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

. 2018 Jun 13;3(3):e00229-18. doi: 10.1128/mSphere.00229-18. Print 2018 Jun 27. Potential Mechanism of Detoxification of Cyanide Compounds by Gut Microbiomes of Bamboo-Eating Pandas

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

Lifeng Zhu et al. mSphere. 2018.

. 2018 Jun 13;3(3):e00229-18. doi: 10.1128/mSphere.00229-18. Print 2018 Jun 27. Affiliations

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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.

Keywords: bamboo; comparative genomics; cyanide compound detoxification; gut microbial metagenomes; pandas.

Copyright © 2018 Zhu et al.

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Figures

FIG 1

The cyanide compound concentrations in…

FIG 1

The cyanide compound concentrations in the food of bamboo-eating pandas (giant pandas and…

FIG 1

The cyanide compound concentrations in the food of bamboo-eating pandas (giant pandas and red pandas) and Père David’s deer, and the animals’ gut microbial communities. (A) Cyanide compound concentrations in the dietary plants of bamboo-eating pandas and Père David’s deer. (B) Dominant gut microbial phyla in bamboo-eating-panda and Père David’s deer gut microbiomes. (C) Dominant gut microbial families in bamboo-eating-panda and Père David’s deer gut microbiomes. NS, nonsignificant.

FIG 2

Taxonomic classifications of total predicted…

FIG 2

Taxonomic classifications of total predicted gene sequences among 94 mammal gut metagenomes from…

FIG 2

Taxonomic classifications of total predicted gene sequences among 94 mammal gut metagenomes from the following groups: RP, red pandas; GP, giant pandas; CAR, carnivorous mammals; OM, omnivorous mammals; HE, herbivorous mammals; Milu, Père David’s deer. (A) The top 50 genera among the six groups. (B) Nonmetric multidimensional scaling (NMDS) analysis in Vegan using Bray-Curtis distances of putative genus abundances of 94 fecal microbiota revealed potential dissimilar clusters. GP, 19 fresh samples, three of them from Qinling populations (22); CAR (20); OM (20); HE (20).

FIG 3

Potential for cyanide compound degradation…

FIG 3

Potential for cyanide compound degradation and detoxification by gut microbes from bamboo-eating pandas…

FIG 3

Potential for cyanide compound degradation and detoxification by gut microbes from bamboo-eating pandas (giant pandas and red pandas). (A) The proportions of genes coding for the following putative vital enzymes that are related to the potential degradation and detoxification of cyanide compounds in gut microbiomes of bamboo-eating pandas: nitrilase (Nit) (EC 3.5.5.1), thiosulfate/3-mercaptopyruvate sulfurtransferase (encoded by TST gene, MPST gene, and sseA) (EC 2.8.1.1/2.8.1.2), and cob(I)alamin adenosyltransferase (EC 2.5.1.17). Blue bars, bamboo-eating pandas; dark yellow bars, Père David’s deer. (B) The taxonomic assignments of the identified genes (glpE, TST gene, MPST gene, and sseA) coding for thiosulfate/3-mercaptopyruvate sulfurtransferases (EC 2.8.1.1/2.8.1.2). (C) The taxonomic assignments of the recognized genes coding for nitrilase (EC 3.5.5.1). The relative abundances in panels B and C are the proportions of reads assigned to specific taxa in comparison to total reads (glpE, TST gene, MPST gene, and sseA) coding for putative thiosulfate/3-mercaptopyruvate sulfurtransferases (EC 2.8.1.1/2.8.1.2) or nitrilase (EC 3.5.5.1).

FIG 4

The abundances of genes coding…

FIG 4

The abundances of genes coding for four putative enzymes involved in cyanide compound…

FIG 4

The abundances of genes coding for four putative enzymes involved in cyanide compound degradation and detoxification among 94 gut metagenomes from the following mammal groups: RP, red pandas; GP, giant pandas (19 fresh samples, 3 of them from Qinling populations [22]); CAR, carnivorous mammals (20); OM, omnivorous mammals (20); HE, herbivorous mammals (20); Milu, Père David’s deer.

Similar articles Cited by References
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