Effects of Captivity and Season on the Gut Microbiota of the Brown Frog (Rana dybowskii)

Abstract

The gut microbiota of amphibians is affected by exogenous and endogenous factors. We performed a comprehensive analysis using high-throughput sequencing technology and functional predictions and observed general changes in the gut microbiota of frogs in different growth stages, seasons, and growth environments. There were no significant differences in microbial richness and diversity between juvenile and adult wild frogs, between the summer and autumn groups of captive frogs, or between wild and captive frogs. There were significant differences in the gut microbiota community structure of Rana dybowskii between the summer and autumn groups of captive frogs and between wild and captive R. dybowskii , whereas the differences between juvenile and adult wild frogs were not significant. The dominant gut bacterial phyla in frogs from both captive and wild environments included Firmicutes, Bacteroidetes, Proteobacteria, and Actinobacteria. Linear discriminant effect size (LEfSe) analysis showed that Bacteroidetes and Firmicutes were significantly enriched in captive and wild R. dybowskii , respectively linear discriminant analysis (LDA > 4). The core operational taxonomical units (OTUs) that were found in >90% of all frogs tested encompassed 15 core OTUs. The captive frogs exhibited 15 core OTUs in addition to the above overall core microbiota, whereas the wild frogs exhibited 19 core OTUs in addition to the above overall core microbiota. Predictions made using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) suggested that eleven KEGG pathways, such as infectious diseases, immune system diseases, metabolism, metabolism of other amino acids, metabolism of cofactors and vitamins, metabolism of terpenoids and polyketides, neurodegenerative diseases, and transport and catabolism, were enriched in captive frogs. The relative abundance of several red-leg-syndrome-related pathogens increased significantly in captive frogs compared with that in wild frogs. To our knowledge, this is the first study on the effects of individual seasons and captivity on the gut microbiota of frogs.

Comparison of Gut Microbiota Diversity and Predicted Functions Between Healthy and Diseased Captive Rana dybowskii

“…At present, the brown frog farming industry is stagnant, primarily due to the long growth cycle (at least 18 months from hatching to slaughtering), complex management procedures based on life history (primarily including spawning, hatching, tadpoles, metamorphosis, the growth of 1-year-old young frogs, hibernation, emergence, the growth of 2-year-old young frogs and other stages of feeding and management techniques), and high incidence of disease in frog farms ( Tong et al, 2019 ). Diseases that frequently occur during the growth of frogs are a considerable obstacle to the development of the brown frog aquaculture industry ( Xiang et al, 2018 ; Tong et al, 2019 ). Most diseases of captive amphibians are directly or indirectly related to feeding and management ( Densmore and Green, 2007 ).…”

“…Functional predictions can link the structure of the gut microbiome with the function of the gut microbiota and thus may better clarify the pathogenesis ( Xiong et al, 2017 ; Yu et al, 2018 ). Several studies have shown that captivity may increase the relative abundance of some potential pathogenic bacteria in the amphibian gut microbiota ( Xiang et al, 2018 ; Tong et al, 2019 ). Studies have been conducted on the correlation between disease occurrence and the composition of the gut microbiome in some aquaculture animals (e.g., shrimp) ( Xiang et al, 2018 ; Tong et al, 2019 ).…”

“…Several studies have shown that captivity may increase the relative abundance of some potential pathogenic bacteria in the amphibian gut microbiota ( Xiang et al, 2018 ; Tong et al, 2019 ). Studies have been conducted on the correlation between disease occurrence and the composition of the gut microbiome in some aquaculture animals (e.g., shrimp) ( Xiang et al, 2018 ; Tong et al, 2019 ). However, the current study focuses on the correlation between disease occurrence and the composition of the gut microbiota and on obtaining functional information on how community changes affect microbial correlations ( Yu et al, 2018 ).…”

“…Rana dybowskii (brown frog) is an important aquaculture species with both medicinal and nutritional value ( Tong et al, 2018 ). The conditions in which amphibians live in captivity are highly different from those in the wild, and a higher mortality of frogs occurs at higher densities in culture environments ( Xiang et al, 2018 ; Tong et al, 2019 ). There may be one or more stressors in the cultured environment that indirectly make animals susceptible to disease ( Hedrick, 1998 ; Densmore and Green, 2007 ).…”

Influence of the lab adopted natural diet and environmental and parental microbiota on life history and metabolic phenotype of Drosophila melanogaster larvae

“…The wild populations of gut microbiota in Drosophila was shown to vary with collection location and diet (Adair et al, 2018, Wong et al, 2013, Staubach et al, 2013, Martinez-Porchas et al, 2017. In other insects and wild populations of vertebrates, gut microbiota was shown to change even with seasonality (Behar et al, 2008, Ferguson et al, 2018, Tong and Zhang, 2019, Maurice et al, 2015).…”