Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate
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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00530/full |
| _version_ | 1818684726087516160 |
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| author | Alberto Scoma Alberto Scoma Alberto Scoma Way Cern Khor Marta Coma Robert Heyer Ruben Props Jonas Schoelynck Tim Bouts Dirk Benndorf Dirk Benndorf Desheng Li Hemin Zhang Korneel Rabaey |
| author_facet | Alberto Scoma Alberto Scoma Alberto Scoma Way Cern Khor Marta Coma Robert Heyer Ruben Props Jonas Schoelynck Tim Bouts Dirk Benndorf Dirk Benndorf Desheng Li Hemin Zhang Korneel Rabaey |
| author_sort | Alberto Scoma |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-17T10:55:12Z |
| format | Article |
| id | doaj.art-2961fff9003542569522b65367816337 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-17T10:55:12Z |
| publishDate | 2020-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2961fff9003542569522b653678163372022-12-21T21:51:49ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-03-011110.3389/fmicb.2020.00530519254Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to LactateAlberto Scoma0Alberto Scoma1Alberto Scoma2Way Cern Khor3Marta Coma4Robert Heyer5Ruben Props6Jonas Schoelynck7Tim Bouts8Dirk Benndorf9Dirk Benndorf10Desheng Li11Hemin Zhang12Korneel Rabaey13Center for Microbial Ecology and Technology, University of Ghent, Ghent, BelgiumDepartment of Bioscience, Microbiology Section, Aarhus University, Aarhus C, DenmarkDepartment of Engineering, Biological and Chemical Engineering, Aarhus University, Aarhus N, DenmarkCenter for Microbial Ecology and Technology, University of Ghent, Ghent, BelgiumCenter for Microbial Ecology and Technology, University of Ghent, Ghent, BelgiumBioprocess Engineering, Otto von Guericke University of Magdeburg, Magdeburg, GermanyCenter for Microbial Ecology and Technology, University of Ghent, Ghent, BelgiumDepartment of Biology, University of Antwerp, Antwerp, BelgiumPairi Daiza Foundation, Brugelette, BelgiumBioprocess Engineering, Otto von Guericke University of Magdeburg, Magdeburg, GermanyBioprocess Engineering, Max Planck Institute for Dynamics of Complex Technical Systems, Magdeburg, GermanyChina Conservation and Research Centre for Giant Panda, Dujiangyan City, ChinaChina Conservation and Research Centre for Giant Panda, Dujiangyan City, ChinaCenter for Microbial Ecology and Technology, University of Ghent, Ghent, BelgiumThe 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.https://www.frontiersin.org/article/10.3389/fmicb.2020.00530/fullgiant pandacellulosehemicellulosealpha amylaselignocellulosefermentation |
| spellingShingle | Alberto Scoma Alberto Scoma Alberto Scoma Way Cern Khor Marta Coma Robert Heyer Ruben Props Jonas Schoelynck Tim Bouts Dirk Benndorf Dirk Benndorf Desheng Li Hemin Zhang Korneel Rabaey Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate Frontiers in Microbiology giant panda cellulose hemicellulose alpha amylase lignocellulose fermentation |
| title | Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate |
| title_full | Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate |
| title_fullStr | Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate |
| title_full_unstemmed | Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate |
| title_short | Substrate-Dependent Fermentation of Bamboo in Giant Panda Gut Microbiomes: Leaf Primarily to Ethanol and Pith to Lactate |
| title_sort | substrate dependent fermentation of bamboo in giant panda gut microbiomes leaf primarily to ethanol and pith to lactate |
| topic | giant panda cellulose hemicellulose alpha amylase lignocellulose fermentation |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00530/full |
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