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

  • Environmental biotechnology
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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.

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References

  • 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 25:3389–3402

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amato KR (2013) Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci Med 1:10–29

    Article  Google Scholar 

  • 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):e105707

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):396–404

    Article  PubMed  CAS  Google Scholar 

  • 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 15:1403–1414

    Article  PubMed  CAS  Google Scholar 

  • 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 83:1116–1132

    Article  PubMed  CAS  Google Scholar 

  • 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):979–987

    Article  PubMed  PubMed Central  Google Scholar 

  • Bray J, Curtis J (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • 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):1493–1502

    Article  PubMed  CAS  Google Scholar 

  • Bromberg JS, Fricke WF, Brinkman CC, Simon T, Mongodin EF (2015) Microbiota-implications for immunity and transplantation. Nat Rev Nephrol 11:342–353

    Article  PubMed  CAS  Google Scholar 

  • 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):1913–1920

    Article  PubMed  CAS  Google Scholar 

  • Clemens E (1977) Sites of organic acid production and patterns of digesta movement in the gastrointestinal tract of the rock hyrax. J Nutr 107:1954–1961

    Article  PubMed  CAS  Google Scholar 

  • 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 81:1375–1386

    Article  CAS  Google Scholar 

  • 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 18:1391–1402

    Article  PubMed  CAS  Google Scholar 

  • 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):517–526

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):35–42

    Google Scholar 

  • Du J, Li Q, Chen X (1984) Effect of simulated altitude on liver of Ochotona curzoniae and rats. Acta Zool Fenn 171:201–203

    Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Escobar JS, Klotz B, Valdes BE, Agudelo GM (2014) The gut microbiota of Colombians differs from that of Americans, Europeans and Asians. BMC Microbiol 14:311

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 110:9066–9071

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):131–149

    Article  CAS  Google Scholar 

  • Fan N, Jing Z, Zhang D (1995) Studies on the food resource niches of plateau pika and Daurian pika. Acta Theriol Sin 15:36–40

    Google Scholar 

  • Flint HJ, Duncan SH, Scott KP, Louis P (2015) Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 74(1):13–22

    Article  PubMed  CAS  Google Scholar 

  • 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–H1799

    CAS  Google Scholar 

  • 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):e59668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hume I (1997) Fermentation in the hindgut of mammals. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New York, pp 84–115

    Chapter  Google Scholar 

  • Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37–50

    Article  Google Scholar 

  • 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):814–821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124(4):837–848

    Article  PubMed  CAS  Google Scholar 

  • 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):1647–1651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):776–788

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659

    Article  PubMed  CAS  Google Scholar 

  • 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):949–961

    Article  PubMed  CAS  Google Scholar 

  • 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 7:1169

    PubMed  PubMed Central  Google Scholar 

  • 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 7:1269

    PubMed  PubMed Central  Google Scholar 

  • 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 7:758

    PubMed  PubMed Central  Google Scholar 

  • 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:fix149

    Google Scholar 

  • 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):5519–5529

    Article  PubMed  CAS  Google Scholar 

  • 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):fix009

    Article  CAS  Google Scholar 

  • 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):1904–1916

    Article  PubMed  Google Scholar 

  • 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 28:358–366

    Google Scholar 

  • Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):352–357

    Article  PubMed  CAS  Google Scholar 

  • 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):5859–5864

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):2712–2724

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • 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):1132–1145

    Article  PubMed  CAS  Google Scholar 

  • Niu Y, Wei F, Li M, Liu X, Feng Z (2004) Phylogeny of pikas (Lagomorpha, Ochotona) inferred from mitochondrial cytochrome b sequences. Folia Zool 53:141–155

    Google Scholar 

  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):33–39

    Article  Google Scholar 

  • 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 32:123–137

    Article  Google Scholar 

  • 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):22082–22090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1268–1283

    Article  PubMed  Google Scholar 

  • Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35(1, Suppl):S35–S38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):31

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevens C, Hume I (2004) Comparative physiology of the vertebrate digestive system. Cambridge University Press, Cambridge

    Google Scholar 

  • 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):210–217

    Article  PubMed  CAS  Google Scholar 

  • 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 22:4673–4680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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:e40863

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242–249

    Article  PubMed  CAS  Google Scholar 

  • Turnbaugh PJ, Gordon JI (2009) The core gut microbiome, energy balance and obesity. J Physiol 587(Pt 17):4153–4158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang D, Wang Z (2001) Seasonal variations in digestive tract morphology in plateau pikas (Ochotona curzoniae) on the Qinghai-Tibetan Plateau. Acta Zool Sin 47:495–501

    Google Scholar 

  • 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):5261–5267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3(1):89–101

    Article  Google Scholar 

  • 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):4158–4163

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 84:1027–1033

    PubMed  CAS  Google Scholar 

  • Wolever TM, Spadafora P, Eshuis H (1991) Interaction between colonic acetate and propionate in humans. Am J Gastroenterol 84:1027–1033

    Google Scholar 

  • Yang Z, Bielawski J (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503

    Article  PubMed  CAS  Google Scholar 

  • 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):118–124

    Article  CAS  Google Scholar 

  • 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):e1472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 18:127–130

    Google Scholar 

  • Zhang H, Sparks JB, Karyala SV, Settlage R, Luo XM (2015) Host adaptive immunity alters gut microbiota. ISME J 9(3):770–781

    Article  PubMed  CAS  Google Scholar 

  • 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 108:17714–17719

    Article  PubMed  PubMed Central  Google Scholar 

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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.

Funding

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

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Author notes

  1. Huan Li and Jiapeng Qu contributed equally to this work.

Authors and Affiliations

  1. Institute of Occupational Health and Environmental Health, School of Public Health, Lanzhou University, Lanzhou, 730000, China

    Huan Li

  2. Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810008, Qinghai, People’s Republic of China

    Jiapeng Qu & Yanming Zhang

  3. Department of Applied Biology, College of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou, 310014, People’s Republic of China

    Tongtong Li

  4. Leibniz-Centre for Agricultural Landscape Research (ZALF), Institute of Landscape Biogeochemistry, Eberswalder Str. 84, 15374, Muncheberg, Germany

    Stephan Wirth

  5. Key Laboratory of Environmental and Applied Microbiology, CAS; Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, Sichuan, People’s Republic of China

    Xinquan Zhao & Xiangzhen Li

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  1. Huan Li
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  2. Jiapeng Qu
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  5. Yanming Zhang
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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.

Corresponding authors

Correspondence to Yanming Zhang or Xiangzhen Li.

Ethics declarations

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.

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Li, H., Qu, J., Li, T. et al. Diet simplification selects for high gut microbial diversity and strong fermenting ability in high-altitude pikas. Appl Microbiol Biotechnol 102, 6739–6751 (2018). https://doi.org/10.1007/s00253-018-9097-z

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