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Fermentation Ability of Gut Microbiota of Wild Japanese Macaques in the Highland and Lowland Yakushima: In Vitro Fermentation Assay and Genetic Analyses

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Abstract

Wild Japanese macaques (Macaca fuscata Blyth) living in the highland and lowland areas of Yakushima are known to have different diets, with highland individuals consuming more leaves. We aim to clarify whether and how these differences in diet are also reflected by gut microbial composition and fermentation ability. Therefore, we conduct an in vitro fermentation assay using fresh feces from macaques as inoculum and dry leaf powder of Eurya japonica Thunb. as a substrate. Fermentation activity was higher for feces collected in the highland, as evidenced by higher gas and butyric acid production and lower pH. Genetic analysis indicated separation of highland and lowland in terms of both community structure and function of the gut microbiota. Comparison of feces and suspension after fermentation indicated that the community structure changed during fermentation, and the change was larger for lowland samples. Analysis of the 16S rRNA V3-V4 barcoding region of the gut microbiota showed that community structure was clearly clustered between the two areas. Furthermore, metagenomic analysis indicated separation by gene and pathway abundance patterns. Two pathways (glycogen biosynthesis I and D-galacturonate degradation I) were enriched in lowland samples, possibly related to the fruit-eating lifestyle in the lowland. Overall, we demonstrated that the more leaf-eating highland Japanese macaques harbor gut microbiota with higher leaf fermentation ability compared with the more fruit-eating lowland ones. Broad, non-specific taxonomic and functional gut microbiome differences suggest that this pattern may be driven by a complex interplay between many taxa and pathways rather than single functional traits.

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Data Availability

The nucleotide sequence data reported are available in the DDBJ database under the accession numbers DRA009238 and DRA009275.

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Acknowledgments

We would like to thank our friends and colleagues in Yakushima, the fellow students and staff who joined the Yakushima Field Science Course in the spring of 2016, and the administrative staff who made the course possible behind the scenes. Drs. Misako Yamazaki, Ayako Izuno, Catherine Aquino, Lucas Mohn, Sirisha Aluri, Sayaka Tsuchida, Masayuki Suzuki, and members of the Department of Evolutionary Biology and Environmental Studies, University of Zurich, and Functional Genomics Center Zurich helped us with genetic and SCFA analyses. The Sarugoya Committee and Wildlife Research Center of Kyoto University offered us excellent facilities for fieldwork. Permission to conduct this study was given by the Yakushima Forest Ecosystem Conservation Center and Kagoshima Prefecture.

Funding

The study was financed by the Leading Graduate Program of Primatology and Wildlife Science of Kyoto University, MEXT Grant-in-Aid for Promotion of Joint International Research (Fostering Joint International Research) (15KK0256 and 19KK0186) and for Scientific Research B (25291100 and 18H02508) to GH, and by the University Research Priority Program of Evolution in Action from University of Zurich.

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Authors and Affiliations

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

    Goro Hanya, Akiko Sawada, Wanyi Lee, Akito Toge, Kota Kuroki & Takashi Hayakawa

  2. Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland

    Janko Tackmann & Christian von Mering

  3. Chubu University Academy of Emerging Sciences, Kasugai, Japan

    Akiko Sawada & Kazunari Ushida

  4. Centre for Ecological Sciences, Indian Institute of Science, Bengaluru, India

    Sanjeeta Sharma Pokharel

  5. Amazon National Institute of Research, Manaus, Brazil

    Valdevino Gisele de Castro Maciel

  6. Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, Japan

    Ryoma Otsuka

  7. Graduate School of Science, Kyoto University, Kyoto, Japan

    Ryoma Mabuchi

  8. Wildlife Research Center, Kyoto University, Kyoto, Japan

    Jie Liu

  9. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

    Masaomi Hatakeyama, Eri Yamasaki, Rie Shimizu-Inatsugi & Kentaro K. Shimizu

  10. Functional Genomics Center Zurich, Zurich, Switzerland

    Masaomi Hatakeyama

  11. Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Japan

    Takashi Hayakawa

  12. Japan Monkey Centre, Inuyama, Japan

    Takashi Hayakawa

  13. Kihara Institute for Biological Research, Yokohama City University, Yokohama, Japan

    Kentaro K. Shimizu

Authors
  1. Goro Hanya
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  2. Janko Tackmann
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  6. Valdevino Gisele de Castro Maciel
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  7. Akito Toge
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Contributions

Goro Hanya, Akiko Sawada, Christian von Mering, Rie Shimizu-Inatsugi, Kentaro K. Shimizu, and Kazunari Ushida designed the research. Goro Hanya, Akiko Sawada, Sanjeeta Sharma Pokharel, Valdevino Gisele de Castro Maciel, Akito Toge, Kota Kuroki, Ryoma Otsuka, Ryoma Mabuchi, Jie Liu, Takashi Hayakawa, and Kazunari Ushida collected samples and performed the in vitro fermentation assay. Goro Hanya, Akiko Sawada, Wanyi Lee, Eri Yamasaki, Rie Shimizu-Inatsugi, and Takashi Hayakawa conducted the genetic analyses. Janko Tackmann and Masaomi Hatakeyama analyzed the sequence data. Goro Hanya wrote the manuscript.

Corresponding author

Correspondence to Goro Hanya.

Ethics declarations

During the fieldwork, we adhered to the “Guideline for field research of non-human primates” of the Primate Research Institute, Kyoto University. Furthermore, our procedure complied with ARRIVE guidelines for the use of animals in research (http://www.nc3rs.org.uk/ARRIVE), as well as the legal requirements of Japan. No prior consent from the Japanese government is required to export biological samples from Japan in the context of Convention on Biological Diversity (http://www.env.go.jp/en/nature/biodiv/abs/index.html).

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

During the fieldwork, we adhered to the “Guideline for field research of non-human primates” of the Primate Research Institute, Kyoto University. According to the guideline, our study is purely non-invasive and does not need approval from an ethical committee.

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Hanya, G., Tackmann, J., Sawada, A. et al. Fermentation Ability of Gut Microbiota of Wild Japanese Macaques in the Highland and Lowland Yakushima: In Vitro Fermentation Assay and Genetic Analyses. Microb Ecol 80, 459–474 (2020). https://doi.org/10.1007/s00248-020-01515-8

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