Pseudomonas -associated bacteria play a key role in obtaining nutrition from bamboo for the giant panda ( Ailuropoda melanoleuca )

Author:

Ning Ruihong12,Li Caiwu3,Xia Maohua4,Zhang Yu1,Gan Yunong1,Huang Yan3,Zhang Tianyou5,Song Haitao3,Zhang Siyuan16ORCID,Guo Wei127ORCID

Affiliation:

1. Sichuan Provincial Engineering Laboratory for Prevention and Control Technology of Veterinary Drug Residue in Animal-origin Food, School of Laboratory Medicine, Chengdu Medical College, Chengdu, China

2. CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization, Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, China

3. Key Laboratory of State Forestry and Grassland Administration (SFGA) on Conservation Biology of Rare Animals in the Giant Panda National Park, The China Conservation and Research Center for the Giant Panda (CCRCGP), Chengdu, China

4. Beijing Key Laboratory of Captive Wildlife Technology, Beijing Zoo, Beijing, P.R. China

5. Chimelong Safari Park in Guangdong Province, Guangzhou, China

6. The Second Affiliated Hospital of Chengdu Medical College, China National Nuclear Corporation 416 Hospital, Chengdu, China

7. School of Laboratory Medicine, Chengdu Medical College, Chengdu, China

Abstract

ABSTRACT Gut microbiota plays a vital role in obtaining nutrition from bamboo for giant pandas. However, low cellulase activity has been observed in the panda’s gut. Besides, no specific pathway has been implicated in lignin digestion by gut microbiota of pandas. Therefore, the mechanism by which they obtain nutrients is still controversial. It is necessary to elucidate the precise pathways employed by gut microbiota of pandas to degrade lignin. Here, the metabolic pathways for lignin degradation in pandas were explored by comparing 209 metagenomic sequencing data from wild species with different feeding habits. Lignin degradation central pathways, including beta-ketoadipate and homogentisate pathway, were enriched in the gut of wild bamboo-eating pandas. The gut microbiome of wild bamboo-eating specialists was enriched with genes from pathways implicated in degrading ferulate and p -coumarate into acetyl-CoA and succinyl-CoA, which can potentially provide the raw materials for metabolism in pandas. Specifically, Pseudomonas , as the most dominant gut bacteria genus, was found to be the main bacteria to provide genes involved in lignin or lignin derivative degradation. Herein, three Pseudomonas -associated strains isolated from the feces of wild pandas showed the laccase, lignin peroxidase, and manganese peroxidase activity and extracellular lignin degradation ability in vitro . A potential mechanism for pandas to obtain nutrition from bamboo was proposed based on the results. This study provides novel insights into the adaptive evolution of pandas from the perspective of lignin metabolism. IMPORTANCE Although giant pandas only feed on bamboo, the mechanism of lignin digestion in pandas is unclear. Here, the metabolic pathways for lignin degradation in wild pandas were explored by comparing gut metagenomic from species with different feeding habits. Results showed that lignin degradation central pathways, including beta-ketoadipate and homogentisate pathway, were enriched in the gut of wild bamboo-eating pandas. Genes from pathways involved in degrading ferulate and p -coumarate via beta-ketoadipate pathway were also enriched in bamboo-eating pandas. The final products of the above process, such as acetyl-CoA, can potentially provide the raw materials for metabolism in pandas. Specifically, Pseudomonas , as the most dominant gut bacteria genus, mainly provides genes involved in lignin degradation. Herein, Pseudomonas -associated strains isolated from the feces of pandas could degrade extracellular lignin. These findings suggest that gut microbiome of pandas is crucial in obtaining nutrition from lignin via Pseudomonas , as the main lignin-degrading bacteria.

Funder

MOST | National Natural Science Foundation of China

Publisher

American Society for Microbiology

Subject

Infectious Diseases,Cell Biology,Microbiology (medical),Genetics,General Immunology and Microbiology,Ecology,Physiology

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