The impact of aquaculture system on the microbiome and gut metabolome of juvenile Chinese softshell turtle (Pelodiscus sinensis)

Abstract

The commercial aquatic animal microbiome may markedly affect the successful host's farming in various aquaculture systems. However, very little was known about it. Here, two different aquaculture systems, the rice–fish culture (RFC) and intensive pond culture (IPC) systems, were compared to deconstruct the skin, oral, and gut microbiome, as well as the gut metabolome of juvenile Chinese softshell turtle (Pelodiscus sinensis). Higher alpha‐diversity and functional redundancy of P. sinensis microbial community were found in the RFC than those of the IPC. The aquaculture systems have the strongest influence on the gut microbiome, followed by the skin microbiome, and finally the oral microbiome. Source‐tracking analysis showed that the RFC's microbial community originated from more unknown sources than that of the IPC across all body regions. Strikingly, the RFC's oral and skin microbiome exhibited a significantly higher proportion of generalists and broader habitat niche breadth than those of the IPC, but not the gut. Null model analysis revealed that the RFC's oral and skin microbial community assembly was governed by a significantly greater proportion of deterministic processes than that of the IPC, but not the gut. We further identified the key gene and microbial contribution to five significantly changed gut metabolites, 2‐oxoglutarate, N‐acetyl‐d‐mannosamine, cis‐4‐hydroxy‐d‐proline, nicotinamide, and l‐alanine, which were significantly correlated with important categories of microbe‐mediated processes, including the amino acid metabolism, GABAergic synapse, ABC transporters, biosynthesis of unsaturated fatty acids, as well as citrate cycle. Moreover, different aquaculture systems have a significant impact on the hepatic lipid metabolism and body shape of P. sinensis. Our results provide new insight into the influence of aquaculture systems on the microbial community structure feature and assembly mechanism in an aquatic animal, also highlighting the key microbiome and gene contributions to the metabolite variation in the gut microbiome‐metabolome association.

QMD: A new method to quantify microbial absolute abundance differences between groups

“…As we stated, each group is composed of several samples in common practices. The sample size varies from tens [ 14 , 16 ] to hundreds [ 17 , 18 ]. We use the difference in expectations of logged absolute abundance between groups to estimate microbial absolute abundance changes.…”

Fish predation risk alters the microbiota of Daphnia in the process of inducing its life‐history defence traits

“…The composition of the host‐associated microbiota is highly plastic and capable of being reconfigured in response to environmental changes, thus affecting the host's health and ecological adaptation (Alberdi et al., 2016; Moeller & Sanders, 2020). These plastic changes can be very subtle, may simply activate or inactivate certain metabolic pathways, and may lead to changes in the composition and function of the entire microbial community (Ding et al., 2022). Multiple factors influence the composition of host‐associated bacterial communities, such as the pool of environmental bacteria (Mushegian et al., 2019; Smith et al., 2015), host genotype (Macke, Tasiemski, et al., 2017), host sex (Bolnick et al., 2014), diet (Akbar et al., 2020), and abiotic conditions (Akbar et al., 2021; Ma et al., 2019).…”

Comparative Analysis of the Growth, Physiological Responses, and Gene Expression of Chinese Soft-Shelled Turtles Cultured in Different Modes

“…Turtles have been found to experience less stress in and showed a distinct preference for an enriched environment [ 12 , 13 ] and may have different growth rates or metabolic rates depending on the availability of resources or the presence of stressors [ 14 ]. P. sinensis is an opportunistic predator; in different habitats, it will make adaptive responses in behavior, growth, physiology, and metabolism [ 15 , 16 ]. Growth is a highly complex process that involves the regulation of appetite, muscle growth, and weight gain [ 17 ], which is affected by genetic factors, initial body size, age, sex, and culture conditions [ 18 , 19 ].…”