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Shift of Maternal Gut Microbiota of Tibetan Antelope (Pantholops hodgsonii) During the Periparturition Period

Current Microbiology volume 78, pages 727–738 (2021)Cite this article

Abstract

The maternal gut microbiota can influence and be affected by the substantial physiological changes taking place during the periparturition period. However, little information is known about the changes in the maternal gut microbiota and hormonal variations during this period in nonmodel organisms. Tibetan antelope (Pantholops hodgsonii) provide a unique system to address this issue because their summer migration cycle is synchronized with the periparturition period. Here, we used fecal microbiota as a proxy of gut microbiota. We characterized fecal microbial community of female migratory Tibetan antelope in the late pregnancy and postpartum periods using 16S rRNA gene sequencing and quantified fecal glucocorticoids (GCs) and triiodothyronine (T3) metabolite concentrations through enzyme immunoassays to identify the associations between maternal gut microbiota and physiological changes related with reproduction. We found that the fecal microbiota of Tibetan antelope was dominated by Firmicutes and Bacteroidetes. The microbial composition was significantly altered during the transition from late pregnancy to the postpartum period. Fecal T3 concentration was significantly higher in the postpartum period compared to late pregnancy, whereas GC metabolite concentration did not significantly differ between two reproductive states. We identified six genera (Anaerofustis, Bacteroides, Coprococcus_2, Ruminiclostridium_5, Ruminococcaceae_UCG-007, and Tyzzerella) that were significantly associated with reproductive states. We also found two genera (Christensenellaceae_R-7_group and Rikenellaceae_RC9_gut_group) significantly associated with GC metabolite concentration and two genera (Agathobacter and Papillibacter) significantly associated with T3 metabolite concentration, though these correlations were weak with coefficient values ranging from − 0.007 to 0.03. Our results indicate that many members of the gut microbiota are associated with the physiological changes in the transition from late pregnancy to the postpartum period, likely reflecting the metabolic and immune system dynamics during the periparturition period. This study highlights the importance of integrating microbiota, hormones and migration pattern to study the reproductive health of wildlife. By establishing a baseline of the physiological changes during the migration/periparturition period, we can have a better understanding of the impacts of increasing human activities on the Tibetan Plateau on the reproductive health of Tibetan antelope.

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Data Availability

Raw sequence reads (fastq.gz) used in this research along with corresponding metadata were archived in the NCBI Sequence Read Archive (BioProject ID: PRJNA673151) using the publicly accessible Genomic Observatories Metadatabase (GUID: https://n2t.net/ark:/21547/Dfw2). Scripts used in this study were deposited on Github (https://github.com/melodysyue/TibetanAntelope_Microbiome_Hormone). ASV sequences (fasta), ASV abundance table and taxonomic classification (tsv), and sample metadata information (csv) along with intermediate data files generated from various analyses were deposited in the same Github repository as well.

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Acknowledgements

We thank Rebecca Booth for advice on hormonal assays. We thank Kekexili Natural Nature Reserve Administration for assistance in the fieldwork. We thank Richard G. Olmstead, Noah Synder-Mackler, Hyeon Jeong Kim, and three anonymous reviewers for feedback that greatly improved the manuscript.

Funding

The study was funded by the China Scholarship Council (CSC) Graduate Research Fellowship, Fritz/Boeing International Research Fellowship, and WRF Hall Fellowship.

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  1. Yue Shi

    Present address: College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 17101 Point Lena Loop Road, Juneau, AK, 99801, USA

  2. Jian-Ping Su and Samuel K. Wasser are Co-last authors.

Authors and Affiliations

  1. Department of Biology, University of Washington, Box 351800, Seattle, WA, 98195, USA

    Yue Shi & Samuel K. Wasser

  2. Qinghai Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, No. 23 Xinning Road, Xining, 810008, Qinghai, China

    Zi-Yan Miao & Jian-Ping Su

  3. Museum of Natural Resources of Qinghai Province, Xining, 810008, Qinghai, China

    Zi-Yan Miao

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Contributions

YS involved in conceptualization, project administration, methodology, investigation, formal analysis, data curation, visualization, and writing-original draft; ZYM contributed to investigation and resources; JPS performed conceptualization, project administration, investigation, and supervision; SKW participated in conceptualization and writing-reviewing & editing.

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Correspondence to Yue Shi.

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Conflict of interest

The Authors and the legal representative of Jian-Ping Su declare that they have no conflicts of interest.

Ethical Approval

Tibetan antelope is listed in the Category I of the National Key Protected Wild Animal Species under China’s Wild Animal Protection Law. In September 2016, Tibetan antelope were reclassified from Endangered to Near Threatened by the International Union for Conservation of Nature (IUCN) Red List due to the recovery of their population size. Sample collection and field studies adhered to the Wild Animals Protection Law of the People’s Republic of China. Fresh scat samples were collected under University of Washington IACUC protocol #2850–12 and local regulations to minimize disturbance.

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Deceased Jian-Ping Su on 27 June 2018.

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Shi, Y., Miao, ZY., Su, JP. et al. Shift of Maternal Gut Microbiota of Tibetan Antelope (Pantholops hodgsonii) During the Periparturition Period. Curr Microbiol 78, 727–738 (2021). https://doi.org/10.1007/s00284-020-02339-y

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  • DOI: https://doi.org/10.1007/s00284-020-02339-y