ABSTRACT Successful rearing of fish in hatcheries is critical for conservation, recreational fishing, commercial fishing through wild stock enhancements, and aquaculture production. Flowthrough (FT) hatcheries require more water than recirculating aquaculture systems (RAS), which enable up to 99% of their water to be recycled, thus significantly reducing environmental impacts. Here, we evaluated the biological and physical microbiome interactions of three Atlantic salmon hatcheries (RAS n = 2, FT n = 1). Gill, skin, and digesta from six juvenile fish along with tank biofilms and water were sampled from tanks in each of the hatcheries (60 fish across 10 tanks) to assess the built environment and mucosal microbiota using 16S rRNA gene sequencing. The water and tank biofilm had more microbial richness than fish mucus, while skin and digesta from RAS fish had 2 times the richness of FT fish. Body sites each had unique microbiomes ( P < 0.001) and were influenced by hatchery system type ( P < 0.001), with RAS being more similar. A strong association between the tank and fish microbiome was observed. Water and tank biofilm richness was positively correlated with skin and digesta richness. Strikingly, the gill, skin, and digesta communities were more similar to that in the origin tank biofilm than those in all other experimental tanks, suggesting that the tank biofilm has a direct influence on fish-associated microbial communities. Lastly, microbial diversity and mucous cell density were positively associated with fish growth and length. The results from this study provide evidence for a link between the tank microbiome and the fish microbiome, with the skin microbiome as an important intermediate. IMPORTANCE Atlantic salmon, Salmo salar , is the most farmed marine fish worldwide, with an annual production of 2,248 million metric tons in 2016. Salmon hatcheries are increasingly changing from flowthrough toward recirculating aquaculture system (RAS) design to accommodate more control over production along with improved environmental sustainability due to lower impacts on water consumption. To date, microbiome studies of hatcheries have focused either on the fish mucosal microbiota or on the built environment microbiota but have not combined the two to understand their interactions. Our study evaluates how the water and tank biofilm microbiota influences the fish microbiota across three mucosal environments (gill, skin, and digesta). Results from this study highlight how the built environment is a unique source of microbes to colonize fish mucus and, furthermore, how this can influence fish health. Further studies can use this knowledge to engineer built environments to modulate fish microbiota for beneficial phenotypes.
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Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, Scomber japonicus
ABSTRACT Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestinal tract [GI], and pyloric ceca) from 229 Pacific chub mackerel, Scomber japonicus , collected across 38 time points spanning 1 year from the Scripps Institution of Oceanography Pier (La Jolla, CA). Mucosal sites had unique microbial communities significantly different from the surrounding seawater and sediment communities with over 10 times more total diversity than seawater. The external surfaces of skin and gill were more similar to seawater, while digesta was more similar to sediment. Alpha and beta diversity of the skin and gill was explained by environmental and biological factors, specifically, sea surface temperature, chlorophyll a , and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by regional migration of chub mackerel subpopulations by nanopore sequencing a 14,769-bp region of the 16,568-bp mitochondria across all temporal fish specimens. A cosmopolitan pathogen, Photobacterium damselae , was prevalent across multiple body sites all year but highest in the skin, GI, and digesta between June and September, when the ocean is warmest. The longitudinal fish microbiome study evaluates the extent to which the environment and host biology drives mucosal microbial ecology and establishes a baseline for long-term surveys linking environment stressors to mucosal health of wild marine fish. IMPORTANCE Pacific chub mackerel, Scomber japonicus , are one of the largest and most economically important fisheries in the world. The fish is harvested for both human consumption and fish meal. Changing ocean conditions driven by anthropogenic stressors like climate change may negatively impact fisheries. One mechanism for this is through disease. As waters warm and chemistry changes, the microbial communities associated with fish may change. In this study, we performed a holistic analysis of all mucosal sites on the fish over a 1-year time series to explore seasonal variation and to understand the environmental drivers of the microbiome. Understanding seasonality in the fish microbiome is also applicable to aquaculture production for producers to better understand and predict when disease outbreaks may occur based on changing environmental conditions in the ocean.
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- Award ID(s):
- 1837116
- NSF-PAR ID:
- 10164948
- Date Published:
- Journal Name:
- mSphere
- Volume:
- 5
- Issue:
- 3
- ISSN:
- 2379-5042
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)The fish gut microbiome is impacted by a number of biological and environmental factors including fish feed formulations. Unlike mammals, vertical microbiome transmission is largely absent in fish and thus little is known about how the gut microbiome is initially colonized during hatchery rearing nor the stability throughout growout stages. Here we investigate how various microbial-rich surfaces from the built environment “BE” and feed influence the development of the mucosal microbiome (gill, skin, and digesta) of an economically important marine fish, yellowtail kingfish, Seriola lalandi , over time. For 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 mucous (gill, skin, and digesta), the BE (tank side, water, inlet pipe, airstones, and air diffusers) and feed were sampled from indoor reared fish at three ages (43, 137, and 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. 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 “allochthonous” microbiome becomes increasingly differentiated from the environment over time. Feed had a relatively low impact on driving microbial communities. Our findings suggest that S. lalandi mucosal microbiomes are differentially influenced by the BE 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 biofouling in the rearing environment may influence fish microbiome development which is important for animal health and aquaculture production.more » « less
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Abstract As a crucial step in developing a bioenergetics model for Pacific Chub Mackerel
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mSphere.00401-20
