Rapid and reversible fish skin mucosal microbiota shift toward environmental microbial communities within a day

ABSTRACT Fish are constantly exposed to the surrounding environmental water, and fish skin mucosal microbiota is considered to be strongly influenced by the microbiota of the surrounding environmental water. However, the temporal dynamics of these changes, how rapidly and to what extent the fish skin microbiota becomes similar to the environmental water microbiota, remain unclear. Here, we repeatedly transferred Tanakia lanceolata between an artificial aquaponic system and a pond resembling a natural environment to characterize temporal changes and reproducibility. 16S rRNA gene amplicon analysis revealed that the fish skin microbiota underwent rapid community restructuring within 1 day after transfer and became more similar to the microbial community composition of the destination water than to that of the pre-transfer water. This pattern was consistently observed across two independent experiments involving multiple transfers. The main taxa in the skin belonged to the phylum Proteobacteria. Gammaproteobacteria were abundant in the aquaponics system, whereas Alphaproteobacteria and Actinobacteria were also abundant in Fukada Pond. The core skin microbiota for each environment differed markedly between the two environments and exhibited increases, decreases, or replacement following transfer. Furthermore, alpha diversity of both skin and environmental water microbiota increased in natural ponds and decreased in the aquaponic systems. These findings provide new insights into host-environment microbial interactions and demonstrate the ecological plasticity of fish-associated microbiota in response to rapid environmental changes. IMPORTANCE With respect to the response of the fish skin microbiota to changes in environmental water, high-resolution short-term temporal data would allow for the assessment and management of fish health during short periods, such as transfers between tanks. Here, we revealed that fish skin microbiota is highly plastic and rapidly and reversibly restructures itself in response to environmental changes. Two experiments reproducibly demonstrated that repeatedly transferring fish between different environments leads to the reconstruction of the skin microbiota within 1 day post-transfer, resulting in a composition more similar to that of the destination’s environmental water microbiota than to that of the pre-transfer water. These results indicate that fish skin microbiota respond dynamically to the surrounding microbial environment. These findings provide a foundation for understanding host-environment microbial interactions in fish health management and aquaculture system design.