BackgroundMicrobial succession in vertebrates has primarily focused on vertical transmission and ontogenetic development in the mammalian gut. Teleosts comprise the majority of vertebrate diversity, yet little is known about how the microbiome develops in fish, particularly when vertical transmission is limited or absent for broadcast spawners. Biological factors such as diet, age, phylogeny, and trophic level along with environmental factors such as water salinity, temperature, and depth have been shown to influence the mucosal microbiomes of fish. Here we investigate how various microbial-rich surfaces from the built environment ‘BE’ influence the development of the mucosal microbiome (gill, skin, and digesta) of an economically important marine fish, yellowtail kingfish, Seriola lalandi, over time.ResultsFor the first experiment, we sampled gill and skin microbiomes from 36 fish reared in three tank conditions, and demonstrate that the gill is more influenced by the surrounding environment than the skin. In a second experiment, fish microbiomes (gill, skin, and digesta) and the BE (tank side, water, inlet pipe, airstones, and air diffusers) were sampled from indoor reared fish at three ages (43 dph, 137 dph, 430 dph; n=12 per age). At 430 dph, 20 additional fish were sampled from an outdoor ocean net pen. A total of 304 samples were processed for 16S rRNA gene sequencing. Gill and skin alpha diversity increased while gut diversity decreased with age. Diversity was much lower in fish from the ocean net pen compared to indoor fish. We quantified the change in community dynamics driven by the BE and show that the gill and skin are most influenced by the BE early in development, with aeration equipment having more impact in later ages, while the gut microbiome becomes increasingly differentiated from the environment over time.ConclusionsOur findings suggest that fish mucosal microbiomes are differentially influenced by the built environment with a high turnover and rapid succession occurring in the gill and skin while the gut microbiome is more stable. We demonstrate how individual components of a hatchery system, especially aeration equipment, may contribute directly to microbiome development in a marine fish. In addition, results demonstrate how early life (larval) exposure to stressors in the rearing environment may influence fish microbiome development which is important for animal health and aquaculture production.