 for prediction of metagenome functions","volume":"38","author":"Douglas","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"600","DOI":"10.1038\/s41568-023-00594-2","article-title":"Bacteria in cancer initiation, promotion and progression","volume":"23","author":"El Tekle","year":"2023","journal-title":"Nat. Rev. Cancer."},{"key":"B15","doi-asserted-by":"publisher","first-page":"6207","DOI":"10.3390\/ijms21176207","article-title":"Involvement of fusobacterium species in oral cancer progression: A literature review including other types of cancer","volume":"21","author":"Fujiwara","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1007\/978-1-4939-8728-3_8","article-title":"16S rRNA gene analysis with QIIME2","volume":"1849","author":"Hall","year":"2018","journal-title":"Methods Mol. Biol. (Clifton N.J.)"},{"key":"B17","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1001\/jamaoncol.2017.4777","article-title":"Association of oral microbiome with risk for incident head and neck squamous cell cancer","volume":"4","author":"Hayes","year":"2018","journal-title":"JAMA Oncol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1552","DOI":"10.1101\/gr.120618.111","article-title":"Integrative analysis of environmental sequences using MEGAN4","volume":"21","author":"Huson","year":"2011","journal-title":"Genome Res."},{"key":"B19","doi-asserted-by":"publisher","first-page":"849","DOI":"10.7589\/2014-12-289","article-title":"Dental abnormalities of eight wild qinling giant pandas (Ailuropoda melanoleuca qinlingensis), shaanxi province, China","volume":"51","author":"Jin","year":"2015","journal-title":"J. Wildl Dis."},{"key":"B20","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1016\/j.jcpa.2011.08.001","article-title":"Dental abnormalities in eight captive giant pandas (Ailuropoda melanoleuca) in China","volume":"146","author":"Jin","year":"2012","journal-title":"J. Comp. Pathol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"5029","DOI":"10.1038\/s41467-019-13036-1","article-title":"Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis","volume":"10","author":"Johnson","year":"2019","journal-title":"Nat. Commun."},{"key":"B22","doi-asserted-by":"publisher","first-page":"3059","DOI":"10.1093\/nar\/gkf436","article-title":"MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform","volume":"30","author":"Katoh","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"B23","doi-asserted-by":"publisher","first-page":"5271","DOI":"10.1111\/mec.12481","article-title":"Towards a unified paradigm for sequence-based identification of fungi","volume":"22","author":"Koljalg","year":"2013","journal-title":"Mol. Ecol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1111\/omi.12403","article-title":"Role of oral microbiome in oral oncogenesis, tumor progression, and metastasis","volume":"38","author":"Li","year":"2023","journal-title":"Mol. Oral. Microbiol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1099\/mic.0.000086","article-title":"Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus","volume":"161","author":"Liu","year":"2015","journal-title":"Microbiol. (Reading)"},{"key":"B26","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1177\/0022034520913248","article-title":"Structural and functional characteristics of the microbiome in deep-dentin caries","volume":"99","author":"Liu","year":"2020","journal-title":"J. Dental Res."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2022.866410","article-title":"The plaque microbiota community of giant panda (Ailuropoda melanoleuca) cubs with dental caries","volume":"12","author":"Ma","year":"2022","journal-title":"Front. Cell. Infection Microbiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1038\/nrgastro.2011.191","article-title":"The clinical importance of emerging Campylobacter species","volume":"8","author":"Man","year":"2011","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1890\/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2","article-title":"Fitting multivariate models to community data: A comment on distance-based redundancy analysis","volume":"82","author":"McArdle","year":"2001","journal-title":"Ecology"},{"key":"B30","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/0022-5193(66)90013-0","article-title":"Measurement of diversity in different types of biological collections","volume":"13","author":"Pielou","year":"1966","journal-title":"J. Theor. Biol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1641","DOI":"10.1093\/molbev\/msp077","article-title":"FastTree: computing large minimum evolution trees with profiles instead of a distance matrix","volume":"26","author":"Price","year":"2009","journal-title":"Mol. Biol. Evol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1186\/1471-2180-12-144","article-title":"Comparison of oral microbiota in tumor and non-tumor tissues of patients with oral squamous cell carcinoma","volume":"12","author":"Pushalkar","year":"2012","journal-title":"BMC Microbiol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1111\/fem.2007.62.issue-2","article-title":"Multivariate analyses in microbial ecology","volume":"62","author":"Ramette","year":"2007","journal-title":"FEMS Microbiol. Ecol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1016\/j.tim.2021.01.010","article-title":"Porphyromonas gingivalis","volume":"29","author":"Reyes","year":"2021","journal-title":"Trends Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","article-title":"Metagenomic biomarker discovery and explanation","volume":"12","author":"Segata","year":"2011","journal-title":"Genome Biol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1002\/bltj.1948.27.issue-4","article-title":"A mathematical theory of communication","volume":"27","author":"Shannon","year":"1948","journal-title":"Bell System Tech. J."},{"key":"B37","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1002\/bltj.1948.27.issue-3","article-title":"A mathematical theory of communication","volume":"27","author":"Shannon","year":"1948","journal-title":"Bell System Tech. J."},{"key":"B38","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1038\/163688a0","article-title":"Measurement of diversity","volume":"163","author":"Simpson","year":"1949","journal-title":"Nature"},{"key":"B39","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1007\/s10620-010-1263-9","article-title":"The role of oral hygiene in inflammatory bowel disease","volume":"56","author":"Singhal","year":"2011","journal-title":"Digestive Dis. Sci."},{"key":"B40","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1099\/00207713-32-2-191","article-title":"Fusobacterium-simiae, a new species from monkey dental plaque","volume":"32","author":"Slots","year":"1982","journal-title":"Int. J. Systematic Bacteriology"},{"key":"B41","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.semcancer.2021.11.002","article-title":"The oral microbiota and its role in carcinogenesis","volume":"86","author":"Stasiewicz","year":"2022","journal-title":"Semin. Cancer Biol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1186\/s12917-022-03300-w","article-title":"Characterization of the bacterial microbiota in different gut and oral compartments of splendid japalure (Japalura sensu lato)","volume":"18","author":"Tian","year":"2022","journal-title":"BMC Vet. Res."},{"key":"B43","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1186\/s40168-019-0717-3","article-title":"Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage","volume":"7","author":"Velsko","year":"2019","journal-title":"Microbiome"},{"key":"B44","doi-asserted-by":"publisher","first-page":"129","DOI":"10.4161\/gmic.1.3.11673","article-title":"What is black and white and a puzzle all over","volume":"1","author":"Viswanathan","year":"2010","journal-title":"Gut Microbes"},{"key":"B45","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1111\/j.2041-210X.2011.00127.x","article-title":"Distance-based multivariate analyses confound location and dispersion effects","volume":"3","author":"Warton","year":"2012","journal-title":"Methods Ecol. Evol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1280","DOI":"10.1016\/j.cub.2020.01.062","article-title":"Assessing the effectiveness of China\u2019s panda protection system","volume":"30","author":"Wei","year":"2020","journal-title":"Curr. Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1177\/0022034520909312","article-title":"Porphyromonas gingivalis promotes oral squamous cell carcinoma progression in an immune microenvironment","volume":"99","author":"Wen","year":"2020","journal-title":"J. Dent. Res."},{"key":"B48","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1111\/1462-2920.12502","article-title":"Oral cavity contains distinct niches with dynamic microbial communities","volume":"17","author":"Xu","year":"2014","journal-title":"Environ. Microbiol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1186\/1471-2180-9-259","article-title":"Defining the healthy \u201ccore microbiome\u201d of oral microbial communities","volume":"9","author":"Zaura","year":"2009","journal-title":"BMC Microbiol."},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2019.00476","article-title":"The oral microbiota may have influence on oral cancer","volume":"9","author":"Zhang","year":"2020","journal-title":"Front. Cell. Infection Microbiol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1016\/j.biopha.2018.01.146","article-title":"Human oral microbiota and its modulation for oral health","volume":"99","author":"Zhang","year":"2018","journal-title":"BioMed. Pharmacother."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1356907\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,28]],"date-time":"2024-05-28T05:29:40Z","timestamp":1716874180000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1356907\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,28]]},"references-count":51,"alternative-id":["10.3389\/fcimb.2024.1356907"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2024.1356907","relation":{},"ISSN":["2235-2988"],"issn-type":[{"type":"electronic","value":"2235-2988"}],"subject":[],"published":{"date-parts":[[2024,5,28]]},"article-number":"1356907"}}