Dataset Information

Potential Mechanism of Detoxification of Cyanide Compounds by Gut Microbiomes of Bamboo-Eating Pandas.

ABSTRACT: Gut microbes can enhance the ability of hosts to consume secondary plant compounds and, therefore, expand the dietary niche breadth of mammalian herbivores. The giant and red pandas are bamboo-eating specialists within the mammalian order Carnivora. Bamboo contains abundant plant secondary metabolites (e.g., cyanide-containing compounds). However, Carnivora species, including the giant panda, have deficient levels of rhodanese (one of the essential cyanide detoxification enzymes) in their tissues compared with the same tissues of herbivores. Here, we make a comparative analysis of 94 gut metagenomes, including 25 from bamboo-eating pandas (19 from giant pandas and 6 from red pandas), 30 from Père David's deer, and 39 from published data for other mammals. The bamboo-eating pandas' gut microbiomes had some common features, such as high proportions of Pseudomonas bacteria. The results revealed that bamboo-eating pandas' gut microbiomes were significantly enriched in putative genes coding for enzymes related to cyanide degradation (e.g., rhodanese) compared with the gut microbiomes of typical herbivorous mammals, which might have coevolved with their special bamboo diets. The enrichment of putative cyanide-digesting gut microbes, in combination with adaptations related to morphology (e.g., pseudothumbs) and genomic signatures, show that the giant panda and red panda have evolved some common traits to adapt to their bamboo diet.IMPORTANCE The giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens), two obligate bamboo feeders, have distinct phylogenetic positions in the order Carnivora. Bamboo is extraordinarily rich in plant secondary metabolites, such as allied phenolic and polyphenolic compounds and even toxic cyanide compounds. Here, the enrichment of putative cyanide-digesting gut microbes, in combination with adaptations related to morphology (e.g., pseudothumbs) and genomic signatures, show that the giant panda and red panda have evolved some common traits to adapt to their bamboo diet. Thus, here is another story of diet-driven gut microbiota in nature.

SUBMITTER: Zhu L

PROVIDER: S-EPMC6001608 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Potential Mechanism of Detoxification of Cyanide Compounds by Gut Microbiomes of Bamboo-Eating Pandas.

Zhu Lifeng L Yang Zhisong Z Yao Ran R Xu Liangliang L Chen Hua H Gu Xiaodong X Wu Tonggui T Yang Xuyu X

mSphere 20180613 3

Gut microbes can enhance the ability of hosts to consume secondary plant compounds and, therefore, expand the dietary niche breadth of mammalian herbivores. The giant and red pandas are bamboo-eating specialists within the mammalian order Carnivora. Bamboo contains abundant plant secondary metabolites (e.g., cyanide-containing compounds). However, Carnivora species, including the giant panda, have deficient levels of rhodanese (one of the essential cyanide detoxification enzymes) in their tissue ...[more]

PMID: 29898983

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Project description:BackgroundIt is inevitable to change the function or expression of genes during the environmental adaption of species. Both the giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to Carnivora and have developed similar adaptations to the same dietary switch to bamboos at the morphological and genomic levels. However, the genetic adaptation at the gene expression level is unclear. Therefore, we aimed to examine the gene expression patterns of giant and red panda convergent specialized bamboo-diets. We examined differences in liver and pancreas transcriptomes between the two panda species and other non-herbivorous species.ResultsThe clustering and PCA plots suggested that the specialized bamboo diet may drive similar expression shifts in these two species of pandas. Therefore, we focused on shared liver and pancreas DEGs (differentially expressed genes) in the giant and red panda relative to other non-herbivorous species. Genetic convergence occurred at multiple levels spanning carbohydrate metabolism, lipid metabolism, and lysine degradation. The shared adaptive convergence DEGs in both organs probably be an evolutionary response to the high carbohydrate, low lipid and lysine bamboo diet. Convergent expression of those nutrient metabolism-related genes in both pandas was an intricate process and subjected to multi-level regulation, including DNA methylation and transcription factor. A large number of lysine degradation and lipid metabolism related genes were hypermethylated in promoter regions in the red panda. Most genes related to carbohydrate metabolism had reduced DNA methylation with increased mRNA expression in giant pandas. Unlike the red panda, the core gene of the lysine degradation pathway (AASS) doesn't exhibit hypermethylation modification in the giant panda, and dual-luciferase reporter assay showed that transcription factor, NR3C1, functions as a transcriptional activator in AASS transcription through the binding to AASS promoter region.ConclusionsOur results revealed the adaptive expressions and regulations of the metabolism-related genes responding to the unique nutrients in bamboo food and provided data accumulation and research hints for the future revelation of complex mechanism of two pandas underlying convergent adaptation to a specialized bamboo diet.

Project description:UNLABELLED:The giant panda evolved from omnivorous bears. It lives on a bamboo-dominated diet at present, but it still retains a typical carnivorous digestive system and is genetically deficient in cellulose-digesting enzymes. To find out whether this endangered mammalian species, like other herbivores, has successfully developed a gut microbiota adapted to its fiber-rich diet, we conducted a 16S rRNA gene-based large-scale structural profiling of the giant panda fecal microbiota. Forty-five captive individuals were sampled in spring, summer, and late autumn within 1 year. Significant intraindividual variations in the diversity and structure of gut microbiota across seasons were observed in this population, which were even greater than the variations between individuals. Compared with published data sets involving 124 gut microbiota profiles from 54 mammalian species, these giant pandas, together with 9 captive and 7 wild individuals investigated previously, showed extremely low gut microbiota diversity and an overall structure that diverged from those of nonpanda herbivores but converged with those of carnivorous and omnivorous bears. The giant panda did not harbor putative cellulose-degrading phylotypes such as Ruminococcaceae and Bacteroides bacteria that are typically enriched in other herbivores, but instead, its microbiota was dominated by Escherichia/Shigella and Streptococcus bacteria. Members of the class Clostridia were common and abundant in the giant panda gut microbiota, but most of the members present were absent in other herbivores and were not phylogenetically related with known cellulolytic lineages. Therefore, the giant panda appears not to have evolved a gut microbiota compatible with its newly adopted diet, which may adversely influence the coevolutionary fitness of this herbivore. IMPORTANCE:The giant panda, an endangered mammalian species endemic to western China, is well known for its unique bamboo diet. Unlike other herbivores that have successfully evolved anatomically specialized digestive systems to efficiently deconstruct fibrous plant matter, the giant panda still retains a gastrointestinal tract typical of carnivores. We characterized the fecal bacterial communities from a giant panda population to determine whether this animal relies on its symbiotic gut microbiota to cope with the complex carbohydrates that dominate its diet, as is common in other herbivores. We found that the giant panda gut microbiota is low in diversity and highly variable across seasons. It also shows an overall composition typical of bears and entirely differentiated from other herbivores, with low levels of putative cellulose-digesting bacteria. The gut microbiota of this herbivore, therefore, may not have well adapted to its highly fibrous diet, suggesting a potential link with its poor digestive efficiency.

Project description:Giant pandas have developed a series of foraging strategies to adapt to their special bamboo diets. Although bamboo is an important food resource for giant pandas in Liziping National Nature Reserve (Liziping NR), China, there are relatively few studies on their phyllosphere fungal community and its influencing factors. Herein, we used ITS1 amplification and metagenomic sequencing to analyze the phyllosphere fungi diversity and functions (KEGG, CAZyme, and antibiotic resistance gene) and explore the influencing factors for the three giant pandas foraging bamboo species (Arundinaria spanostachya, AS; Yushania lineolate, YL; and Fargesia ferax, FF) over different seasons (spring vs. autumn) in Liziping NR, China. We found that Ascomycota and Basidiomycota were the most dominant phyla in the bamboo phyllosphere. The alpha diversity (e.g., the Sobs index and Shannon index) was relatively higher in autumn samples than in spring samples, and the community structure differed significantly between the three bamboo species in spring and autumn. Some biotic and abiotic variables (e.g., the elevation and mean base diameter of bamboo) significantly influenced the abundance, diversity, and community structure of the bamboo phyllosphere fungal community. Moreover, the functional analysis showed the differences in the glycoside hydrolase community and antibiotic resistance gene (ARG) profile between spring and autumn samples. Co-occurrence network modeling suggested that AS phyllosphere fungal communities in autumn employed a much more complex network than that in spring, and the abundance of multidrug, tetracycline, and glycopeptide resistance genes was high and closely correlated with other ARGs. These results indicate that fungal community's abundance, diversity, and community structure are mainly affected by the season, host species, and elevation. The season and host species are major factors affecting the biological functions (KEGG and CAZyme), ARGs, and interactions between sympatric bacterial and fungal communities in bamboo phyllosphere. This integrated study can provide a reference basis for the seasonal management of bamboo resources foraged by wild giant pandas, and predict the risk of antibiotic resistance in bamboo phyllosphere fungal flora in Liziping NR (Xiaoxiangling mountains), China.

Project description:The giant panda is known worldwide for having successfully moved to a diet almost exclusively based on bamboo. Provided that no lignocellulose-degrading enzyme was detected in panda's genome, bamboo digestion is believed to depend on its gut microbiome. However, pandas retain the digestive system of a carnivore, with retention times of maximum 12 h. Cultivation of their unique gut microbiome under controlled laboratory conditions may be a valid tool to understand giant pandas' dietary habits, and provide valuable insights about what component of lignocellulose may be metabolized. Here, we collected gut microbiomes from fresh fecal samples of a giant panda (either entirely green or yellow stools) and supplied them with green leaves or yellow pith (i.e., the peeled stem). Microbial community composition was substrate dependent, and resulted in markedly different fermentation profiles, with yellow pith fermented to lactate and green leaves to lactate, acetate and ethanol, the latter to strikingly high concentrations (∼3%, v:v, within 3.5 h). Microbial metaproteins pointed to hemicellulose rather than cellulose degradation. The alpha-amylase from the giant panda (E.C. 3.2.1.1) was the predominant identified metaprotein, particularly in reactors inoculated with pellets derived from fecal samples (up to 60%). Gut microbiomes assemblage was most prominently impacted by the change in substrate (either leaf or pith). Removal of soluble organics from inocula to force lignocellulose degradation significantly enriched Bacteroides (in green leaf) and Escherichia/Shigella (in yellow pith). Overall, different substrates (either leaf or pith) markedly shaped gut microbiome assemblies and fermentation profiles. The biochemical profile of fermentation products may be an underestimated factor contributing to explain the peculiar dietary behavior of giant pandas, and should be implemented in large scale studies together with short-term lab-scale cultivation of gut microbiomes.

Dataset Information

Potential Mechanism of Detoxification of Cyanide Compounds by Gut Microbiomes of Bamboo-Eating Pandas.

Publications

Potential Mechanism of Detoxification of Cyanide Compounds by Gut Microbiomes of Bamboo-Eating Pandas.

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