Hibernation alters the diversity and composition of mucosa-associated bacteria while enhancing antimicrobial defence in the gut of 13-lined ground squirrels

Molecular Ecology

Volumn 23, Issue 18, 2014, Pages 4658-4669

  Dill Mcfarland, Kimberly A ^a   Neil, Katie L ^b   Zeng, Austin ^b   Sprenger, Ryan J ^c   Kurtz, Courtney C ^c   Suen, Garret ^a   Carey, Hannah V ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN OSHKOSH   (United States)

Author keywords

Diet; Fasting; Hibernation; Host microbe interactions; Microbiota; Pyrosequencing

Indexed keywords

MUCIN 2; RNA 16S; TOLL LIKE RECEPTOR;

ANIMAL; ARTICLE; BACTERIUM; CECUM; CLASSIFICATION; DIET; DIET RESTRICTION; DNA SEQUENCE; FEMALE; GASTROINTESTINAL TRACT; GENETICS; HIBERNATION; HOST-MICROBE INTERACTIONS; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA; PYROSEQUENCING; SCIURIDAE; SEASON;

DIET; FASTING; HIBERNATION; HOST-MICROBE INTERACTIONS; MICROBIOTA; PYROSEQUENCING;

ANIMALS; BACTERIA; CECUM; FEMALE; GASTROINTESTINAL TRACT; HIBERNATION; INTESTINAL MUCOSA; MICROBIOTA; MUCIN-2; RNA, RIBOSOMAL, 16S; SCIURIDAE; SEASONS; SEQUENCE ANALYSIS, DNA; TOLL-LIKE RECEPTORS;

EID: 84908115906     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12884     Document Type: Article

References (56)

1. Backhed F, Ding H, Wang T et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America, 101, 15718-15723.
2. Biswas A, Wilmanski J, Forsman H et al. (2011) Negative regulation of Toll-like receptor signaling plays an essential role in homeostasis of the intestine. European Journal of Immunology, 41, 182-194.
3. Carey HV (1990) Seasonal changes in mucosal structure and function in ground squirrel intestine. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 259, R385-R392.
4. Carey HV, Duddleston KN (2014) Animal-microbial symbioses in changing environments. Journal of Thermal Biology, 44, 78-84.
5. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiological Reviews, 83, 1153-1181.
6. Carey HV, Pike AC, Weber CR et al. (2012) Impact of hibernation on gut microbiota and intestinal barrier function in ground squirrels. In: Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations (eds Ruf T, Bieber C, Arnold A, Millesi E), pp. 281-291. Springer, Heidelberg.
7. Carey HV, Walters WA, Knight R (2013) Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 304, R33-R42.
8. Crawford PA, Crowley JR, Sambandam N et al. (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proceedings of the National Academy of Sciences of the United States of America, 106, 11276-11281.
9. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience, 13, 701-712.
10. Cullender TC, Chassaing B, Janzon A et al. (2013) Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host & Microbe, 14, 571-581.
11. David LA, Maurice CF, Carmody RN et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505, 559-563.
12. De Filippo C, Cavalieri D, Di Paola M et al. (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America, 107, 14691-14696.
13. Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp nov, a human intestinal mucin-degrading bacterium. International Journal of Systematic and Evolutionary Microbiology, 54, 1469-1476.
14. DeSantis TZ, Hugenholtz P, Larsen N et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environment Microbiology, 72, 5069-5072.
15. El Aidy S, Derrien M, Merrifield CA et al. (2013) Gut bacteriahost metabolic interplay during conventionalisation of the mouse germfree colon. ISME Journal, 7, 743-755.
16. Faith JJ, McNulty NP, Rey FE, Gordon JI (2011) Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science, 333, 101-104.
17. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes, 3, 289-306.
18. Good I (1952) The population frequencies of species and the estimation of population parameters. Biometrika, 40, 237-264.
19. Gower J (1966) A Q-technique for the calculation of canonical variates. Biometrika, 53, 588-590.
20. Herlemann DP, Geissinger O, Ikeda-Ohtsubo W et al. (2009) Genomic analysis of "Elusimicrobium minutum", the first cultivated representative of the phylum "Elusimicrobia" (formerly termite group 1). Applied and Environment Microbiology, 75, 2841-2849.
21. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science, 336, 1268-1273.
22. Horn HS (1966) Measurement of "overlap" in comparative ecological studies. The American Naturalist, 100, 419-424.
23. Kashyap PC, Marcobal A, Ursell LK et al. (2013) Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proceedings of the National Academy of Sciences of the United States of America, 110, 17059-17064.
24. Koenig JE, Spor A, Scalfone N et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 108, 4578-4585.
25. Kohl KD, Dearing MD (2013) Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environmental Microbiology Reports, 6, 191-195.
26. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. Journal of American Statistical Association, 47, 583-621.
27. Kurtz CC, Carey HV (2007) Seasonal changes in the intestinal immune system of hibernating ground squirrels. Developmental and Comparative Immunology, 31, 415-428.
28. Liu Y, Fatheree NY, Mangalat N, Rhoads JM (2012) Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-kappaB signaling in the intestine. American Journal of Physiology. Gastrointestinal and Liver Physiology, 302, G608-G617.
29. Lozupone C, Hamady M, Knight R (2006) UniFrac-An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics, 7, 371.
30. Marcobal A, Southwick AM, Earle KA, Sonnenburg JL (2013) A refined palate: bacterial consumption of host glycans in the gut. Glycobiology, 23, 1038-1046.
31. 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.
32. McFall-Ngai M, Hadfield MG, Bosch TC et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229-3236.
33. McGuckin MA, Linden SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nature Reviews Microbiology, 9, 265-278.
34. Morita RY (1975) Psychrophilic bacteria. Bacteriological Reviews, 39, 144-167.
35. Okada T, Fukuda S, Hase K et al. (2013) Microbiota-derived lactate accelerates colon epithelial cell turnover in starvationrefed mice. Nature Communications, 4, 1654.
36. Ouwerkerk JP, de Vos WM, Belzer C (2013) Glycobiome: bacteria and mucus at the epithelial interface. Best Practice & Research Clinical Gastroenterology, 27, 25-38.
37. Pengelley ET, Fisher KC (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis tescorum. Canadian Journal of Zoology, 39, 105-120.
38. Png CW, Linden SK, Gilshenan KS et al. (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. American Journal of Gastroenterology, 105, 2420-2428.
39. Prescott D, Lee J, Philpott DJ (2013) An epithelial armamentarium to sense the microbiota. Seminars in Immunology, 25, 323-333.
40. Pruesse E, Quast C, Knittel K et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research, 35, 7188-7196.
41. Quince C (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics, 12, 38.
42. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell, 118, 229-241.
43. Salyers AA, Vercellotti JR, West SE, Wilkins TD (1977) Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Applied and Environment Microbiology, 33, 319-322.
44. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environment Microbiology, 71, 1501-1506.
45. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environment Microbiology, 75, 7537-7541.
46. Schluter J, Foster KR (2012) The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biology, 10, e1001424.
47. Shannon CE (2001) A mathematical theory of communication. SIGMOBILE Mobile Computing and Communications Review, 5, 3-55.
48. Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. University of Kansas Science Bulletin, 38, 1409-1438.
49. Sonnenburg JL, Xu J, Leip DD et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science, 307, 1955-1959.
50. Sonoyama K, Fujiwara R, Takemura N et al. (2009) Response of gut microbiota to fasting and hibernation in Syrian hamsters. Applied and Environment Microbiology, 75, 6451-6456.
51. Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences of the United States of America, 99, 15451-15455.
52. Stevenson TJ, Duddleston KN, Buck CL (2014) The cecal microbial community of the arctic ground squirrel shifts in diversity, activity and numbers across the hibernation season. Applied and Environment Microbiology, 80, 5611-5622.
53. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S (2011) The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiology Reviews, 35, 681-704.
54. Vijay-Kumar M, Sanders CJ, Taylor RT et al. (2007) Deletion of TLR5 results in spontaneous colitis in mice. The Journal of Clinical Investigation, 117, 3909-3921.
55. Wang Y, Devkota S, Musch MW et al. (2010) Regional mucosaassociated microbiota determine physiological expression of TLR2 and TLR4 in murine colon. PLoS ONE, 5, e13607.
56. Zoetendal EG, von Wright A, Vilpponen-Salmela T et al. (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Applied and Environment Microbiology, 68, 3401-3407.