Skip to main content

Alteration of Gut Microbiota of a Food-Storing Hibernator, Siberian Chipmunk Tamias sibiricus

Abstract

Hibernation represents a state of fasting because hibernators cease eating in the torpid periods. Therefore, food deprivation during hibernation is expected to modify the gut microbiota of host. However, there are few reports of gut microbiota in food-storing hibernators that feed during the interbout arousals. Here we collected fecal samples of Siberian chipmunk T. sibiricus to character and examine changes in the gut microbiota at various stages relative to hibernation: pre-hibernation, early-hibernation, mid-hibernation, late-hibernation, and post-hibernation. Compared to the pre-hibernation state, alpha-diversity of gut microbiota was significantly increased during the interbout arousal periods. In addition, beta-diversity of the fecal communities from pre-hibernation and interbout arousal periods grouped together, and post-hibernation gut microbiota resembled the counterpart at late-hibernation. Hibernation significantly decreased the relative abundance of Firmicutes but increased Bacteroidetes, reflecting a shift of microbiota toward taxa in favor of host-derived substrates. The increased abundance of Ruminococcaceae_UCG-014, Lactobacillus, and Christensenellaceae_R-7_group in gut microbiota may help the chipmunks reduce intestinal inflammation and then maintain healthy bowel during hibernation. KEGG pathway indicated that hibernation altered the metabolic function of gut microflora of T. sibiricus. Our study provides evidence that the gut microbiota of food-storing hibernators, despite feeding during the interbout arousals, shows similar response to hibernation that has well documented in fat-storing counterparts, suggesting the potential for a core gut microbiota during hibernation of mammals. Importantly, these results will broaden our understanding of the effects of hibernation on gut microbiota of mammal hibernators.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data availability

Sequence data that support the findings of this study have been deposited in the National Center for Biotechnology Information (NCBI) with the Sequence Read Archive (SRA) accession number PRJNA760982 (72 data: include triplicate of pre-hibernation, early-hibernation, mid-hibernation, late-hibernation, and post-arousal).

References

  1. 1.

    Malinicová L, Hamarová L, Maxinová E, Uhrin M, Pristas P (2017) The dynamics of Mediterranean horseshoe bat (Rhinolophus euryale, Chiroptera) gut microflora during hibernation. Acta Chiropterol 19:211–218

    Article  Google Scholar 

  2. 2.

    Weng CH, Yang YJ, Wang D (2016) Functional analysis for gut microbes of the brown tree frog (Polypedates megacephalus) in artificial hibernation. BMC Genomics 17:1024

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. 3.

    Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    PubMed  Article  PubMed Central  Google Scholar 

  5. 5.

    Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926

    PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966

    Article  Google Scholar 

  8. 8.

    Florant GL (1998) Lipid metabolism in hibernators: the importance of essential fatty acids. Am Zool 38:331–340

    CAS  Article  Google Scholar 

  9. 9.

    Andrews MT, Russeth KP, Drewes LR, Henry PG (2009) Adaptive mechanisms regulate preferred utilization of ketones in the heart and brain of a hibernating mammal during arousal from torpor. Am J Physiol Regul Integr Comp Physiol 296:R383–R393

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  10. 10.

    Thomas DW, Munro D, Humphries MM (2008) Extreme suppression of aboveground activity by a food-storing hibernator, the eastern chipmunk (Tamias striatus). Can J Zool 86:364–370

    Article  Google Scholar 

  11. 11.

    Sonoyama K, Fujiwara R, Takemura N, Ogasawara T, Watanabe J, Ito H, Morita T (2009) Response of gut microbiota to fasting and hibernation in Syrian hamsters. Appl Environ Microbiol 75:6451–6456

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Carey HV, Walters WA, Knight R (2013) Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. Am J Physiol Regul Integr Comp Physiol 304:R33–R42

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Michener GR (1992) Sexual differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernation. Oecologia 89:397–406

    PubMed  Article  Google Scholar 

  14. 14.

    Healy JE, Ostrom CE, Wilkerson GK, Florant GL (2010) Plasma ghrelin concentrations change with physiological state in a sciurid hibernator (Spermophilus lateralis). Gen Comp Endocrinol 166:372–378

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Ren Y, Song SY, Liu XY, Yang M (2020) Phenotypic changes in the metabolic profile and adiponectin activity during seasonal fattening and hibernation in female Daurian ground squirrels (Spermophilus dauricus). Integr Zool. https://doi.org/10.1111/1749-4877.12504

    Article  PubMed  Google Scholar 

  16. 16.

    Concannon P, Levac K, Rawson R, Tennant B, Bensadoun A (2001) Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am J Physiol Regul Integr Comp Physiol 281:951–959

    Article  Google Scholar 

  17. 17.

    Carey HV, Pike AC, Weber CR, Turner JR, Visser A, Beijer-Liefers SC, Rouma HR, Kroese FGM (2012) Impact of hibernation on gut microbiota and intestinal barrier function in ground squirrels. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world. Springer, Berlin, pp 281–291

    Chapter  Google Scholar 

  18. 18.

    Gazzard A, Baker PJ (2020) Patterns of feeding by householders affect activity of hedgehogs (Erinaceus europaeus) during the hibernation period. Animals 10:1344

    PubMed Central  Article  PubMed  Google Scholar 

  19. 19.

    Sommer F, Ståhlman M, Ilkayeva O, Arnemo JM, Kindberg J, Josefsson J, Bäckhed F (2016) The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep 14:1655–1661

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386

    Article  Google Scholar 

  21. 21.

    Buck CL, Barnes BM (1999) Annual cycle of body composition and hibernation in free-living arctic ground squirrels. J Mammal 80:430–442

    Article  Google Scholar 

  22. 22.

    Gillis EA, Morrison SF, Zazula GD, Hik DS (2005) Evidence for selective caching by arctic ground squirrels living in alpine meadows in the Yukon. Arctic 59:354–360

    Google Scholar 

  23. 23.

    Mori E, Zozzoli R, Menchetti M (2018) Global distribution and status of introduced Siberian chipmunks Eutamias sibiricus. Mammal Rev 48:139–152

    Article  Google Scholar 

  24. 24.

    Yi X, Yang Y, Zhang M (2019) Cache placement near nests by a multiple-prey loader, the Siberian chipmunk. Anim Behav 15:1–8

    CAS  Article  Google Scholar 

  25. 25.

    Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T (2006) Circannual control of hibernation by HP complex in the brain. Cell 125:161–172

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    Yi X, Guo J, Wang M, Xue C, Ju M (2021) Inter-trophic interaction of gut microbiota in a tripartite system. Microb Ecol 81:1075–1087

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  28. 28.

    Grond K, Bell KC, Demboski JR, Santos M, Hird SM (2019) No evidence for phylosymbiosis in western chipmunk species. FEMS Microbiol Ecol 96:fiz182

    Article  CAS  Google Scholar 

  29. 29.

    Lu HP, Wang YB, Huang SW, Lin CY, Wu M, Hsieh CH, Yu HT (2012) Metagenomic analysis reveals a functional signature for biomass degradation by cecal microbiota in the leaf-eating flying squirrel (Petaurista alborufus lena). BMC Genom 13:466

    CAS  Article  Google Scholar 

  30. 30.

    Stevenson TJ, Duddleston KN, Buck CL (2014) Diversity, density and activity of the arctic ground squirrel cecal microbiota: effects of season and host physiological state. Appl Environ Microbiol 80:5611–5622

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. 31.

    Debebe T, Biagi E, Soverini M et al (2017) Unraveling the gut microbiome of the long-lived naked mole-rat. Sci Rep 7:1–9

    Article  Google Scholar 

  32. 32.

    Xiang Z, Zhu H, Yang B, Fan H, Guo J, Liu J, Kong Q, Teng Q, Shang H, Su L, Qin C (2020) A glance at the gut microbiota of five experimental animal species through fecal samples. Sci Rep 10:16628

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Yang X, Yao Y, Zhang X, Zhong J, Yuan Z (2020) Seasonal breeding leads to changes for gut microbiota diversity in the wild ground squirrel (Spermophilus dauricus). https://doi.org/10.21203/rs.3.rs-96089/v1

  34. 34.

    Barnes EM, Burton GC (1970) The effect of hibernation on the caecal flora of the thirteen-lined ground squirrel (Citellus tridecemlineatus). J Appl Bacteriol 33:505–514

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. 35.

    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Kohl KD, Varner J, Wilkening JL, Dearing MD (2018) Gut microbial communities of American pikas (Ochotona princeps): evidence for phylosymbiosis and adaptations to novel diets. J Anim Ecol 87:323–330

    PubMed  Article  PubMed Central  Google Scholar 

  37. 37.

    Anufriev AI, Solomonov NG, Yadrikhinsky VF, Solomonova TN, Arkhipov GG (2009) Changes in the body temperature of hibernating animals of the Sciuridae family in the year life cycle. Doklady Biol Sci 427:370–373

    CAS  Article  Google Scholar 

  38. 38.

    Dill-Mcfarland KA, Neil KL, Zeng A, Sprenger RJ, Kurtz CC, Suen G, Carey HV (2015) Hibernation alters the diversity and composition of mucosa-associated bacteria while enhancing antimicrobial defence in the gut of 13-lined ground squirrels. Mol Ecol 23:4658–4669

    Article  CAS  Google Scholar 

  39. 39.

    Xiao G, Liu S, Xiao Y, Zhu Y, Feng J (2019) Seasonal changes in gut microbiota diversity and composition in the greater horseshoe bat. Front Microbiol 10:2247

    PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955–1959

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. 41.

    Sommer K, Zeng A, Dill-Mcfarland KA, Suen G, Carey HV (2013) Hibernation alters mucosa-associated bacterial communities and mucin expression in 13-lined ground squirrels. The FASEB J 27(937):26

    Google Scholar 

  42. 42.

    Conlon MA, Topping DL (2016) Dietary polysaccharides and polyphenols can promote health by influencing gut microbiota populations. Food Funct 7:1730–1730

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. 43.

    De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:14691–14696

    PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Theriot CM, Bowman BAA, Youngb BVB (2016) Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for clostridium difficile spore germination and outgrowth in the large intestine. mSphere 1:e00045-15

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  45. 45.

    Umbrello G, Esposito S (2016) Microbiota and neurologic diseases: potential effects of probiotics. J Transl Med 14:298

    PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  47. 47.

    Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420–2428

    CAS  Article  Google Scholar 

  48. 48.

    Rajilić-Stojanović M, Shanahan F, Guarner F, de Vos WM (2013) Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis 19:481–488

    PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Giroud S, Frare C, Strijkstra A, Boerema A, Arnold W, Ruf T (2013) Membrane phospholipid fatty acid composition regulates cardiac SERCA activity in a hibernator, the Syrian hamster (Mesocricetus auratus). PLoS ONE 8:e63111

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

Funding for this study was supported by the National Natural Science Foundation of China (Grant Nos. 32070447, 41807053 and 31760156) and Youth Talent Introduction and Education Program of Shandong Province (Grant No. 20190601).

Author information

Affiliations

Authors

Contributions

XY designed the study; JZ and MW collected the data; JZ did the analyses; XY and JZ wrote the first draft of the manuscript; and all authors contributed intellectually to the manuscript.

Corresponding author

Correspondence to Xianfeng Yi.

Ethics declarations

Conflict of interest

We declare we have no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 113 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhou, J., Wang, M. & Yi, X. Alteration of Gut Microbiota of a Food-Storing Hibernator, Siberian Chipmunk Tamias sibiricus. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01877-7

Download citation

Keywords

  • Siberian chipmunk
  • Food-storing hibernator
  • Gut microbiota