Advertisement

Diet simplification selects for high gut microbial diversity and strong fermenting ability in high-altitude pikas

Environmental biotechnology

Abstract

The gut microbiota in mammals plays a key role in host metabolism and adaptation. However, relatively little is known regarding to how the animals adapts to extreme environments through regulating gut microbial diversity and function. Here, we investigated the diet, gut microbiota, short-chain fatty acid (SCFA) profiles, and cellulolytic activity from two common pika (Ochotona spp.) species in China, including Plateau pika (Ochotona curzoniae) from the Qinghai-Tibet Plateau and Daurian pika (Ochotona daurica) from the Inner Mongolia Grassland. Despite a partial diet overlap, Plateau pikas harbored lower diet diversity than Daurian pikas. Some bacteria (e.g., Prevotella and Ruminococcus) associated with fiber degradation were enriched in Plateau pikas. They harbored higher gut microbial diversity, total SCFA concentration, and cellulolytic activity than Daurian pikas. Interestingly, cellulolytic activity was positively correlated with the gut microbial diversity and SCFAs. Gut microbial communities and SCFA profiles were segregated structurally between host species. PICRUSt metagenome predictions demonstrated that microbial genes involved in carbohydrate metabolism and energy metabolism were overrepresented in the gut microbiota of Plateau pikas. Our results demonstrate that Plateau pikas harbor a stronger fermenting ability for the plant-based diet than Daurian pikas via gut microbial fermentation. The enhanced ability for utilization of plant-based diets in Plateau pikas may be partly a kind of microbiota adaptation for more energy requirements in cold and hypoxic high-altitude environments.

Keywords

Pika Diet Gut microbiota SCFA profiles Cellulolytic activity Fermenting ability 

Notes

Acknowledgements

We thank Jon G. Sanders for advice on the manuscript revision. We thank Xiaoyuan Zhang (Chengdu Institute of Biology, CAS) and Haibo Fu (Northwest Institute of Plateau Biology, CAS) for their help in sample collection.

Author’s contributions

H.L. designed experiments; H.L., J.Q., T.L., and X.Z. contributed to experimental work; H.L. performed the data analysis and wrote the manuscript. H.L., W.S., Y.Z., and X. L. revised the manuscript.

Funding information

The authors thank the support by National Natural Science Foundation of China (, 41371268 and 41301272).

Compliance with ethical standards

Animal ethics approval for the present project was obtained from the Animal Ethics Committee of Chengdu Institute of Biology. Processing of wild animals and sample collection were strictly congruent with the guidelines of our academic institution.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2018_9097_MOESM1_ESM.pdf (728 kb)
ESM 1 (PDF 727 kb)

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amato KR (2013) Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci Med 1:10–29CrossRefGoogle Scholar
  3. Bäuerl C, Collado MC, Zúñiga M, Blas E, Pérez Martínez G (2014) Changes in cecal microbiota and mucosal gene expression revealed new aspects of epizootic rabbit enteropathy. PLoS One 9(8):e105707CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baxter NT, Wan JJ, Schubert AM, Jenior ML, Myers P, Schloss PD (2015) Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric peromyscus populations. Appl Environ Microbiol 81(1):396–404CrossRefPubMedGoogle Scholar
  5. Bengtsson-Palme J, Hartmann M, Eriksson KM, Pal C, Thorell K, Larsson DG, Nilsson RH (2015) Metaxa2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol Ecol Resour 15:1403–1414CrossRefPubMedGoogle Scholar
  6. Bevans D, Beauchemin K, Schwartzkopf-Genswein K, McKinnon J, McAllister T (2005) Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle. J Anim Sci 83:1116–1132CrossRefPubMedGoogle Scholar
  7. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG, Svanback R (2014) Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17(8):979–987CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bray J, Curtis J (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  9. Brinkworth GD, Noakes M, Clifton PM, Bird AR (2009) Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. Br J Nutr 101(10):1493–1502CrossRefPubMedGoogle Scholar
  10. Bromberg JS, Fricke WF, Brinkman CC, Simon T, Mongodin EF (2015) Microbiota-implications for immunity and transplantation. Nat Rev Nephrol 11:342–353CrossRefPubMedGoogle Scholar
  11. Clarke SF, Murphy EF, O’Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery IB, Wood-Martin R, Kerins DM, Quigley E, Ross RP, O’Toole PW, Molloy MG, Falvey E, Shanahan F, Cotter PD (2014) Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63(12):1913–1920CrossRefPubMedGoogle Scholar
  12. Clemens E (1977) Sites of organic acid production and patterns of digesta movement in the gastrointestinal tract of the rock hyrax. J Nutr 107:1954–1961CrossRefPubMedGoogle Scholar
  13. Dai X, Tian Y, Li J, Su X, Wang X, Zhao S, Liu L, Luo Y, Liu D, Zheng H, Wang J, Dong Z, Hu S, Huang L (2014) Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in cow rumen. Appl Environ Microbiol 81:1375–1386CrossRefGoogle Scholar
  14. Dill-McFarland KA, Weimer PJ, Pauli JN, Peery MZ, Suen G (2015) Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environ Microbiol 18:1391–1402CrossRefPubMedGoogle Scholar
  15. Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13(5):517–526CrossRefPubMedPubMedCentralGoogle Scholar
  16. Du J, Li Q (1982) Effects of simulated hypoxic acclimation on organism, organ and hematology in Ochotona curzoniae and rats. Acta Theriol Sin 2(1):35–42Google Scholar
  17. Du J, Li Q, Chen X (1984) Effect of simulated altitude on liver of Ochotona curzoniae and rats. Acta Zool Fenn 171:201–203Google Scholar
  18. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  19. Escobar JS, Klotz B, Valdes BE, Agudelo GM (2014) The gut microbiota of Colombians differs from that of Americans, Europeans and Asians. BMC Microbiol 14:311CrossRefPubMedPubMedCentralGoogle Scholar
  20. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 110:9066–9071CrossRefPubMedPubMedCentralGoogle Scholar
  21. Falcão-e-Cunha L, Peres HB, Freire JP, Castro-Solla L (2004) Effects of alfalfa, wheat bran or beet pulp, with or without sunflower oil, on caecal fermentation and on digestibility in the rabbit. Anim Feed Sci Technol 117(1–2):131–149CrossRefGoogle Scholar
  22. Fan N, Jing Z, Zhang D (1995) Studies on the food resource niches of plateau pika and Daurian pika. Acta Theriol Sin 15:36–40Google Scholar
  23. Flint HJ, Duncan SH, Scott KP, Louis P (2015) Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 74(1):13–22CrossRefPubMedGoogle Scholar
  24. Ge RL, Kubo K, Kobayashi T, Sekiguchi M, Honda T (1998) Blunted hypoxic pulmonary vasoconstrictive response in the rodent Ochotona curzoniae (pika) at high altitude. Am J Phys 274(5):H1792–H1799Google Scholar
  25. Ge D, Wen Z, Xia L, Zhang Z, Erbajeva M, Huang C, Yang Q (2013) Evolutionary history of lagomorphs in response to global environmental change. PLoS One 8(4):e59668CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hume I (1997) Fermentation in the hindgut of mammals. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New York, pp 84–115CrossRefGoogle Scholar
  27. Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37–50CrossRefGoogle Scholar
  28. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124(4):837–848CrossRefPubMedGoogle Scholar
  30. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R (2008a) Evolution of mammals and their gut microbes. Science 320(5883):1647–1651CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008b) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6(10):776–788CrossRefPubMedPubMedCentralGoogle Scholar
  32. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659CrossRefPubMedGoogle Scholar
  33. Li Q, Sun R, Huang C, Wang Z, Liu X, Hou J, Liu J, Cai L, Li N, Zhang S (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A Mol Integr Physiol 129(4):949–961CrossRefPubMedGoogle Scholar
  34. Li H, Li T, Beasley DE, Hedenec P, Xiao Z, Zhang S, Li J, Lin Q, Li X (2016a) Diet diversity is associated with beta but not alpha diversity of pika gut microbiota. Front Microbiol 7:1169PubMedPubMedCentralGoogle Scholar
  35. Li H, Li T, Yao M, Li J, Zhang S, Wirth S, Cao W, Lin Q, Li X (2016b) Pika gut may select for rare but diverse environmental bacteria. Front Microbiol 7:1269PubMedPubMedCentralGoogle Scholar
  36. Li H, Qu J, Li T, Li J, Lin Q, Li X (2016c) Pika population density is associated with composition and diversity of gut microbiota. Front Microbiol 7:758PubMedPubMedCentralGoogle Scholar
  37. Li H, Li T, Berasategui A, Rui J, Zhang X, Li C, Xiao Z, Li X (2017a) Gut region influences the diversity and interactions of bacterial communities in pikas (Ochotona curzoniae and Ochotona daurica). FEMS Microbiol Ecol 93:fix149Google Scholar
  38. Li H, Li T, Tu B, Kou Y, Li X (2017b) Host species shapes the co-occurrence patterns rather than diversity of stomach bacterial communities in pikas. Appl Microbiol Biotechnol 101(13):5519–5529CrossRefPubMedGoogle Scholar
  39. Li H, Qu J, Li T, Yao M, Li J, Li X (2017c) Gut microbiota may predict host divergence time during Glires evolution. FEMS Microbiol Ecol 93(3):fix009CrossRefGoogle Scholar
  40. Linnenbrink M, Wang J, Hardouin EA, Künzel S, Metzler D, Baines JF (2013) The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol 22(7):1904–1916CrossRefPubMedGoogle Scholar
  41. Liu W, Zhang Y, Wang X, Zhao J, Xu Q, Zhou L (2008) Food selection by plateau pikas in different habitats during plant growing. Acta Theriol Sin 28:358–366Google Scholar
  42. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230CrossRefPubMedPubMedCentralGoogle Scholar
  43. Luo Y, Gao W, Gao Y, Tang S, Huang Q, Tan X, Chen J, Huang T (2008) Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation. Mitochondrion 8(5):352–357CrossRefPubMedGoogle Scholar
  44. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, Shah N, Wang C, Magrini V, Wilson RK, Cantarel BL, Coutinho PM, Henrissat B, Crock LW, Russell A, Verberkmoes NC, Hettich RL, Gordon JI (2009) Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci U S A 106(14):5859–5864CrossRefPubMedPubMedCentralGoogle Scholar
  45. McDonald R, Zhang F, Watts JE, Schreier HJ (2015) Nitrogenase diversity and activity in the gastrointestinal tract of the wood-eating catfish Panaque nigrolineatus. ISME J 9(12):2712–2724CrossRefPubMedPubMedCentralGoogle Scholar
  46. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428CrossRefGoogle Scholar
  47. Nelson TM, Rogers TL, Carlini AR, Brown MV (2013) Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ Microbiol 15(4):1132–1145CrossRefPubMedGoogle Scholar
  48. Niu Y, Wei F, Li M, Liu X, Feng Z (2004) Phylogeny of pikas (Lagomorpha, Ochotona) inferred from mitochondrial cytochrome b sequences. Folia Zool 53:141–155Google Scholar
  49. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pei S, Fu H, Wan C (2008) Changes in soil properties and vegetation following exclosure and grazing in degraded Alxa desert steppe of Inner Mongolia, China. Agr Ecosyst Environ 124(1–2):33–39CrossRefGoogle Scholar
  51. Poppi D, Minson D, Ternouth J (1981) Studies of cattle and sheep eating leaf and stem fractions of grasses. 3. The retention time in the rumen of large feed particles. Aust J Agric Res 32:123–137CrossRefGoogle Scholar
  52. Rey FE, Faith JJ, Bain J, Muehlbauer MJ, Stevens RD, Newgard CB, Gordon JI (2010) Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 285(29):22082–22090CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sanders JG, Powell S, Kronauer DJ, Vasconcelos HL, Frederickson ME, Pierce NE (2014) Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 23(6):1268–1283CrossRefPubMedGoogle Scholar
  54. Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35(1, Suppl):S35–S38CrossRefPubMedPubMedCentralGoogle Scholar
  55. Shin JH, Sim M, Lee JY, Shin DM (2016) Lifestyle and geographic insights into the distinct gut microbiota in elderly women from two different geographic locations. J Physiol Anthropol 35(1):31CrossRefPubMedPubMedCentralGoogle Scholar
  56. Stevens C, Hume I (2004) Comparative physiology of the vertebrate digestive system. Cambridge University Press, CambridgeGoogle Scholar
  57. Sun YZ, Mao SY, Zhu WY (2010) Rumen chemical and bacterial changes during stepwise adaptation to a high-concentrate diet in goats. Animal 4(2):210–217CrossRefPubMedGoogle Scholar
  58. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  59. Toju H, Tanabe A, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of Ascomycetes and Basidiomycetes in environmental samples. PLoS One 7:e40863CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242–249CrossRefPubMedGoogle Scholar
  61. Turnbaugh PJ, Gordon JI (2009) The core gut microbiome, energy balance and obesity. J Physiol 587(Pt 17):4153–4158CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wang D, Wang Z (2001) Seasonal variations in digestive tract morphology in plateau pikas (Ochotona curzoniae) on the Qinghai-Tibetan Plateau. Acta Zool Sin 47:495–501Google Scholar
  63. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  64. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3(1):89–101CrossRefGoogle Scholar
  65. Werner JJ, Knights D, Garcia ML, Scalfonea NB, Smith S, Yarasheski K, Cummings TA, Beers AR, Knight R, Angenent LT (2011) Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc Natl Acad Sci U S A 108(10):4158–4163CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wolever TM, Brighenti F, Royall D, Jenkins AL, Jenkins DJ (1989) Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterol 84:1027–1033PubMedGoogle Scholar
  67. Wolever TM, Spadafora P, Eshuis H (1991) Interaction between colonic acetate and propionate in humans. Am J Gastroenterol 84:1027–1033Google Scholar
  68. Yang Z, Bielawski J (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503CrossRefPubMedGoogle Scholar
  69. Yang Y, Yue C, Guoen J, Zhenzhong B, Lan M, Haixia Y, Rili G (2007) Molecular cloning and characterization of hemoglobin α and β chains from plateau pika (Ochotona curzoniae) living at high altitude. Gene 403(1):118–124Google Scholar
  70. Yang J, Wang ZL, Zhao XQ, Xu BH, Ren YH, Tian HF (2008) Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress. PLoS One 3(1):e1472CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yu N, Zheng C, Shi L (1998) The correlation between the environmental changes and the evolution of the two sibling species of pika (genus Ochotona). Acta Theriol Sin 18:127–130Google Scholar
  72. Zhang H, Sparks JB, Karyala SV, Settlage R, Luo XM (2015) Host adaptive immunity alters gut microbiota. ISME J 9(3):770–781CrossRefPubMedGoogle Scholar
  73. Zhu L, Wu Q, Dai J, Zhang S, Wei F (2011) Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci U S A 108:17714–17719CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Occupational Health and Environmental Health, School of Public HealthLanzhou UniversityLanzhouChina
  2. 2.Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau BiologyChinese Academy of SciencesXiningPeople’s Republic of China
  3. 3.Department of Applied Biology, College of Biotechnology and BioengineeringZhejiang University of TechnologyHangzhouPeople’s Republic of China
  4. 4.Leibniz-Centre for Agricultural Landscape Research (ZALF)Institute of Landscape BiogeochemistryMunchebergGermany
  5. 5.Key Laboratory of Environmental and Applied Microbiology, CAS; Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of BiologyChinese Academy of SciencesChengduPeople’s Republic of China

Personalised recommendations