Characterization of the Oral Microbiota in Captive Sichuan Golden Snub-nosed Monkeys (Rhinopithecus roxellana) of Different Ages

Springer Science and Business Media LLC - Tập 44 - Trang 1149-1165 - 2023
Rong Chen1, Xinyi Liu2, Meirong Li1, Xiaojuan Xu1, Ran Lv1, Yuanyuan Chen1, Guodong Wang1, Changlin Deng1, Nan Chen1, Ting Jia3, Siteng Wang2, Guangjin Liu2,4
1Nanjing Hongshan Forest Zoo, Nanjing, China
2College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China
3Beijing Zoo, Beijing, China
4Department of Preventive Veterinary Medicine, Nanjing Agricultural University, Nanjing, China

Tóm tắt

The oral microbiota is essential for the maintenance of oral and systemic health but is poorly characterized in primates. We used positive reinforcement training to collect 20 oral samples from three infant, ten juvenile/subadult, and seven adult Sichuan golden snub-nosed monkeys (Rhinopithecus roxellana). We subjected these samples to 16S rRNA high-throughput sequencing, as well as bacterial culture and identification. The 16S rRNA sequencing data showed the diversity of the oral flora did not differ significantly across these three age groups, while at the phyla level, the dominant flora in the oral cavity were Firmicutes and Proteobacteria (totaling 77.62%), and the relative abundance of Firmicutes in the adults was significantly higher than in the juvenile/subadults. Meanwhile, Enterococcus was the most abundant genus in this population, and there was no significant difference in the oral flora at the genus level across the age groups. We also isolated several opportunistic pathogenic bacteria in the oral samples from noninfant, Sichuan golden snub-nosed monkeys. Although our sample size is small, particularly for infants, our study describes the characteristics of oral flora in captive, Sichuan golden snub-nosed monkeys of different age groups and provides important information about possibly pathogenic bacteria.

Tài liệu tham khảo

Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I., & Dewhirst, F. E. (2005). Defining the normal bacterial flora of the oral cavity. Journal of Clinical Microbiology, 43(11), 5721–5732. https://doi.org/10.1128/Jcm.43.11.5721-5732.2005 Amos, G. C. A., Logan, A., Anwar, S., Fritzsche, M., Mate, R., Bleazard, T., & Rijpkema, S. (2020). Developing standards for the microbiome field. Microbiome, 8(1). ARTN 98. https://doi.org/10.1186/s40168-020-00856-3 Belda-Ferre, P., Alcaraz, L. D., Cabrera-Rubio, R., Romero, H., Simon-Soro, A., Pignatelli, M., & Mira, A. (2012). The oral metagenome in health and disease. Isme Journal, 6(1), 46–56. https://doi.org/10.1038/ismej.2011.85 Bik, E. M., Long, C. D., Armitage, G. C., Loomer, P., Emerson, J., Mongodin, E. F., Nelson, K. E., Gill, S. R., Fraser-Liggett, C. M., & Relman, D. A. (2010). Bacterial diversity in the oral cavity of 10 healthy individuals. Isme Journal, 4(8), 962–974. https://doi.org/10.1038/ismej.2010.30 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 improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10(1), 57-U11. https://doi.org/10.1038/Nmeth.2276 Boleij, A., van Gelder, M. M., Swinkels, D. W., & Tjalsma, H. (2011). Clinical Importance of Streptococcus gallolyticus infection among colorectal cancer patients: Systematic review and meta-analysis. Clin Infect Dis, 53(9), 870–878. https://doi.org/10.1093/cid/cir609 Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J. E., Bittinger, K., Brejnrod, A., Brislawn, C. J., Brown, C. T., Callahan, B. J., Caraballo-Rodriguez, A. M., Chase, J., . . . Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 (vol 37, pg 852, 2019). Nature Biotechnology, 37(9), 1091–1091. https://doi.org/10.1038/s41587-019-0252-6 Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-+. https://doi.org/10.1038/Nmeth.3869 Chen, B. Y., Lin, W. Z., Li, Y. L., Bi, C., Du, L. J., Liu, Y., Zhou, L. J., Liu, T., Xu, S., Shi, C. J., Zhu, H., Wang, Y. L., Sun, J. Y., Liu, Y., Zhang, W. C., Lu, H. X., Wang, Y. H., Feng, Q., Chen, F. X., . . . Duan, S. Z. (2023). Roles of oral microbiota and oral-gut microbial transmission in hypertension. Journal of Advanced Research, 43, 147–161. https://doi.org/10.1016/j.jare.2022.03.007 Cheng, X., Xin, X., Zhou, X. (2017). Relationship between oral and gut microbes. West China Journal of Stomatology, 35(3), 322–327. https://doi.org/10.7518/hxkq.2017.03.017 Costalonga, M., & Herzberg, M. C. (2014). The oral microbiome and the immunobiology of periodontal disease and caries. Immunology Letters, 162(2), 22–38. https://doi.org/10.1016/j.imlet.2014.08.017 Dmitrenko, O. A., Balbutskaya, A. A., & Skvortsov, V. N. (2016). [Specific Features of Ecology, Pathogenic Properties, and Role of the Staphylococcus Intermedius Group Members in Animal and Human Infectious Pathology.]. Mol Gen Mikrobiol Virusol, 34(3), 83–89. https://www.ncbi.nlm.nih.gov/pubmed/30383929 Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America, 107(26), 11971–11975. https://doi.org/10.1073/pnas.1002601107 Dunn, O. J. (1964). Multiple Comparisons Using Rank Sums. Technometrics, 6, 241–252. Dzidic, M., Collado, M. C., Abrahamsson, T., Artacho, A., Stensson, M., Jenmalm, M. C., & Mira, A. (2018). Oral microbiome development during childhood: An ecological succession influenced by postnatal factors and associated with tooth decay. Isme Journal, 12(9), 2292–2306. https://doi.org/10.1038/s41396-018-0204-z Ebersole, J. L., Holt, S. C., & Delaney, J. E. (2014). Acquisition of Oral Microbes and Associated Systemic Responses of Newborn Nonhuman Primates. Clinical and Vaccine Immunology, 21(1), 21–28. https://doi.org/10.1128/Cvi.00291-13 Fakhruddin, K. S., Ngo, H. C., & Samaranayake, L. P. (2019). Cariogenic microbiome and microbiota of the early primary dentition: A contemporary overview. Oral Diseases, 25(4), 982–995. https://doi.org/10.1111/odi.12932 Gizani, S., Papaioannou, W., Haffajee, A. D., Kavvadia, K., Quirynen, M., & Papagiannoulis, L. (2009). Distribution of selected cariogenic bacteria in five different intra-oral habitats in young children. International Journal of Paediatric Dentistry, 19(3), 193–200. https://doi.org/10.1111/j.1365-263X.2008.00956.x Gomez-Arango, L. F., Barrett, H. L., McIntyre, H. D., Callaway, L. K., Morrison, M., & Nitert, M. D. (2017). Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. Scientific Reports, 7(1), 2860. https://doi.org/10.1038/s41598-017-03066-4 Gopalakrishnan, V., Spencer, C. N., Nezi, L., Reuben, A., Andrews, M. C., Karpinets, T. V., Prieto, P. A., Vicente, D., Hoffman, K., Wei, S. C., Cogdill, A. P., Zhao, L., Hudgens, C. W., Hutchinson, D. S., Manzo, T., de Macedo, M. P., Cotechini, T., Kumar, T., Chen, W. S., . . . Wargo, J. A. (2018). Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science, 359(6371), 97–103. https://doi.org/10.1126/science.aan4236GraphPad Software. In. (2020). www.graphpad.com Human Microbiome Project, C. (2012). Structure, function and diversity of the healthy human microbiome. Nature, 486(7402), 207-214.https://doi.org/10.1038/nature11234 Hung, W., SP, T., HJ, C., Tsai, J.-C., Chang, C.-H., Lee, T.-F., Hsueh, P.-R., & Teng, L.-J. (2010). Use of groesl as a targetfot identification of Abiotrophia. Journal of Clinical Microbiology, 48(10), 3532–3538. https://doi.org/10.1128/JCM.00787-10 Kang, C. W., Pu, X. B., Tan, G., Dong, C. C., Yan, Z. K., & Wu, L. X. (2022). Streptococcus gordonii finger infection: Case report and a review of the literature. Medicine (Baltimore), 101(51), e32506. https://doi.org/10.1097/MD.0000000000032506 Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059–3066. https://doi.org/10.1093/nar/gkf436 Kirkpatrick, R., & Grueter, C. (2010). Snub-Nosed Monkeys: Multilevel Societies Across Varied Environments. Evolutionary Anthropology: Issues, News, and Reviews, 19, 98–113. https://doi.org/10.1002/evan.20259 Le Floch, A. S., Cassir, N., Hraiech, S., Guervilly, C., Papazian, L., & Rolain, J. M. (2013). Haemophilus parahaemolyticus septic shock after aspiration pneumonia, France. Emerging Infectious Diseases, 19(10), 1694–1695. https://doi.org/10.3201/eid1910.130608 Li, X., Trivedi, U., Brejnrod, A. D., Vestergaard, G., Mortensen, M. S., Bertelsen, M. F., & Sorensen, S. J. (2020). The microbiome of captive hamadryas baboons. Animal Microbiome, 2(1), 25. https://doi.org/10.1186/s42523-020-00040-w Liu, X. (2016). Golden monkey husbandry guideline China Agricultural Press. Lozupone, C., & Knight, R. (2005). UniFrac: A new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology, 71(12), 8228–8235. https://doi.org/10.1128/Aem.71.12.8228-8235.2005 Lozupone, C. A., Hamady, M., Kelley, S. T., & Knight, R. (2007). Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology, 73(5), 1576–1585. https://doi.org/10.1128/Aem.01996-06 McArdle, B. H., & Anderson, M. J. (2001). Fitting Multivariate Models to Community Data: A Comment on Distance-Based Redundancy Analysis. Ecology, 82(1), 290–297. https://doi.org/10.1890/0012-9658(2001)082[0290:Fmmtcd]2.0.Co;2 Nakamura, Y., Uemura, T., Kawata, Y., Hirose, B., Yamauchi, R., & Shimohama, S. (2021). Streptococcus oralis Meningitis with Gingival Bleeding in a Patient: A Case Report and Review of the Literature. Internal Medicine, 60(5), 789–793. https://doi.org/10.2169/internalmedicine.5628-20 Ozga, A. T., Gilby, I., Nockerts, R. S., Wilson, M. L., Pusey, A., & Stone, A. C. (2019). Oral microbiome diversity in chimpanzees from Gombe National Park. Scientific Reports, 9. ARTN 17354. https://doi.org/10.1038/s41598-019-53802-1 Payette, F., Charlebois, A., Fairbrother, J. H., Beauchamp, G., & Leclere, M. (2021). Nicoletella semolina in the airways of healthy horses and horses with severe asthma. Journal of Veterinary Internal Medicine, 35(3), 1612–1619. https://doi.org/10.1111/jvim.16140 Periasamy, S., & Kolenbrander, P. E. (2010). Central Role of the Early Colonizer Veillonella sp in Establishing Multispecies Biofilm Communities with Initial, Middle, and Late Colonizers of Enamel. Journal of Bacteriology, 192(12), 2965–2972. https://doi.org/10.1128/Jb.01631-09 Price, M. N., Dehal, P. S., & Arkin, A. P. (2009). FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix. Molecular Biology and Evolution, 26(7), 1641–1650. https://doi.org/10.1093/molbev/msp077 Qian, Y., Yu, H., Yuan, W., Wu, J., Xu, Q., Mei, N., Wang, X., & Wang, C. (2020). Alveolar Bone Loss, Tooth Loss and Oral Cancer Mortality in Older Patients: A Retrospective Cohort Study. Clinical Interventions Aging, 15, 1419–1425. https://doi.org/10.2147/CIA.S263947 Ramette, A. (2007). Multivariate analyses in microbial ecology. Fems Microbiology Ecology, 62(2), 142–160. https://doi.org/10.1111/j.1574-6941.2007.00375.x Ross, I., & Robert, G. (1996). R: A Language for Data Analysis and Graphics. Journal of Computational and Graphical Statistics, 5(3), 299–314. Said, H. S., Suda, W., Nakagome, S., Chinen, H., Oshima, K., Kim, S., Kimura, R., Iraha, A., Ishida, H., Fujita, J., Mano, S., Morita, H., Dohi, T., Oota, H., & Hattori, M. (2014). Dysbiosis of salivary microbiota in inflammatory bowel disease and its association with oral immunological biomarkers. DNA Research, 21(1), 15–25. https://doi.org/10.1093/dnares/dst037 Sawaswong, V., Praianantathavorn, K., Chanchaem, P., Khamwut, A., Kemthong, T., Hamada, Y., Malaivijitnond, S., & Payungporn, S. (2021). Comparative analysis of oral-gut microbiota between captive and wild long-tailed macaque in Thailand. Scientific Reports, 11(1), 14280. https://doi.org/10.1038/s41598-021-93779-4 Schloss, P. D., & Handelsman, J. (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied Environmental Microbiology, 71(3), 1501–1506. https://doi.org/10.1128/AEM.71.3.1501-1506.2005 Selwitz, R. H., Ismail, A. I., & Pitts, N. B. (2007). Dental caries. Lancet, 369(9555), 51–59. https://doi.org/10.1016/S0140-6736(07)60031-2 Sharma, K., Mudgil, P., Whitehall, J. S., & Gosbell, I. (2017). Aggregatibacter actinomycetemcomitans osteomyelitis in a 12 year old boy: Case report emphasizing the importance of tissue culture, and review of literature. Annals of Clinical Microbiology and Antimicrobiology, 16(1), 12. https://doi.org/10.1186/s12941-017-0186-0 Supriya Kheur, Aneesha Acharya, Mohit Kheur, Vinay Jain , & Hazarey, V. K. (2022). In S. Routray (Ed.), Microbes and Oral Squamous Cell Carcinoma. Springer Singapore. https://doi.org/10.1007/978-981-19-0592-6 Takehara, S., Zeredo, J. L., Kumei, Y., Kagiyama, K., Fukasawa, K., Oshiro, A., Ueno, M., Kojimahara, N., Minakuchi, S., & Kawaguchi, Y. (2019). Characterization of oral microbiota in marmosets: Feasibility of using the marmoset as a human oral disease model. PLoS One, 14(2), e0207560. https://doi.org/10.1371/journal.pone.0207560 Thatrimontrichai, A., Chanvitan, P., Janjindamai, W., Dissaneevate, S., & Maneenil, G. (2012). Early onset neonatal bacterial meningitis caused by Streptococcus gallolyticus subsp. paste urianus. Southeast Asian Journal of Tropical Medicine Public Health, 43(1), 145–151. https://www.ncbi.nlm.nih.gov/pubmed/23082565 Torre, D., Ferraro, G., Fiori, G. P., Martegani, R., Speranza, F., Tambini, R., & Zeroli, C. (1992). Ventriculoatrial shunt infection caused by Staphylococcus warneri: Case report and review. Clinical Infectious Diseases, 14(1), 49–52. https://doi.org/10.1093/clinids/14.1.49 Tribble, G. D., & Lamont, R. J. (2010). Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontology, 52, 68–83. https://doi.org/10.1111/j.1600-0757.2009.00323.x Vavricka, S. R., Manser, C. N., Hediger, S., Vogelin, M., Scharl, M., Biedermann, L., Rogler, S., Seibold, F., Sanderink, R., Attin, T., Schoepfer, A., Fried, M., Rogler, G., & Frei, P. (2013). Periodontitis and gingivitis in inflammatory bowel disease: A case-control study. Inflammatory Bowel Diseases, 19(13), 2768–2777. https://doi.org/10.1097/01.MIB.0000438356.84263.3b Verma, D., Garg, P. K., & Dubey, A. K. (2018). Insights into the human oral microbiome. Archives of Microbiology, 200(4), 525–540. https://doi.org/10.1007/s00203-018-1505-3 Whittaker, R. H. (1972). Evolution and Measurement of Species Diversity. Taxon, 21(2–3), 213–251. https://doi.org/10.2307/1218190 William Kruskal, & Wallis, W. A. (1952). Use of Ranks in One-Criterion Variance Analysis. Journal of the American Statistical Association, 47(260), 583–621. https://doi.org/10.1080/01621459.1952.10483441 Xiao, J., Fiscella, K. A., & Gill, S. R. (2020). Oral microbiome: Possible harbinger for children’s health. International Journal of Oral Science, 12(1), 12. https://doi.org/10.1038/s41368-020-0082-x Yang, S. C., Lin, C. H., Aljuffali, I. A., & Fang, J. Y. (2017). Current pathogenic Escherichia coli foodborne outbreak cases and therapy development. Archives of Microbiology, 199(6), 811–825. https://doi.org/10.1007/s00203-017-1393-y Yao, L., Li, X., Zhou, Z., Shi, D., Li, Z., Li, S., Yao, H., Yang, J., Yu, H., & Xiao, Y. (2021). Age-Based Variations in the Gut Microbiome of the Shennongjia (Hubei) Golden Snub-Nosed Monkey (Rhinopithecus roxellana hubeiensis). Biomedical Research International, 2021, 6667715. https://doi.org/10.1155/2021/6667715 Yongcheng, L., & Richardson, M. (2021). Rhinopithecus roxellana (amended version of 2020 assessment). The IUCN Red List https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T19596A196491153.en Zhang, Z., Su, Y., Chan, R. C., & Reimann, G. (2008). A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). American Journal of Primatology, 70(2), 148–152. https://doi.org/10.1002/ajp.20466 Zhu, B., Macleod, L. C., Kitten, T., & Xu, P. (2018). Streptococcus sanguinis biofilm formation & interaction with oral pathogens. Future Microbiology, 13(8), 915–932. https://doi.org/10.2217/fmb-2018-0043