Stomach and colonic microbiome of wild Japanese macaques.


Journal

American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949

Informations de publication

Date de publication:
05 2021
Historique:
revised: 18 01 2021
received: 30 04 2020
accepted: 31 01 2021
pubmed: 11 2 2021
medline: 25 11 2021
entrez: 10 2 2021
Statut: ppublish

Résumé

Within the gastrointestinal tract, the physiochemical microenvironments are highly diversified among the different stages of food digestion. Accordingly, gut microbiome composition and function vary at different gut sites. In this study, we examine and compare the compositional and functional potential between the stomach and colonic microbiome of wild Japanese macaques (Macaca fuscata yakui) living in the evergreen forest of Yakushima Island. We find a significantly lower microbial diversity in the stomach than in the colon, possibly due to the stomach's acidic and aerobic environment, which is suboptimal for microbial survival. According to past studies, the microbial taxa enriched in the stomach are aero- and acid-tolerant. By functional prediction through PICRUSt2, we reveal that the stomach microbiome is more enriched in pathways relating to the metabolism of simple sugars. On the contrary, the colonic microbiota is more enriched with fiber-degrading microbes, such as those from Lachnospiracea, Ruminococcaceae, and Prevotella. Our study shows a clear difference in the microbiome between the stomach and colon of Japanese macaques in both composition and function. This study provides a preliminary look at the alpha diversity and taxonomic composition within the stomach microbiome of Japanese macaques, a hindgut-fermenting nonhuman primate.

Identifiants

pubmed: 33566369
doi: 10.1002/ajp.23242
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23242

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Abranches, J., Zeng, L., Kajfasz, J. K., Palmer, S., Chakraborty, B., Wen, Z., & Lemos, J. A. (2019). Biology of oral Streptococci. In V. A. Fischetti, R. P. Novick, J. J. Ferretti, D. A. Portnoy, M. Braunstein, & J. I. Rood (Eds.), Gram-Positive Pathogens (pp. 426-434). John Wiley & Sons, Ltd. https://doi.org/10.1128/9781683670131.ch26
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. https://doi.org/10.1007/s00248-014-0554-7
Amato, K. R., Metcalf, J. L., Song, S. J., Hale, V. L., Clayton, J., Ackermann, G., Humphrey, G., Niu, K., Cui, D., Zhao, H., Schrenzel, M. D., Tan, C. L., Knight, R., & Braun, J. (2016). Using the gut microbiota as a novel tool for examining colobine primate GI health. Global Ecology and Conservation, 7, 225-237. https://doi.org/10.1016/j.gecco.2016.06.004
Biddle, A., Stewart, L., Blanchard, J., & Leschine, S. (2013). Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity, 5(3), 627-640. https://doi.org/10.3390/d5030627
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-Rodríguez, A. M., Chase, J., … Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8), 852-857. https://doi.org/10.1038/s41587-019-0209-9
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), 581-583. https://doi.org/10.1038/nmeth.3869
Camilleri, M., Colemont, L. J., Phillips, S. F., Brown, M. L., Thomforde, G. M., Chapman, N., & Zinsmeister, A. R. (1989). Human gastric emptying and colonic filling of solids characterized by a new method. The American Journal of Physiology, 257(2), G284-G290. https://doi.org/10.1152/ajpgi.1989.257.2.g284
Chen, T., Long, W., Zhang, C., Liu, S., Zhao, L., & Hamaker, B. R. (2017). Fiber-utilizing capacity varies in Prevotella-versus Bacteroides-dominated gut microbiota. Scientific Reports, 7(1), 2594. https://doi.org/10.1038/s41598-017-02995-4
Cizauskas, C. A. (2008). Zoo animal & wildlife immobilization and anesthesia. Journal of Wildlife Diseases, 44(2), 528-530. https://doi.org/10.7589/0090-3558-44.2.528
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. https://doi.org/10.1002/ajp.22867
Clayton, J. B., Shields-Cutler, R. R., Hoops, S. L., Al-Ghalith, G. A., Sha, J. C. M., Johnson, T. J., & Knights, D. (2019). Bacterial community structure and function distinguish gut sites in captive red-shanked doucs (Pygathrix nemaeus). American Journal of Primatology, 81(10-11), e22977. https://doi.org/10.1002/ajp.22977
Doel, J. J., Benjamin, N., Hector, M. P., Rogers, M., & Allaker, R. P. (2005). Evaluation of bacterial nitrate reduction in the human oral cavity. European Journal of Oral Sciences, 113(1), 14-19. https://doi.org/10.1111/j.1600-0722.2004.00184.x
Douglas, G. M., Maffei, V. J., Zaneveld, J., Yurgel, S. N., Brown, J. R., Taylor, C. M., Huttenhower, C., & Langille, M. G. I. (2019). PICRUSt2: An improved and extensible approach for metagenome inference. BioRxiv. https://doi.org/10.1101/672295
Gu, S., Chen, D., Zhang, J.-N., Lv, X., Wang, K., Duan, L.-P., Nie, Y., & Wu, X. L. (2013). Bacterial community mapping of the mouse gastrointestinal tract. PLOS One, 8(10), e74957. https://doi.org/10.1371/journal.pone.0074957
Hanya, G. (2004). Diet of a Japanese macaque troop in the coniferous forest of Yakushima. International Journal of Primatology, 25(1), 55-71. https://doi.org/10.1023/B:IJOP.0000014645.78610.32
Hanya, G., Kiyono, M., Takafumi, H., Tsujino, R., & Agetsuma, N. (2007). Mature leaf selection of Japanese macaques: Effects of availability and chemical content. Journal of Zoology, 273(2), 140-147. https://doi.org/10.1111/j.1469-7998.2007.00308.x
Hanya, G., Noma, N., & Agetsuma, N. (2003). Altitudinal and seasonal variations in the diet of Japanese macaques in Yakushima. Primates, 44(1), 51-59. https://doi.org/10.1007/s10329-002-0007-7
Hayakawa, T., Nathan, S. K. S. S., Stark, D. J., Saldivar, D. A. R., Sipangkui, R., Goossens, B., Tuuga, A., Clauss, M., Sawada, A., Fukuda, S., Imai, H., & Matsuda, I. (2018). First report of foregut microbial community in proboscis monkeys: Are diverse forests a reservoir for diverse microbiomes? Environmental Microbiology Reports, 10(6), 655-662. https://doi.org/10.1111/1758-2229.12677
Hayakawa, T., Sawada, A., Tanabe, A. S., Fukuda, S., Kishida, T., Kurihara, Y., Matsushima, K., Liu, J., Akomo-Okoue, E. F., Gravena, W., Kashima, M., Suzuki, M., Kadowaki, K., Suzumura, T., Inoue, E., Sugiura, H., Hanya, G., & Agata, K. (2018). Improving the standards for gut microbiome analysis of fecal samples: Insights from the field biology of Japanese macaques on Yakushima Island. Primates, 59(5), 423-436. https://doi.org/10.1007/s10329-018-0671-x
Hill, D. A. (1997). Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. American Journal of Primatology, 43(4), 305-320. https://doi.org/10.1002/(SICI)1098-2345(1997)43:4%3C305::AID-AJP2%3E3.0.CO;2-0
Hillman, E. T., Lu, H., Yao, T., & Nakatsu, C. H. (2017). Microbial ecology along the gastrointestinal tract. Microbes and Environments, 32(4), 300-313. https://doi.org/10.1264/jsme2.ME17017
Jandhyala, S. M., Talukdar, R., Subramanyam, C., Vuyyuru, H., Sasikala, M., & Reddy, D. N. (2015). Role of the normal gut microbiota. World Journal of Gastroenterology, 21(29), 8787-8803. https://doi.org/10.3748/wjg.v21.i29.8787
Kandlikar, G. S., Gold, Z. J., Cowen, M. C., Meyer, R. S., Freise, A. C., Kraft, N. J. B., Moberg-Parker, J., Sprague, J., Kushner, D. J., & Curd, E. E. (2018). Ranacapa: An R package and shiny web app to explore environmental DNA data with exploratory statistics and interactive visualizations. F1000Research, 7, 1734. https://doi.org/10.12688/f1000research.16680.1
Kurihara, Y., Kinoshita, K., Shiroishi, I., & Hanya, G. (2020). Seasonal variation in energy balance of wild Japanese macaques (Macaca fucata yakui) in a warm-temperate forest: A preliminary assessment in the coastal forest of Yakushima. Primates, 61(3), 427-442. https://doi.org/10.1007/s10329-020-00797-3
Lahti, L., & Shetty, S. (2012). Microbiome R package. http://microbiome.github.io/microbiome
Lambert, J. E. (1998). Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology, 7(1), 8-20. https://doi.org/10.1002/(SICI)1520-6505(1998)7:1%3C8::AID-EVAN3%3E3.0.CO;2-C
Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., Beiko, R. G., & Huttenhower, C. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology, 31(9), 814-821. https://doi.org/10.1038/nbt.2676
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. https://doi.org/10.1002/ajp.23072
Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., & Gordon, J. I. (2008). Worlds within worlds: Evolution of the vertebrate gut microbiota. Nature Reviews Microbiology, 6(10), 776-788. https://doi.org/10.1038/nrmicro1978
Li, D., Chen, H., Zhao, J., Zhang, H., & Chen, W. (2019). Potential functions of the gastrointestinal microbiome inhabiting the length of the rat digest tract. International Journal of Molecular Sciences, 20(5), 1232. https://doi.org/10.3390/ijms20051232
Li, H., Li, T., Berasategui, A., Rui, J., Zhang, X., Li, C., Xiao, Z., & Li, X. (2017). Gut region influences the diversity and interactions of bacterial communities in pikas (Ochotona curzoniae and Ochotona daurica). FEMS Microbiology Ecology, 93(12), fix149. https://doi.org/10.1093/femsec/fix149
Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D., & Dangl, J. L. (2013). Practical innovations for high-throughput amplicon sequencing. Nature Methods, 10(10), 999-1002. https://doi.org/10.1038/nmeth.2634
Matsuda, I., Chapman, C. A., & Clauss, M. (2019). Colobine forestomach anatomy and diet. Journal of Morphology, 280(11), 1608-1616. https://doi.org/10.1002/jmor.21052
McMurdie, P. J., & Holmes, S. (2013). Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLOS One, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
Merrell, D. S., Goodrich, M. L., Otto, G., Tompkins, L. S., & Falkow, S. (2003). pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infection and Immunity, 71(6), 3529-3539. https://doi.org/10.1128/IAI.71.6.3529-3539.2003
Meyer, W., Kacza, J., Schnapper, A., Verspohl, J., Hornickel, I., & Seeger, J. (2010). A first report on the microbial colonisation of the equine oesophagus. Annals of Anatomy, 192(1), 42-51. https://doi.org/10.1016/j.aanat.2009.10.004
Moon, C. D., Young, W., Maclean, P. H., Cookson, A. L., & Bermingham, E. N. (2018). Metagenomic insights into the roles of Proteobacteria in the gastrointestinal microbiomes of healthy dogs and cats. MicrobiologyOpen, 7(5), e00677. https://doi.org/10.1002/mbo3.677
Müller, M., Hermes, G. D. A., Canfora, E. E., Smidt, H., Masclee, A. A. M., Zoetendal, E. G., & Blaak, E. E. (2019). Distal colonic transit is linked to gut microbiota diversity and microbial fermentation in humans with slow colonic transit. American Journal of Physiology. Gastrointestinal and Liver Physiology, 318(2), G361-G369. https://doi.org/10.1152/ajpgi.00283.2019
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., & Wagner, H. (2019). Vegan: Community ecology package. https://CRAN.R-project.org/package=vegan
Primate Research Institute, Kyoto University (KUPRI). (2010). Guidelines for care and use of nonhuman primates. https://www.pri.kyoto-u.ac.jp/research/sisin2010/Guidelines_for_Care_and_Use_of_Nonhuman_Primates20100609.pdf
Reed, A., Pigage, J. C., Pigage, H. K., Glickman, C., & Bono, J. M. (2019). Comparative analysis of microbiota along the length of the gastrointestinal tract of two tree squirrel species (Sciurus aberti and S. niger) living in sympatry. Ecology and Evolution, 9(23), 13344-13358. https://doi.org/10.1002/ece3.5789
Roager, H. M., Hansen, L. B. S., Bahl, M. I., Frandsen, H. L., Carvalho, V., Gøbel, R. J., Dalgaard, M. D., Plichta, D. R., Sparholt, M. H., Vestergaard, H., Hansen, T., Sicheritz-Pontén, T., Nielsen, H. B., Pedersen, O., Lauritzen, L., Kristensen, M., Gupta, R., & Licht, T. R. (2016). Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nature Microbiology, 1(9), 16093. https://doi.org/10.1038/nmicrobiol.2016.93
Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology, 31(1), 107-133. https://doi.org/10.1146/annurev.mi.31.100177.000543
Seedorf, H., Griffin, N. W., Ridaura, V. K., Reyes, A., Cheng, J., Rey, F. E., Smith, M. I., Simon, G. M., Scheffrahn, R. H., Woebken, D., Spormann, A. M., Van Treuren, W., Ursell, L. K., Pirrung, M., Robbins-Pianka, A., Cantarel, B. L., Lombard, V., Henrissat, B., Knight, R., & Gordon, J. I. (2014). Bacteria from diverse habitats colonize and compete in the mouse gut. Cell, 159(2), 253-266. https://doi.org/10.1016/j.cell.2014.09.008
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12, R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shin, N.-R., Whon, T. W., & Bae, J.-W. (2015). Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends in Biotechnology, 33(9), 496-503. https://doi.org/10.1016/j.tibtech.2015.06.011
Stevens, C. E., & Hume, I. D. (1998). Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews, 78(2), 393-427. https://doi.org/10.1152/physrev.1998.78.2.393
Sun, B., Wang, X., Bernstein, S., Huffman, M. A., Xia, D.-P., Gu, Z., Chen, R., Sheeran, L. K., Wagner, R. S., & Li, J. (2016). Marked variation between winter and spring gut microbiota in free-ranging Tibetan macaques (Macaca thibetana). Scientific Reports, 6(1), 26035. https://doi.org/10.1038/srep26035
Vega, N. M. (2019). Experimental evolution reveals microbial traits for association with the host gut. PLOS Biology, 17(2), e3000129. https://doi.org/10.1371/journal.pbio.3000129
Walter, J. (2008). Ecological role of Lactobacilli in the gastrointestinal tract: Implications for fundamental and biomedical research. Applied and Environmental Microbiology, 74(16), 4985-4996. https://doi.org/10.1128/AEM.00753-08
Yumoto, T., Noma, N., & Maruhashi, T. (1998). Cheek-pouch dispersal of seeds by Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates, 39, 325-338. https://doi.org/10.1007/bf02573081

Auteurs

Wanyi Lee (W)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Takashi Hayakawa (T)

Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido, Japan.
Japan Monkey Centre, Inuyama, Aichi, Japan.

Yosuke Kurihara (Y)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.
Center for Education and Research in Field Sciences, Faculty of Agriculture, Shizuoka University, Hamamatsu, Japan.

Maho Hanzawa (M)

Department of Zoology, Graduate School of Science, Kyoto University, Kyoto, Japan.

Akiko Sawada (A)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.
Academy of Emerging Sciences, Chubu University, Kasugai, Aichi, Japan.

Akihisa Kaneko (A)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Yoshiki Morimitsu (Y)

Institute of Natural and Environmental Sciences, University of Hyogo, Sanda, Hyogo, Japan.

Takayoshi Natsume (T)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Seitaro Aisu (S)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Tsuyoshi Ito (T)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Takeaki Honda (T)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Goro Hanya (G)

Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH