Article

Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J

Department of Chemistry and Biochemistry, University of Colorado, Boulder, CO 80309-0215, USA.
The ISME Journal (Impact Factor: 9.3). 11/2010; 4(11):1375-85. DOI: 10.1038/ismej.2010.71
Source: PubMed

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.

Download full-text

Full-text

Available from: Elizabeth Kate Costello, Feb 11, 2015
  • Source
    • "According to data published by Food and Agriculture Organization of the United Nations (FAO), global soft-shell turtle production reached 348 thousand tons in 2013 and is increasing rapidly, turning it into a multi-billion dollar industry [4]. However, the microbiology of the reptilian gastrointestinal tract (GIT), its composition and effects on the host still remain almost unknown and only a few studies have been published [8, 9]. Most scientific papers are concerned with reptiles only as pathogen carriers and as a zoonotic threat to people10111213. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Probiotics are widely used in nutrition, and their mode of action is intensively studied in mammals and birds; however, it is almost unknown in reptiles. In the present study, Trachemys scripta scripta and Sternotherus odoratus were used to assess the effects of dietary probiotics on chelonian gastrointestinal tract microecology. In the first, 20-week experiment, 40 young T. s. scripta were randomly distributed to four experimental groups: 1st, (CON)-with no additives; 2nd, (SSPA) with Bacillus subtilis PB6; 3rd, (MSP)-with multiple strain probiotic; and 4th, (SSPB) with Bacillus subtilis C-3102. The first study has shown that SSPA and MSP decreased the numbers of total bacteria, Enterobacteriace, Staphylococcus sp. and Streptococcus sp. excreted to water and increased the villous height and mucosa thickness in duodenum. SSPB improved the duodenal microstructure; however, it also increased numbers of kanamycin and vancomycin resistant bacteria, Staphylococcus sp. and Streptococcus sp., in water. In the second, 52-week experiment, 30 S. odoratus were randomly assigned to three dietary treatments. CON, SSPA and MSP groups. The MSP preparation increased the body weight gain, crude ash, Ca and P share in the turtles' shells. Both probiotics affected duodenal histomorphology. SSPA decreased the villous height, while MSP increased the villous height and mucosa thickness, and decreased the crypt depth. SSPA decreased the concentrations of bacteria excreted to water. In the case of intestinal microbiota, bacteria suppressing effects were observed in the case of both probiotics. MSP increased the number of Bifidobacterium sp. and Lactobacillus sp./Enteroccoccus sp., and decreased the number of Clostridium perfringens and Campylobacter sp. in the small intestine. In the large intestine it lowered, amongst others, Bacteroides-Pervotella cluster, Clostridium leptum subgroup and Clostridium perfringens numbers. The above-mentioned results suggest that probiotics are useful in turtle nutrition due to their positive effects on growth performance, shell mineralization, duodenal histomorphology and microbiota.
    Full-text · Article · Mar 2016 · PLoS ONE
    • "Some studies demonstrated the influence of geographic location or environment on the composition (e.g., Yatsunenko et al. 2012), suggesting that perhaps these sets of variables exert the greatest control. Other studies, including one of the Burmese python (Costello et al. 2010) highlight the role of diet or feeding status on modulating the composition of microbial assemblages. Additionally, a similar conclusion has been reached by several studies focusing on the microbial ecology of the GI tracts of humans and other mammals (e.g., Nelson et al. 2013). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Vertebrates coexist with microorganisms in diverse symbiotic associations that range from beneficial to detrimental to the host. Most research has aimed at deciphering the nature of the composite microbial assemblage's genome, or microbiome, from the gastrointestinal (GI) tract and skin of mammals (i.e., humans). In mammals, the GI tract's microbiome aids digestion, enhances uptake of nutrients, and prevents the establishment of pathogenic microorganisms. However, because the GI tract microbiome of the American alligator (Alligator mississippiensis) is distinct from that of all other vertebrates studied to date, being comprised of Fusobacteria in the lower GI tract with lesser abundances of Firmicutes, Proteobacteria, and Bacteroidetes, the function of these assemblages is largely unknown. This review provides a synthesis of our current understanding of the composition of alligators' microbiomes, highlights the potential role of microbiome members in alligators' health (the good), and presents a brief summary of microorganisms detrimental to alligators' health (the bad) including Salmonella spp. and others. Microbial assemblages of the GI tract have co-evolved with their vertebrate host over geologic time, which means that evolutionary hypotheses can be tested using information about the microbiome. For reptiles and amphibians, the number of taxa studied at present is limited, thereby restricting evolutionary insights. Nevertheless, we present a compilation of our current understanding of reptiles' and amphibians' microbiomes, and highlight future avenues of research (the unknown). As in humans, composition of microbiome assemblages provides a promising tool for assessing hosts' health or disease. By further exploring present-day associations between symbiotic microorganisms in the microbiomes of reptiles and amphibians, we can better identify good (beneficial) and bad (detrimental) microorganisms, and unravel the evolutionary history of the acquisition of microbiomes by these poorly-studied vertebrates. © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.
    No preview · Article · Apr 2015 · Integrative and Comparative Biology
  • Source
    • "Whereas species with more flexible diets may exhibit wider variance in gut communities even in natural populations (Nelson et al. 2013; Bolnick et al. 2014b,c), obligate herbivores are likely to be more reliant than other species on stable, specifically functioning gut communities. Studies characterizing reptilian gut microbiota are sparse (Costello et al. 2010; Hong et al. 2011; Keenan et al. 2013; Gaillard 2014) despite the wide-ranging dietary modes and repeated independent evolution of herbivory (Vitt 2004). Thus, further work on a diverse assemblage of reptilian species across a variety of dietary modes is needed to understand the evolution of mutualistic gut microbes in this group. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Herbivorous vertebrates rely on complex communities of mutualistic gut bacteria to facilitate the digestion of celluloses and hemicelluloses. Gut microbes are often convergent based on diet and gut morphology across a phylogenetically diverse group of mammals. However, little is known about microbial communities of herbivorous hindgut-fermenting reptiles. Here, we investigate how factors at the individual level might constrain the composition of gut microbes in an obligate herbivorous reptile. Using multiplexed 16S rRNA gene sequencing, we characterized the fecal microbial community of a population of gopher tortoises (Gopherus polyphemus), and examined how age, genetic diversity, spatial structure, and kinship influence differences among individuals. We recovered phylotypes associated with known cellulolytic function, including candidate phylum Termite Group 3, suggesting their importance for gopher tortoise digestion. Although host genetic structure did not explain variation in microbial composition and community structure, we found that fine-scale spatial structure, inbreeding, degree of relatedness, and possibly ontogeny shaped patterns of diversity in fecal microbiomes of gopher tortoises. Our findings corroborate widespread convergence of fecal-associated microbes based on gut morphology and diet, and demonstrate the role of spatial and demographic structure in driving differentiation of gut microbiota in natural populations. This article is protected by copyright. All rights reserved.
    Full-text · Article · Mar 2015 · Molecular Ecology
Show more