Abstract
Like many hibernators, the 13-lined ground squirrel fasts during winter. The loss of food intake not only affects the hibernator’s gut structure and function but also has the potential to modify the resident gut microbiota. Here we examined the effect of hibernation on numbers of cecal microbes, microbial production of short chain fatty acids, intestinal macromolecular permeability, and expression of the tight junction protein occludin. Compared with the active season, bacteria detected by probes specific for Lactobacillus–Enterococcus and Eubacteria–Clostridium groups were reduced during hibernation but the Bacteroides–Prevotella group was less affected. Cecal concentrations of short chain fatty acids were similar in active season squirrels, aroused hibernators, and hibernators in early torpor, but lower in late torpor. Gut permeability to a macromolecular marker increased during hibernation, as did tight junction localization and phosphorylation of occludin. The results suggest that hibernation selectively alters the gut microbiota, possibly reflecting differential sensitivity to loss of dietary polysaccharides. Hibernation impairs intestinal barrier function, which may require compensatory mechanisms to enhance tight junctional integrity and thus maintain a healthy relationship of the hibernator host with its resident gut microbiota until food intake resumes in the spring.
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References
Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718–15723
Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920
Bailey MT, Walton JC, Dowd SE, Weil ZM, Nelson RJ (2010) Photoperiod modulates gut bacteriabacteria composition in male Siberian hamsters (Phodopus sungorus). Brain Behav Immun 24:577–584
Barnes EM (1970) Effect of hibernation on the intestinal flora. Am J Clin Nutr 23:1519–1524
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
Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70:567–590
Broderick GA, Uden P, Murphy ML, Lapins A (2004) Sources of variation in rates of in vitro ruminal protein degradation. J Dairy Sci 87:1345–1359
Carey HV (1990) Seasonal changes in mucosal structure and function in ground squirrel intestine. Am J Physiol Regul Integr Comp Physiol 259:R385–R392
Carey HV (1992) Effects of fastingfasting and hibernation on ion secretion in ground squirrel intestine. Am J Physiol Regul Integr Comp Physiol 263:R1202–R1208
Cloud-Hansen KA, Villiard KM, Handelsman J, Carey HV (2007) Thirteen-lined ground squirrels (Spermophilus tridecemlineatus) harbor multi-antibiotic resistant bacteria. J Am Assoc Lab Animal Sci 46:17–20
Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK, Hamady M, Knight R, Gordon JI (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci U S A 106:11276–11281
Dokladny K, Moseley PL, Ma TY (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290:G204–G212
Dokladny K, Ye D, Kennedy JC, Moseley PL, Ma TY (2008) Cellular and molecular mechanisms of heat stress-induced up-regulation of occludin protein expression: regulatory role of heat shock factor-1. Am J Pathol 172:659–670
Farshori P, Kachar B (1999) Redistribution and phosphorylation of occludin during opening and resealing of tight junctions bacteria in cultured epithelial cells. J Membr Biol 170:147–156
Ferraris RP, Carey HV (2000) Intestinal transport during fasting and malnutrition. Ann Rev Nutr 20:195–219
Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884
Hume ID, Beiglbock C, Ruf T, Frey-Roos F, Bruns U, Arnold W (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
Kurtz CC, Carey HV (2007) Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol 31:415–428
Leser TD, Lindecrona RH, Jensen TK, Jensen BB, Moller K (2000) Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl Environ Microbiol 66:3290–3296
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
Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848
Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR 2nd, Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189:111–126
Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–457
Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974
Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73:283–309
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
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
Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9:799–809
Vaughan EE, Schut F, Heilig HG, Zoetendal EG, de Vos WM, Akkermans AD (2000) A molecular view of the intestinal ecosystem. Curr Issues Intest Microbiol 1:1–12
Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu PV, Yetukuri L, Islam S, Felin J, Perkins R, Boren J, Oresic M, Backhed F (2010) The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51:1101–1112
Acknowledgments
We thank Michael Grahn for assistance with animal care, and Dr. Glen Broderick (USDA Dairy Forage Research Center, Madison, WI) for SCFA analyses. This work was supported in part by funds from the University of Wisconsin School of Veterinary Medicine.
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Carey, H.V. et al. (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, Heidelberg. https://doi.org/10.1007/978-3-642-28678-0_25
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DOI: https://doi.org/10.1007/978-3-642-28678-0_25
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