1932

Abstract

Animals that undergo seasonal cycles of feeding and fasting have adaptations that maintain integrity of organ systems when dietary nutrients are lacking. Food deprivation also challenges the gut microbiota, which relies heavily on host diet for metabolic substrates and the gastrointestinal tract, which is influenced by enteral nutrients and microbial activity. Winter fasting in hibernators shifts the microbiota to favor taxa with the capacity to degrade and utilize host-derived substrates and disfavor taxa that prefer complex plant polysaccharides. Microbiome alterations may contribute to hibernation-induced changes in the intestinal immune system, epithelial barrier function, and other host features that are affected by microbial short-chain fatty acids and other metabolites. Understanding mechanisms by which the hibernator host and its gut symbionts adapt to the altered nutritional landscape during winter fasting may provide insights into protective mechanisms that are compromised when nonhibernating species, such as humans, undergo long periods of enteral nutrient deprivation.

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2017-08-21
2024-04-13
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Literature Cited

  1. Adelstein SJ, Lyman CP, O'Brien RC, Fisher KC, Dawe AR. 1.  et al. 1967. Cell proliferation kinetics in the tongue and intestinal epithelia of hibernating dormice (Glis glis). Mammalian Hibernation III KC Fisher, AR Dawe, CP Lyman, E Schonbaum, FE South 398–408 Edinburgh: Oliver & Boyd [Google Scholar]
  2. Andrews MT, Russeth KP, Drewes LR, Henry PG. 2.  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:R383–93 [Google Scholar]
  3. Asselin C, Gendron FP. 3.  2014. Shuttling of information between the mucosal and luminal environment drives intestinal homeostasis. FEBS Lett 588:4148–57 [Google Scholar]
  4. Barnes EM, Burton GC. 4.  1970. The effect of hibernation on the caecal flora of the thirteen-lined ground squirrel (Citellus tridecemlineatus). J. Appl. Bacteriol. 33:505–14 [Google Scholar]
  5. Beatty DW, Napier B, Sinclair-Smith CC, McCabe K, Hughes EJ. 5.  1983. Secretory IgA synthesis in Kwashiorkor. J. Clin. Lab. Immunol. 12:31–36 [Google Scholar]
  6. Benson AK, Kelly SA, Legge R, Ma F, Low SJ. 6.  et al. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS 107:18933–38 [Google Scholar]
  7. Burant CF, Flink S, DePaoli AM, Chen J, Lee WS. 7.  et al. 1994. Small intestine hexose transport in experimental diabetes. Increased transporter mRNA and protein expression in enterocytes. J. Clin. Investig. 93:578–85 [Google Scholar]
  8. Carey HV. 8.  1990. Seasonal changes in mucosal structure and function in ground squirrel intestine. Am. J. Physiol. Regul. Integr. Comp. Physiol. 259:R385–92 [Google Scholar]
  9. Carey HV. 9.  1992. Effects of fasting and hibernation on ion secretion in ground squirrel intestine. Am. J. Physiol. Regul. Integr. Comp. Physiol. 263:R1203–8 [Google Scholar]
  10. Carey HV, Andrews MT, Martin SL. 10.  2003. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83:1153–81 [Google Scholar]
  11. Carey HV, Duddleston KN. 11.  2014. Animal-microbial symbioses in changing environments. J. Therm. Biol. 44:78–84 [Google Scholar]
  12. Carey HV, Martin SL. 12.  1996. Preservation of intestinal gene expression during hibernation. Am. J. Physiol. 271:G804–13 [Google Scholar]
  13. Carey HV, Martin SL, Horwitz BA, Yan L, Bailey SM. 13.  et al. 2012. Elucidating nature's solutions to heart, lung, and blood diseases and sleep disorders. Circ. Res. 110:915–21 [Google Scholar]
  14. Carey HV, Pike AC, Weber CR, Turner JL, Visser A. 14.  et al. 2012. Impact of hibernation on gut microbiota and intestinal barrier function in ground squirrels. Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations T Ruf, C Bieber, W Arnold, E Millesi 281–91 Heidelberg: Springer [Google Scholar]
  15. Carey HV, Walters WA, Knight R. 15.  2013. Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304:R33–42 [Google Scholar]
  16. Chassaing B, Miles-Brown JP, Pellizzon M, Ulman E, Ricci M. 16.  et al. 2015. Lack of soluble fiber drives diet-induced adiposity in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 309:7G528–41 [Google Scholar]
  17. Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V. 17.  et al. 2015. Gut microbiota orchestrates energy homeostasis during cold. Cell 163:1360–74 [Google Scholar]
  18. Cloud-Hansen KA, Villiard KM, Handelsman J, Carey HV. 18.  2007. Thirteen-lined ground squirrels (Spermophilus tridecemlineatus) harbor multiantibiotic-resistant bacteria. J. Am. Assoc. Lab. Anim. Sci. 46:21–23 [Google Scholar]
  19. Dark J. 19.  2005. Annual lipid cycles in hibernators: integration of physiology and behavior. Ann. Rev. Nutr. 25:469–97 [Google Scholar]
  20. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE. 20.  et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–63 [Google Scholar]
  21. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB. 21.  et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. PNAS 107:14691–96 [Google Scholar]
  22. Demehri FR, Barrett M, Ralls MW, Miyasaka EA, Feng Y, Teitelbaum DH. 22.  2013. Intestinal epithelial cell apoptosis and loss of barrier function in the setting of altered microbiota with enteral nutrient deprivation. Front. Cell. Infect. Microbiol. 3:105 [Google Scholar]
  23. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos WM. 23.  2011. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. . Front. Microbiol. 2:166 [Google Scholar]
  24. Derrien M, Vaughan EE, Plugge CM, de Vos WM. 24.  2004. Akkermansiamuciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54:1469–76 [Google Scholar]
  25. Dill-McFarland KA, Neil KL, Zeng A, Sprenger RJ, Kurtz CC. 25.  et al. 2014. Hibernation alters the diversity and composition of mucosa-associated bacteria while enhancing antimicrobial defence in the gut of 13-lined ground squirrels. Mol. Ecol. 23:4658–69 [Google Scholar]
  26. Dill-McFarland KA, Suen G, Carey HV. 26.  2016. Bears arouse interest in microbiota's role in health. Trends Microbiol 24:245–46 [Google Scholar]
  27. Donaldson GP, Lee SM, Mazmanian SK. 27.  2016. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14:20–32 [Google Scholar]
  28. Dorrestein PC, Mazmanian SK, Knight R. 28.  2014. Finding the missing links among metabolites, microbes, and the host. Immunity 40:824–32 [Google Scholar]
  29. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. 29.  2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73:1073–78 [Google Scholar]
  30. Epperson LE, Karimpour-Fard A, Hunter LE, Martin SL. 30.  2011. Metabolic cycles in a circannual hibernator. Physiol. Genom. 43:799–807 [Google Scholar]
  31. Epperson LE, Rose JC, Carey HV, Martin SL. 31.  2010. Seasonal proteomic changes reveal molecular adaptations to preserve and replenish liver proteins during ground squirrel hibernation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298:R329–40 [Google Scholar]
  32. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C. 32.  et al. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. PNAS 110:9066–71 [Google Scholar]
  33. Feng YJ, Sun XY, Yang H, Teitelbaum DH. 33.  2009. Dissociation of E-cadherin and beta-catenin in a mouse model of total parenteral nutrition: a mechanism for the loss of epithelial cell proliferation and villus atrophy. J. Physiol. 587:641–54 [Google Scholar]
  34. Fleck CC, Carey HV. 34.  2005. Modulation of apoptotic pathways in intestinal mucosa during hibernation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289:R586–95 [Google Scholar]
  35. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. 35.  2012. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3:289–306 [Google Scholar]
  36. Freeman JJ, Feng Y, Demehri FR, Dempsey PJ, Teitelbaum DH. 36.  2015. TPN-associated intestinal epithelial cell atrophy is modulated by TLR4/EGF signaling pathways. FASEB J 29:2943–58 [Google Scholar]
  37. Fuller A, Mitchell D. 37.  1999. Oral antibiotics reduce body temperature of healthy rabbits in a thermoneutral environment. J. Basic Clin. Physiol. Pharmacol. 10:1–13 [Google Scholar]
  38. Galster W, Morrison PR. 38.  1975. Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am. J. Physiol. 228:325–30 [Google Scholar]
  39. Grabek KR, Martin SL, Hindle AG. 39.  2015. Proteomics approaches shed new light on hibernation physiology. J. Comp. Physiol. B 185:6607–27 [Google Scholar]
  40. Hanning I, Diaz-Sanchez S. 40.  2015. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome 3:51 [Google Scholar]
  41. Harlow H. 41.  2012. Muscle protein and strength retention by bears during winter fasting and starvation. Comparative Physiology of Fasting, Starvation and Food Limitation MD McCue 277–96 Heidelberg: Springer-Verlag [Google Scholar]
  42. Hatton JJ, Stevenson TJ, Buck CL, Duddleston KN. 42.  2017. Diet affects arctic ground squirrel gut microbial metatranscriptome independent of community structure. Environ. Microbiol. 19:1518–35 [Google Scholar]
  43. Haviland JA, Tonelli M, Haughey DT, Porter WP, Assadi-Porter FM. 43.  2012. Novel diagnostics of metabolic dysfunction detected in breath and plasma by selective isotope-assisted labeling. Metabolism 61:1162–70 [Google Scholar]
  44. Heneghan AF, Pierre JF, Kudsk KA. 44.  2013. IL-25 improves IgA levels during parenteral nutrition through the JAK-STAT pathway. Ann. Surg. 258:1065–71 [Google Scholar]
  45. Hodin CM, Visschers RG, Rensen SS, Boonen B, Olde Damink SW. 45.  et al. 2012. Total parenteral nutrition induces a shift in the Firmicutes to Bacteroidetes ratio in association with Paneth cell activation in rats. J. Nutr. 142:2141–47 [Google Scholar]
  46. Hooper LV, Midtvedt T, Gordon JI. 46.  2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22:283–307 [Google Scholar]
  47. Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI. 47.  1999. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. PNAS 96:9833–38 [Google Scholar]
  48. Hume ID, Beiglbock C, Ruf T, Frey-Roos F, Bruns U, Arnold W. 48.  2002. Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J. Comp. Physiol. B 172:197–207 [Google Scholar]
  49. Huse SM, Ye Y, Zhou Y, Fodor AA. 49.  2012. A core human microbiome as viewed through 16S rRNA sequence clusters. PLOS ONE 7:e34242 [Google Scholar]
  50. Kansagra K, Stoll B, Rognerud C, Niinikoski H, Ou CN. 50.  et al. 2003. Total parenteral nutrition adversely affects gut barrier function in neonatal piglets. Am. J. Physiol. Gastrointest. Liver Physiol. 285:G1162–70 [Google Scholar]
  51. Kashyap PC, Marcobal A, Ursell LK, Smits SA, Sonnenburg ED. 51.  et al. 2013. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. PNAS 110:17059–64 [Google Scholar]
  52. Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC. 52.  et al. 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17:662–71 [Google Scholar]
  53. Kiristioglu I, Antony P, Fan Y, Forbush B, Mosley RL. 53.  et al. 2002. Total parenteral nutrition-associated changes in mouse intestinal intraepithelial lymphocytes. Dig. Dis. Sci. 47:1147–57 [Google Scholar]
  54. Kluger MJ, Conn CA, Franklin B, Freter R, Abrams GD. 54.  1990. Effect of gastrointestinal flora on body temperature of rats and mice. Am. J. Physiol. Gastrointest. Liver Physiol. 258:R552–57 [Google Scholar]
  55. Kohl KD, Amaya J, Passement CA, Dearing MD, McCue MD. 55.  2014. Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts. FEMS Microbiol. Ecol. 90:883–94 [Google Scholar]
  56. Kohl KD, Carey HV. 56.  2016. A place for host–microbe symbiosis in the comparative physiologist's toolbox. J. Exp. Biol. 219:3496–504 [Google Scholar]
  57. Kudsk KA, Wu Y, Fukatsu K, Zarzaur BL, Johnson CD. 57.  et al. 2000. Glutamine-enriched total parenteral nutrition maintains intestinal interleukin-4 and mucosal immunoglobulin A levels. J. Parenter. Enter. Nutr. 24:270–74 Discussion. 2000 J. Parenter. Enter. Nutr 24:274–75 [Google Scholar]
  58. Kurtz CC, Carey HV. 58.  2007. Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev. Comp. Immunol. 31:415–28 [Google Scholar]
  59. Leser TD, Lindecrona RH, Jensen TK, Jensen BB, Moller K. 59.  2000. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl. Environ. Microbiol. 66:3290–96 [Google Scholar]
  60. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 60.  2005. Obesity alters gut microbial ecology. PNAS 102:11070–75 [Google Scholar]
  61. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR. 61.  et al. 2008. Evolution of mammals and their gut microbes. Science 320:1647–51 [Google Scholar]
  62. Louis P, Flint HJ. 62.  2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 294:1–8 [Google Scholar]
  63. Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM. 63.  et al. 2014. Differential modulation by Akkermansia muciniphila and. Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio 5:e01438–14 [Google Scholar]
  64. Marcobal A, Southwick AM, Earle KA, Sonnenburg JL. 64.  2013. A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 23:1038–46 [Google Scholar]
  65. Martens EC, Chiang HC, Gordon JI. 65.  2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–57 [Google Scholar]
  66. Martinez I, Muller CE, Walter J. 66.  2013. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLOS ONE 8:e69621 [Google Scholar]
  67. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T. 67.  et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. PNAS 110:3229–36 [Google Scholar]
  68. McLoughlin K, Schluter J, Rakoff-Nahoum S, Smith AL, Foster KR. 68.  2016. Host selection of microbiota via differential adhesion. Cell Host Microbe 19:550–59 [Google Scholar]
  69. Meehan CJ, Beiko RG. 69.  2014. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol. Evol. 6:703–13 [Google Scholar]
  70. Metges CC, Eberhard M, Petzke KJ. 70.  2006. Synthesis and absorption of intestinal microbial lysine in humans and non-ruminant animals and impact on human estimated average requirement of dietary lysine. Curr. Opin. Clin. Nutr. Metab. Care 9:37–41 [Google Scholar]
  71. Millward DJ, Forrester T, Ah-Sing E, Yeboah N, Gibson N. 71.  et al. 2000. The transfer of 15N from urea to lysine in the human infant. Br. J. Nutr. 83:505–12 [Google Scholar]
  72. Miyasaka EA, Feng Y, Poroyko V, Falkowski NR, Erb-Downward J. 72.  et al. 2013. Total parenteral nutrition-associated lamina propria inflammation in mice is mediated by a MyD88-dependent mechanism. J. Immunol. 190:6607–15 [Google Scholar]
  73. Morrison DJ, Preston T. 73.  2016. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:189–200 [Google Scholar]
  74. Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A. 74.  et al. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–74 [Google Scholar]
  75. Nelson CJ, Otis JP, Carey HV. 75.  2010. Global analysis of circulating metabolites in hibernating ground squirrels. Comp. Biochem. Physiol. Part D Genom. Proteom. 5:265–73 [Google Scholar]
  76. Nelson CJ, Otis JP, Martin SL, Carey HV. 76.  2009. Analysis of the hibernation cycle using LC-MS-based metabolomics in ground squirrel liver. Physiol. Genom. 37:43–51 [Google Scholar]
  77. Nelson RA. 77.  1989. Nitrogen conservation and its turnover in hibernation. Living in the Cold A Malan, B Canguilhem 299–307 London: Libbey Eurotext [Google Scholar]
  78. Oelkrug R, Polymeropoulos ET, Jastroch M. 78.  2015. Brown adipose tissue: physiological function and evolutionary significance. J. Comp. Physiol. B 185:587–606 [Google Scholar]
  79. Osborne JM, Dehority BA. 79.  1989. Synergism in degradation and utilization of intact forage cellulose, hemicellulose, and pectin by three pure cultures of ruminal bacteria. Appl. Environ. Microbiol. 55:2247–50 [Google Scholar]
  80. Ouwerkerk JP, de Vos WM, Belzer C. 80.  2013. Glycobiome: bacteria and mucus at the epithelial interface. Best Pract. Res. Clin. Gastroenterol. 27:25–38 [Google Scholar]
  81. Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T. 81.  et al. 2016. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature 535:376–81 [Google Scholar]
  82. Peterson CA, Ney DM, Hinton PS, Carey HV. 82.  1996. Beneficial effects of insulin-like growth factor I on epithelial structure and function in parenterally fed rat jejunum. Gastroenterology 111:1501–8 [Google Scholar]
  83. Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS. 83.  et al. 2010. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am. J. Gastroenterol. 105:2420–28 [Google Scholar]
  84. Ralls MW, Demehri FR, Feng Y, Raskind S, Ruan C. 84.  et al. 2016. Bacterial nutrient foraging in a mouse model of enteral nutrient deprivation: Insight into the gut origin of sepsis. Am. J. Physiol. Gastrointest. Liver Physiol. 311:4G734–43 [Google Scholar]
  85. Ralls MW, Miyasaka E, Teitelbaum DH. 85.  2014. Intestinal microbial diversity and perioperative complications. J. Parenter. Enter. Nutr. 38:392–99 [Google Scholar]
  86. Reunanen J, Kainulainen V, Huuskonen L, Ottman N, Belzer C. 86.  et al. 2015. Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer. Appl. Environ. Microbiol. 81:3655–62 [Google Scholar]
  87. Riedesel ML, Steffen JM. 87.  1980. Protein metabolism and urea recycling in rodent hibernators. Fed. Proc 392959–63 [Google Scholar]
  88. Rogier EW, Frantz AL, Bruno ME, Kaetzel CS. 88.  2014. Secretory IgA is concentrated in the outer layer of colonic mucus along with gut bacteria. Pathogens 3:390–403 [Google Scholar]
  89. Rooks MG, Garrett WS. 89.  2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16:341–52 [Google Scholar]
  90. Rose JC, Epperson LE, Carey HV, Martin SL. 90.  2011. Seasonal liver protein differences in a hibernator revealed by quantitative proteomics using whole animal isotopic labeling. Comp. Biochem. Physiol. Part D Genom. Proteom. 6:163–70 [Google Scholar]
  91. Rosenberg E, Zilber-Rosenberg I. 91.  2016. Do microbiotas warm their hosts. Gut Microbes 7:4283–85 [Google Scholar]
  92. Round JL, Mazmanian SK. 92.  2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:313–23 [Google Scholar]
  93. Ruf T, Geiser F. 93.  2015. Daily torpor and hibernation in birds and mammals. Biol. Rev. Camb. Philos. Soc. 90:3891–926 [Google Scholar]
  94. Schluter J, Foster KR. 94.  2012. The evolution of mutualism in gut microbiota via host epithelial selection. PLOS Biol 10:e1001424 [Google Scholar]
  95. Schwartz C, Andrews MT. 95.  2013. Circannual transitions in gene expression: lessons from seasonal adaptations. Curr. Top. Dev. Biol. 105:247–73 [Google Scholar]
  96. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA. 96.  et al. 2010. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18:190–95 [Google Scholar]
  97. Secor SM, Carey HV. 97.  2016. Integrative physiology of fasting. Compr. Physiol. 6:773–825 [Google Scholar]
  98. Serkova NJ, Rose JC, Epperson LE, Carey HV, Martin SL. 98.  2007. Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol. Genom. 31:15–24 [Google Scholar]
  99. Seth EC, Taga ME. 99.  2014. Nutrient cross-feeding in the microbial world. Front. Microbiol. 5:350 [Google Scholar]
  100. Shade A, Handelsman J. 100.  2012. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14:4–12 [Google Scholar]
  101. Shin NR, Whon TW, Bae JW. 101.  2015. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503 [Google Scholar]
  102. Singer MA. 102.  2003. Do mammals, birds, reptiles and fish have similar nitrogen conserving systems?. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 134:543–58 [Google Scholar]
  103. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA. 103.  et al. 2013. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–73 [Google Scholar]
  104. Sommer F, Ståhlman M, Ilkayeva O, Arnemo JM, Kindberg J. 104.  et al. 2016. The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep 14:1655–61 [Google Scholar]
  105. Sommer K, Zeng A, Dill-McFarland KA, Suen G, Carey HV. 105.  2013. Hibernation alters mucosa-associated bacterial communities and mucin expression in 13-lined ground squirrels. FASEB J 27:Suppl.937.26 [Google Scholar]
  106. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP. 106.  et al. 2005. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955–59 [Google Scholar]
  107. Sonoyama K, Fujiwara R, Takemura N, Ogasawara T, Watanabe J. 107.  et al. 2009. Response of gut microbiota to fasting and hibernation in Syrian hamsters. Appl. Environ. Microbiol. 75:6451–56 [Google Scholar]
  108. Souba WW, Scott TE, Wilmore DW. 108.  1985. Intestinal consumption of intravenously administered fuels. J. Parenter. Enter. Nutr. 9:18–22 [Google Scholar]
  109. Stevenson TJ, Buck CL, Duddleston KN. 109.  2014. Temporal dynamics of the cecal gut microbiota of juvenile arctic ground squirrels: a strong litter effect across the first active season. Appl. Environ. Microbiol. 80:4260–68 [Google Scholar]
  110. Stevenson TJ, Duddleston KN, Buck CL. 110.  2014. Effects of season and host physiological state on the diversity, density, and activity of the arctic ground squirrel cecal microbiota. Appl. Environ. Microbiol. 80:5611–22 [Google Scholar]
  111. Stewart GS, Smith CP. 111.  2005. Urea nitrogen salvage mechanisms and their relevance to ruminants, non-ruminants and man. Nutr. Res. Rev. 18:49–62 [Google Scholar]
  112. Sun X, Yang H, Nose K, Nose S, Haxhija EQ. 112.  et al. 2008. Decline in intestinal mucosal IL-10 expression and decreased intestinal barrier function in a mouse model of total parenteral nutrition. Am. J. Physiol. Gastrointest. Liver Physiol. 294:G139–47 [Google Scholar]
  113. Toien O, Blake J, Barnes BM. 113.  2015. Thermoregulation and energetics in hibernating black bears: metabolic rate and the mystery of multi-day body temperature cycles. J. Comp. Physiol. B 185:447–61 [Google Scholar]
  114. Tremaroli V, Backhed F. 114.  2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242–49 [Google Scholar]
  115. Turnbaugh PJ, Gordon JI. 115.  2009. The core gut microbiome, energy balance and obesity. J. Physiol. 587:4153–58 [Google Scholar]
  116. Turner JR. 116.  2009. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9:799–809 [Google Scholar]
  117. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S. 117.  2011. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol. Rev. 35:681–704 [Google Scholar]
  118. Wan X, Bi J, Gao X, Tian F, Wang X. 118.  et al. 2015. Partial enteral nutrition preserves elements of gut barrier function, including innate immunity, intestinal alkaline phosphatase (IAP) level, and intestinal microbiota in mice. Nutrients 7:6294–312 [Google Scholar]
  119. Wang AH, Li M, Li CQ, Kou GJ, Zuo XL, Li YQ. 119.  2016. Human colorectal mucosal microbiota correlates with its host niche physiology revealed by endomicroscopy. Sci. Rep. 6:21952 [Google Scholar]
  120. Wang X, Pierre JF, Heneghan AF, Busch RA, Kudsk KA. 120.  2015. Glutamine improves innate immunity and prevents bacterial enteroinvasion during parenteral nutrition. J. Parenter. Enter. Nutr. 39:688–97 [Google Scholar]
  121. Wildhaber BE, Yang H, Spencer AU, Drongowski RA, Teitelbaum DH. 121.  2005. Lack of enteral nutrition—effects on the intestinal immune system. J. Surg. Res. 123:8–16 [Google Scholar]
  122. Williams DR, Epperson LE, Li W, Hughes MA, Taylor R. 122.  et al. 2005. Seasonally hibernating phenotype assessed through transcript screening. Physiol. Genom. 24:13–22 [Google Scholar]
  123. Wright DP, Rosendale DI, Robertson AM. 123.  2000. Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucin. FEMS Microbiol. Lett. 190:73–79 [Google Scholar]
  124. Yan J, Barnes BM, Kohl F, Marr TG. 124.  2008. Modulation of gene expression in hibernating arctic ground squirrels. Physiol. Genom. 32:170–81 [Google Scholar]
  125. Yang H, Fan YY, Teitelbaum DH. 125.  2003. Intraepithelial lymphocyte-derived interferon-γ evokes enterocyte apoptosis with parenteral nutrition in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 284:G629–37 [Google Scholar]
  126. Yang H, Kiristioglu I, Fan Y, Forbush B, Bishop DK. 126.  et al. 2002. Interferon-gamma expression by intraepithelial lymphocytes results in a loss of epithelial barrier function in a mouse model of total parenteral nutrition. Ann. Surg. 236:226–34 [Google Scholar]
  127. Yasuda K, Oh K, Ren B, Tickle TL, Franzosa EA. 127.  et al. 2015. Biogeography of the intestinal mucosal and lumenal microbiome in the rhesus macaque. Cell Host Microbe 17:385–91 [Google Scholar]
  128. Zietak M, Kovatcheva-Datchary P, Markiewicz LH, Stahlman M, Kozak LP, Backhed F. 128.  2016. Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab 23:1216–23 [Google Scholar]
  129. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben Amor K, Akkermans AD, de Vos WM. 129.  2002. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl. Environ. Microbiol. 68:3401–7 [Google Scholar]
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  • Article Type: Review Article
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