Insights into the roles of fungi and protist in the giant panda gut microbiome and antibiotic resistome

Zhu, Dong; Lu, Lu; Zhang, Zejun; Qi, Dunwu; Zhang, Mingchun; O’Connor, Patrick J.; Wei, Fuwen; Zhu, Yong‐Guan

doi:10.1016/j.envint.2021.106703

Cited by 39 publications

(33 citation statements)

References 71 publications

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“…The giant panda retains a typical carnivore digestive system and the adaptation of their gut microbiome to a specialized bamboo diet has been widely studied [ 2 , 8 – 11 ]. Several studies have documented, through metagenomic analyses, the ability of the gut microbiome of giant pandas to digest cellulose and hemicellulose [ 12 – 15 ]. It has been reported that the abundance of microbial genes in the gut of giant pandas contributing to lignocellulose degradation is lower than that of ruminants and other herbivores [ 16 , 17 ], and is affected by diet, habitat environment (captive or wild) and seasonal factors (e.g., climate and food availability) [ 3 , 13 , 18 , 19 ].…”

Section: Introductionmentioning

confidence: 99%

Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Xiao

Liang

et al. 2022

The ISME Journal

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Bamboo rats ( Rhizomys pruinosus ) are among the few mammals that lives on a bamboo-based diet which is mainly composed of lignocellulose. However, the mechanisms of adaptation of their gut microbiome and metabolic systems in the degradation of lignocellulose are largely unknown. Here, we conducted a multi-omics analysis on bamboo rats to investigate the interaction between their gut microbiomes and metabolic systems in the pre- and post-weaning periods, and observed significant relationships between dietary types, gut microbiome, serum metabolome and host gene expression. For comparison, published gut microbial data from the famous bamboo-eating giant panda ( Ailuropoda melanoleuca ) were also used for analysis. We found that the adaptation of the gut microbiome of the bamboo rat to a lignocellulose diet is related to a member switch in the order Bacteroidales from family Bacteroidaceae to family Muribaculaceae , while for the famous bamboo-eating giant panda, several aerobes and facultative anaerobes increase after weaning. The conversion of bacteria with an increased relative abundance in bamboo rats after weaning enriched diverse carbohydrate-active enzymes (CAZymes) associated with lignocellulose degradation and functionally enhanced the biosynthesis of amino acids and B vitamins. Meanwhile, the circulating concentration of short-chain fatty acids (SCFAs) derived metabolites and the metabolic capacity of linoleic acid in the host were significantly elevated. Our findings suggest that fatty acid metabolism, including linoleic acid and SCFAs, are the main energy sources for bamboo rats in response to the low-nutrient bamboo diet.

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Section: Introductionmentioning

confidence: 99%

Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Xiao

Liang

et al. 2022

The ISME Journal

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“…A notable outcome is that composting processes can selectively eliminate manure-derived ARGs, whereas certain beta-lactam and multidrug ARGs were consistently enriched across multiple manure composting processes. Whether these enriched ARGs have risks for compost-receiving environments, the extent to which they lead to variations in the resistome of the compost-receiving environments as well as the evolutionary mechanism determining the ARG dissemination across environments via microbial communities (i.e., bacteria, archaea, and eukaryotes) − , requires further investigation. Accordingly, the current study identifies many indicator ARGs that span an extensive array of matured composts that provide a framework upon which to base future research.…”

Section: Resultsmentioning

confidence: 99%

“…As the other essential components in compost microbiota, fungi and protists (i.e., Ascomycota and Excavata) have also been thought to be antibiotic-resistant , and cause infection outbreaks . Furthermore, recent studies have demonstrated that these two microbial components might impact the evolution and maintenance of antibiotic resistance, , and their biological interactions with bacteria exerted certain selection pressures on the resistance events. , To gain a better understanding of the dissemination of antibiotic resistance, much attention should be paid to the associations between ARGs and a wide range of microbial members (including bacteria, fungi, and protists) in compost ecosystems. Additionally, it remains unexplored how their interdomain interactions impact the fate and dynamics of ARGs during manure composting processes.…”

Section: Introductionmentioning

confidence: 99%

Disentangling the Effects of Physicochemical, Genetic, and Microbial Properties on Phase-Driven Resistome Dynamics during Multiple Manure Composting Processes

Cheng

Zhu

Strong

et al. 2021

Environ. Sci. Technol.

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Composting alters manure-derived antibiotic resistance genes (ARGs) to a certain extent, which is largely dependent upon the composting phase, manure type, microbial phylogeny, and physicochemical properties. However, little is known about how these determinants influence the fate and dynamics of ARGs as well as the mechanisms underlying the ecological process of ARGs during composting. Here, we investigated the temporal patterns of ARGs and their correlations with a series of physicochemical, genetic, and microbial properties during pilotscale composting of chicken, maggot, bovine, and swine manure. We detected 237 ARGs, 71 of which were co-occurring across all four composting processes and accounted for >80% of the sum of resistome abundance. In support of this ARG co-occurrence, variance partition analyses demonstrated that the manure type explained less resistome variations (5.6%) than the composting phase (21.6%). During the phase-driven resistome dynamics, ARGs showed divergent variations in abundance, and certain beta-lactams and multidrug ARGs were consistently enriched across multiple manure composting processes. Correlation analyses all led to the conclusion that the divergent ARG variations during composting were attributable to the unequal effects of physicochemical properties, mobile elements, and succession of indigenous microbiota, whereas antibiotic residues' effects were marginal. Ultimately, this study determines the relative importance of various key determinants in the phase-driven divergence of ARGs during multiple manure composting processes and demonstrates a clear need to evaluate risks posed by enriched ARGs toward their receiving environments.

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“…Multidrug resistance to many different classes of antibiotics, which impedes antibiotic treatment, is a huge risk to human life (Zhu et al, 2013;Ouyang et al, 2015), and is also a potential threat to giant panda health. Several recent studies have shown that diverse ARGs exist in the gut of wild and captive giant pandas, and multidrug resistance genes were the dominant type of ARGs in the giant panda gut (Guo et al, 2019;Hu et al, 2020;Mustafa et al, 2021;Zhu et al, 2021). A survey based on ARGs of human gut microbiota in three countries (China, Denmark, and Spain) found that tetracycline resistance genes were the most abundant group of ARGs, followed by MLSs and beta_lactam resistance genes (Hu et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Giant pandas’ staple food bamboo phyllosphere fungal community and its influencing factors

Kang

Luo²,

Dai³

et al. 2022

Front. Microbiol.

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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.

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Insights into the roles of fungi and protist in the giant panda gut microbiome and antibiotic resistome

Cited by 39 publications

References 71 publications

Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Disentangling the Effects of Physicochemical, Genetic, and Microbial Properties on Phase-Driven Resistome Dynamics during Multiple Manure Composting Processes

Giant pandas’ staple food bamboo phyllosphere fungal community and its influencing factors

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