Microbial Ecology in States of Health and Disease Workshop Summary (2014) / Chapter Skim
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A6 Seasonal restructuring of the ground squirrel gutmicrobiota over the annual hibernation cycle--Hannah V. Carey, William A. Walters, and Rob Knight
A6 Seasonal restructuring of the ground squirrel gutmicrobiota over the annual hibernation cycle--Hannah V. Carey, William A. Walters, and Rob Knight
Pages 184-206
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From page 184... ...
Winter fasting in these species eliminates a major source of degradable substrates to support growth of gut microbes, which may affect microbial community structure and hostmicrobial interactions. We explored the effect of the annual hibernation cycle on gut microbiotas using deep sequencing of 16S rRNA genes from ground squirrel cecal contents.
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From page 185... ...
Hibernation reduced cecal short-chain fatty acid and ammonia concentrations, and increased and decreased concentrations of acetate and butyrate, respectively. These results indicate that the ground squirrel microbiota is restructured each year in a manner that reflects differences in microbial preferences for dietary vs.
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From page 186... ...
, which is an aspect of host biology that is both influenced by, and can itself influence, the microbiota. Here, we demonstrate an annual reorganization of the cecal microbiota in 13-lined ground squirrels that reflects the dominant role of host diet in shaping microbial community structure.
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From page 187... ...
SCFA and Ammonia Analyses After thawing, an aliquot of the acidified cecal contents was analyzed by gas chromatography for total SCFA concentrations and molar proportions of propionate, acetate, and butyrate. A separate aliquot was used to measure ammonia concentrations using a kit (no.
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From page 188... ...
For aroused hibernators, days in last torpor bout indicates length of last bout prior to arousal; for torpid squirrels, number of days in continuous torpor.
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From page 189... ...
) , Chao1, and observed species were calculated to determine alpha diversity for squirrel seasonal groups.
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From page 190... ...
Because of this, in subsequent microbiota analyses, torpid and aroused hibernators were combined within the respective Early or Late Winter groups. Age of the animals had no effect on microbiota clustering; for example, Spring microbiotas clustered more closely with those from Mother and Summer squirrels than with the Late Winter group, despite Spring and Late Winter squirrels being closest in age (Figure A6-1, Table A6-1)
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From page 191... ...
diversity within certain clades as environmental selection changes through the hibernation states. Taxonomic Composition of Squirrel Microbiotas Eight bacterial phyla were identified in the ground squirrel microbiota (Supplemental Table S127)
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192 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE FIGURE A6-2 Alpha diversity rarefaction plots of squirrel cecal microbiotas. Top: phylogenetic diversity (PD)
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. Sequences within this phylum matched to a single species, Akkermansia muciniphila (Supplemental Table S1)
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From page 194... ...
Asterisks indicate unclassified families within a taxonomic group. Taxa with relative abundances less than 1.5% were not included.
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From page 195... ...
Butyrate concentration was most affected by hibernation, falling to nearly undetectable levels in many hibernator samples and particularly those from torpid squirrels. Values from two Spring squirrels shown in Table A6-2 were not included in the statistical analysis due to low sample size; however, those data suggest that Spring SCFA concentrations remain closer to winter levels than to Summer, despite the 2-wk period of refeeding and constant homeothermy, which would stimulate rapid production of SCFA from dietary substrates.
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From page 196... ...
. For SCFA, groups analyzed with Kruskal-Wallis test were Summer squirrels and aroused hibernators in Early and Late Winter (no torpid Early Winter samples were available, and the two Spring squirrel samples were not included due to low sample size)
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From page 197... ...
Our UniFrac analysis of 16S rRNA gene sequences confirmed that season plays a dominant role in the structure of ground squirrel microbial communities, as indicated by the close clustering of microbiotas of Spring and Summer pups with those of their Mothers, and the separate clustering of microbiotas in the Winter groups. Moreover, within the hibernation season, the microbiotas of Late Winter squirrels were more tightly clustered than were Early Winter animals, indicating that the Early Winter microbiota is a transitional state that precedes the more severe contraction of the community after 4–5 mo of continuous fasting.
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From page 198... ...
season, and the two seasonal groups that were closest in age -- Late Winter and Spring -- had microbiotas that were the most diverse. FIGURE A6-5 Schematic illustrating major changes in the ground squirrel gut microbiota over the annual hibernation.
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From page 199... ...
That said, we may not have been able to detect subtle, but significant, changes in microbiota structure that reflect dominance of certain species that function better than others at low temperatures. Similar to other mammals, the majority of sequences in the ground squirrel microbiota was assigned to the bacterial phyla Bacteroidetes and Firmicutes, with Verrucomicrobia comprising the next most abundant group.
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From page 200... ...
The lower cecal butyrate concentration during winter may contribute to the changes in intestinal structure and function observed in hibernating squirrels. As the preferred fuel source for epithelial cells, butyrate stimulates epithelial proliferation and restitution, and helps maintain integrity of the intestinal barrier through modulation of apoptosis, permeability, and mucus production (Bugaut and Bentejac, 1993; Gaudier et al., 2004; Louis and Flint, 2009; Peng et al., 2007)
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From page 201... ...
In fact, several changes we noted in the microbiotas of hibernating 13-lined ground squirrels were comparable to those in fasted, but not hibernating hamsters; for example, the fasted hamster microbiota had a greater proportion of sequences represented by A muciniphila, and reduced representation of Firmicutes, including Lachnospiraceae (Sonoyama et al., 2009)
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From page 202... ...
that is well tolerated by both the ground squirrel host and its microbial symbionts. Our study revealed how the gut microbial community responds to this perturbation in terms of taxonomic structure but did not provide insight into functional changes in the microbiome (i.e., the microbiota and their complement of genes and gene products)
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From page 203... ...
Am J Physiol Regul Integr Comp Physiol 296: R383–R393, 2009. Ardawi MS, Newsholme EA.
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From page 204... ...
Impact of hibernation on gut microbiota and intestinal barrier function in ground squirrels. In: Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations , edited by Ruf T, Bieber C, Arnold A, and Millesi E
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Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am J Physiol 228: 325–330, 1975.
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From page 206... ...
The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51: 1101–1112, 2010.
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