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The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas.

ABSTRACT: The gut microbiome (GMB) of folivores metabolizes dietary fiber into nutrients, including short-chain fatty acids (SCFAs); however, experiments probing the consequences of foliage quality on host GMBs are lacking. We therefore examined GMB structure and function via amplicon sequencing and Nuclear Magnetic Resonance spectroscopy in 31 captive sifakas (Propithecus coquereli) during dietary manipulations associated with husbandry. Supplementing standard diets with diverse foliage blends, versus with a single plant species, promoted more diverse GMBs, enriched for taxa implicated in plant-fiber metabolism, but depleted in taxa implicated in starch metabolism and bile tolerance. The consumption of diverse blends was associated with greater concentrations of colonic SCFAs. Abundant foliage, via forest access, promoted compositionally distinct and more stable GMBs, but reduced concentrations of SCFAs, possibly reflecting selection of high-quality leaves. In 11 subjects denied forest access, we examined the temporal pace of microbial shifts when supplemental foliage was abruptly switched between diverse blends and single species. The sifaka GMB responded within days, with community diversity and composition closely tracking foliage diversity. By providing experimental evidence that the folivore GMB is sensitive to minor changes in dietary foliage, we reveal the fragility of specialist GMBs, with implications for managing the wellbeing of endangered wildlife.

SUBMITTER: Greene LK

PROVIDER: S-EPMC6160417 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas.

Greene Lydia K LK McKenney Erin A EA O'Connell Thomas M TM Drea Christine M CM

Scientific reports 20180927 1

The gut microbiome (GMB) of folivores metabolizes dietary fiber into nutrients, including short-chain fatty acids (SCFAs); however, experiments probing the consequences of foliage quality on host GMBs are lacking. We therefore examined GMB structure and function via amplicon sequencing and Nuclear Magnetic Resonance spectroscopy in 31 captive sifakas (Propithecus coquereli) during dietary manipulations associated with husbandry. Supplementing standard diets with diverse foliage blends, versus wi ...[more]

PMID: 30262842

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Project description:BackgroundCaptive animals, compared to their wild counterparts, generally harbor imbalanced gut microbiota owing, in part, to their altered diets. This imbalance is particularly striking for folivores that fundamentally rely on gut microbiota for digestion, yet rarely receive sufficient dietary fiber in captivity. We examine the critically endangered Coquerel's sifaka (Propithecus coquereli), an anatomically specialized, rather than facultative, folivore that consumes a seasonal frugo-folivorous diet in the wild, but is provisioned predominantly with seasonal foliage and orchard vegetables in captivity. Using amplicon and metagenomic sequencing applied to fecal samples collected from two wild and one captive population (each comprising multiple groups), we clarify how dietary variation underlies the perturbational effect of captivity on the structure and function of this species' gut microbiota.ResultsThe gut microbiota of wild sifakas varied by study population, most notably in community evenness and in the abundance of diet-associated microbes from Prevotellaeceae and Lachnospiraceae. Nevertheless, the differences among wild subjects were minor compared to those evident between wild and captive sifakas: Unusually, the consortia of captive sifakas were the most diverse, but lacked representation of endemic Bacteroidetes and metagenomic capacity for essential amino-acid biosynthesis. Instead, they were enriched for complex fiber metabolizers from the Firmicutes phylum, for archaeal methanogens, and for several metabolic pathways putatively linked to plant fiber and secondary compound metabolism.ConclusionsThe relatively minor differences in gut microbial structure and function between wild sifaka populations likely reflect regional and/or temporal environmental variability, whereas the major differences observed in captive conspecifics, including the loss of endemic microbes, but gain in low-abundance taxa, likely reflect imbalanced or unstable consortia. Indeed, community perturbation may not necessarily entail decreased community diversity. Moreover, signatures of greater fiber degradation indicate that captive sifakas consume a more fibrous diet compared to their wild counterparts. These results do not mirror those typically reported for folivores and herbivores, suggesting that the direction and strength of captivity-induced 'dysbiosis' may not be universal across species with similar feeding strategies. We propose that tailored, species-specific dietary interventions in captivity, aimed at better approximating naturally foraged diets, could functionally 'rewild' gut microbiota and facilitate successful management of diverse species.

Project description:Diet can influence the composition of the human microbiome, and yet relatively few dietary ingredients have been systematically investigated with respect to their impact on the functional potential of the microbiome. Dietary resistant starch (RS) has been shown to have health benefits, but we lack a mechanistic understanding of the metabolic processes that occur in the gut during digestion of RS. Here, we collected samples during a dietary crossover study with diets containing large or small amounts of RS. We determined the impact of RS on the gut microbiome and metabolic pathways in the gut, using a combination of "omics" approaches, including 16S rRNA gene sequencing, metaproteomics, and metabolomics. This multiomics approach captured changes in the abundance of specific bacterial species, proteins, and metabolites after a diet high in resistant starch (HRS), providing key insights into the influence of dietary interventions on the gut microbiome. The combined data showed that a high-RS diet caused an increase in the ratio of Firmicutes to Bacteroidetes, including increases in relative abundances of some specific members of the Firmicutes and concurrent increases in enzymatic pathways and metabolites involved in lipid metabolism in the gut.IMPORTANCE This work was undertaken to obtain a mechanistic understanding of the complex interplay between diet and the microorganisms residing in the intestine. Although it is known that gut microbes play a key role in digestion of the food that we consume, the specific contributions of different microorganisms are not well understood. In addition, the metabolic pathways and resultant products of metabolism during digestion are highly complex. To address these knowledge gaps, we used a combination of molecular approaches to determine the identities of the microorganisms in the gut during digestion of dietary starch as well as the metabolic pathways that they carry out. Together, these data provide a more complete picture of the function of the gut microbiome in digestion, including links between an RS diet and lipid metabolism and novel linkages between specific gut microbes and their metabolites and proteins produced in the gut.

Project description:Background: The gut microbiome (GMB) is the first line of defense against enteric pathogens, which are a leading cause of disease and mortality worldwide. One such pathogen, the protozoan Cryptosporidium, causes a variety of digestive disorders that can be devastating and even lethal. The Coquerel's sifaka (Propithecus coquereli) - an endangered, folivorous primate endemic to Madagascar - is precariously susceptible to cryptosporidiosis under captive conditions. If left untreated, infection can rapidly advance to morbidity and death. Objective: To gain a richer understanding of the pathophysiology of this pathogen while also improving captive management of endangered species, we examine the impact of cryptosporidiosis on the GMB of a flagship species known to experience a debilitating disease state upon infection. Design: Using 16S sequencing of DNA extracted from sifaka fecal samples, we compared the microbial communities of healthy sifakas to those of infected individuals, across infection and recovery periods. Results: Over the course of infection, we found that the sifaka GMB responds with decreased microbial diversity and increased community dissimilarity. Compared to the GMB of unaffected individuals, as well as during pre-infection and recovery periods, the GMB during active infection was enriched for microbial taxa associated with dysbiosis and rapid transit time. Time to recovery was inversely related to age, with young animals being slowest to recover GMB diversity and full community membership. Antimicrobial treatment during infection caused a significant depletion in GMB diversity. Conclusions: Although individual sifakas show unique trajectories of microbial loss and recolonization in response to infection, recovering sifakas exhibit remarkably consistent patterns, similar to initial community assembly of the GMB in infants. This observation, in particular, provides biological insight into the rules by which the GMB recovers from the disease state. Fecal transfaunation may prove effective in restoring a healthy GMB in animals with specialized diets.

Project description:BackgroundThe infant intestinal microbiome plays an important role in metabolism and immune development with impacts on lifelong health. The linkage between the taxonomic composition of the microbiome and its metabolic phenotype is undefined and complicated by redundancies in the taxon-function relationship within microbial communities. To inform a more mechanistic understanding of the relationship between the microbiome and health, we performed an integrative statistical and machine learning-based analysis of microbe taxonomic structure and metabolic function in order to characterize the taxa-function relationship in early life.ResultsStool samples collected from infants enrolled in the New Hampshire Birth Cohort Study (NHBCS) at approximately 6-weeks (n = 158) and 12-months (n = 282) of age were profiled using targeted and untargeted nuclear magnetic resonance (NMR) spectroscopy as well as DNA sequencing of the V4-V5 hypervariable region from the bacterial 16S rRNA gene. There was significant inter-omic concordance based on Procrustes analysis (6 weeks: p = 0.056; 12 months: p = 0.001), however this association was no longer significant when accounting for phylogenetic relationships using generalized UniFrac distance metric (6 weeks: p = 0.376; 12 months: p = 0.069). Sparse canonical correlation analysis showed significant correlation, as well as identifying sets of microbe/metabolites driving microbiome-metabolome relatedness. Performance of machine learning models varied across different metabolites, with support vector machines (radial basis function kernel) being the consistently top ranked model. However, predictive R2 values demonstrated poor predictive performance across all models assessed (avg: - 5.06% -- 6 weeks; - 3.7% -- 12 months). Conversely, the Spearman correlation metric was higher (avg: 0.344-6 weeks; 0.265-12 months). This demonstrated that taxonomic relative abundance was not predictive of metabolite concentrations.ConclusionsOur results suggest a degree of overall association between taxonomic profiles and metabolite concentrations. However, lack of predictive capacity for stool metabolic signatures reflects, in part, the possible role of functional redundancy in defining the taxa-function relationship in early life as well as the bidirectional nature of the microbiome-metabolome association. Our results provide evidence in favor of a multi-omic approach for microbiome studies, especially those focused on health outcomes.

Dataset Information

The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas.

Publications

The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas.

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