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. 2010 Nov;4(11):1375-85.
doi: 10.1038/ismej.2010.71. Epub 2010 Jun 3.

Postprandial Remodeling of the Gut Microbiota in Burmese Pythons

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Free PMC article

Postprandial Remodeling of the Gut Microbiota in Burmese Pythons

Elizabeth K Costello et al. ISME J. .
Free PMC article

Abstract

The vertebrate gut microbiota evolved in an environment typified by periodic fluctuations in nutrient availability, yet little is known about its responses to host feeding and fasting. As many model species (for example, mice) are adapted to lifestyles of frequent small meals, we turned to the Burmese python, a sit-and-wait foraging snake that consumes large prey at long intervals (>1 month), to examine the effects of a dynamic nutrient milieu on the gut microbiota. We used multiplexed 16S rRNA gene pyrosequencing to characterize bacterial communities harvested from the intestines of fasted and digesting snakes, and from their rodent meal. In this unprecedented survey of a reptilian host, we found that Bacteroidetes and Firmicutes numerically dominated the python gut. In the large intestine, fasting was associated with increased abundances of the genera Bacteroides, Rikenella, Synergistes and Akkermansia, and with reduced overall diversity. A marked postprandial shift in bacterial community configuration occurred. Between 12 h and 3 days after feeding, Firmicutes, including the taxa Clostridium, Lactobacillus and Peptostreptococcaceae, gradually outnumbered the fasting-dominant Bacteroidetes, and overall 'species'-level diversity increased significantly. Most lineages seemed to be indigenous to the python rather than ingested with the meal, but a dietary source of Lactobacillus could not be ruled out. Thus, the observed large-scale alterations of the gut microbiota that accompany the Burmese python's own dramatic physiological and morphological changes during feeding and fasting emphasize the need to consider both microbial and host cellular responses to nutrient flux. The Burmese python may provide a unique model for dissecting these interrelationships.

Figures

Figure 1
Figure 1
Digestion alters bacterial community membership and taxon relative abundances within the Burmese python large intestine. (a) Average mass of large intestinal contents harvested at each time point (right axis) and unweighted UniFrac distance between fasted and fed communities and, for the fasted time point, between fasted samples only (left axis). (b and c) Average proportional abundance of sequences classified as (b) Bacteroidetes or Firmicutes or as (c) selected Firmicutes taxa at each time point. Because other lineages can also be present, the proportions need not add up to 100%. Error bars indicate one standard error of the mean. Fasted snakes were fed a rodent meal equal to 25% of their body mass. Contents mass shown in (a) does not include the cecum, which contained ∼3-4 g of material on days 2 through 10.
Figure 2
Figure 2
Digestion increases bacterial community diversity and ‘species’ richness within the Burmese python large intestine. (a) Rarefaction curves for phylogenetic diversity measured by the average total branch length in a phylogenetic tree per sample after a specified number of sequences was observed. (b) Rarefaction curves for ‘species’ richness measured by determining the average number of OTUs defined at ≥ 97% sequence similarity per sample. Samples were partitioned into three post-feeding time intervals based on results shown in Figure 1b. Bars indicate 95% confidence intervals. DPF, days post-feeding.
Figure 3
Figure 3
Average proportional abundance of sequences classified as Bacteroidetes or Firmicutes from the Burmese python small intestine at each time point. Because other lineages can also be present, the proportions need not add up to 100%. Error bars are one standard error of the mean. For fasted, N = 1.
Figure 4
Figure 4
Python intestine and rodent meal (i.e., whole rat) bacterial communities appear to have largely divergent membership. Communities clustered using PCoA of unweighted UniFrac distance matrices. Each circle corresponds to a sample colored according to host species. The percentage of the variation explained by the plotted principal coordinates is indicated on the axes. Each panel shows a different taxon-specific analysis. These taxa are: (a) all Bacteria, (b) all Bacteroidetes (note that the four rat samples appear superimposed in this panel), (c) all Firmicutes, (d) all Bacteria but excluding Lactobacillus, (e) all Firmicutes but excluding Lactobacillus, (f) Clostridiales, (g) Peptostreptococcaceae, (h) Lactobacillus. Comparisons of panels a and d, and c and e, show that the Lactobacillus component, which was not host specific, did not greatly influence the clarity of separation in the snake and rat communities. Samples were excluded if they contained fewer than 30 sequences from the specified taxon.

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