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1. Microbial Ecology of Atlantic Salmon ( Salmo salar ) Hatcheries: Impacts of the Built Environment on Fish Mucosal Microbiota

   https://doi.org/10.1128/AEM.00411-20  

   Minich, Jeremiah J.; Poore, Greg D.; Jantawongsri, Khattapan; Johnston, Colin; Bowie, Kate; Bowman, John; Knight, Rob; Nowak, Barbara; Allen, Eric E.; Liu, Shuang-Jiang (June 2020, Applied and Environmental Microbiology)

   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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2. Impacts of the Marine Hatchery Built Environment, Water and Feed on Mucosal Microbiome Colonization Across Ontogeny in Yellowtail Kingfish, Seriola lalandi

   https://doi.org/10.3389/fmars.2021.676731  

   Minich, Jeremiah J.; Nowak, Barbara; Elizur, Abigail; Knight, Rob; Fielder, Stewart; Allen, Eric E. (May 2021, Frontiers in Marine Science)

   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. 

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3. White-nose syndrome restructures bat skin microbiomes

   https://doi.org/10.1128/spectrum.02715-23  

   Ange-Stark, Meghan; Parise, Katy L; Cheng, Tina L; Hoyt, Joseph R; Langwig, Kate E; Frick, Winifred F; Kilpatrick, A Marm; Gillece, John; MacManes, Matthew D; Foster, Jeffrey T (December 2023, Microbiology Spectrum)

   Ding, Xia (Ed.)

   ABSTRACT The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus,Eptesicus fuscus, andPerimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen,Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructanswas present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence ofP. destructansfor any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome inM. lucifugusbut not for other bat species impacted by the disease. IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes ofMyotis lucifugusandPerimyotis subflavusindicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd. 

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4. Microbiome‐mediated effects of habitat fragmentation on native plant performance

   https://doi.org/10.1111/nph.17595  

   Kiesewetter, Kasey N.; Afkhami, Michelle E. (September 2021, New Phytologist)

   Summary Habitat fragmentation is a leading cause of biodiversity and ecosystem function loss in the Anthropocene. Despite the importance of plant–microbiome interactions to ecosystem productivity, we have limited knowledge of how fragmentation affects microbiomes and even less knowledge of its consequences for microbial interactions with plants.Combining field surveys, microbiome sequencing, manipulative experiments, and random forest models, we investigated fragmentation legacy effects on soil microbiomes in imperiled pine rocklands, tested how compositional shifts across 14 fragmentation‐altered soil microbiomes affected performance and resource allocation of three native plant species, and identified fragmentation‐responding microbial families underpinning plant performance.Legacies of habitat fragmentation were associated with significant changes in microbial diversity and composition (across three of four community axes). Experiments showed plants often strongly benefited from the microbiome’s presence, but fragmentation‐associated changes in microbiome composition also significantly affected plant performance and resource allocation across all seven metrics examined. Finally, random forest models identified ten fungal and six bacterial families important for plant performance that changed significantly with fragmentation.Our findings not only support the existence of significant fragmentation effects on natural microbiomes, but also demonstrate for the first time that fragmentation‐associated changes in microbiomes can have meaningful consequences for native plant performance and investment. 

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5. Testing whether adrenal steroids mediate phenotypic and physiologic effects of elevated salinity on larval tiger salamanders

   https://doi.org/10.1111/1749-4877.12669  

   TORNABENE, Brian J.; CRESPI, Erica J.; BREUNER, Creagh W.; HOSSACK, Blake R. (August 2022, Integrative Zoology)

   Abstract Salinity (sodium chloride, NaCl) from anthropogenic sources is a persistent contaminant that negatively affects freshwater taxa. Amphibians can be susceptible to salinity, but some species are innately or adaptively tolerant. Physiological mechanisms mediating tolerance to salinity are still unclear, but changes in osmoregulatory hormones such as corticosterone (CORT) and aldosterone (ALDO) are prime candidates. We exposed larval barred tiger salamanders (Ambystoma mavortium) to environmentally relevant NaCl treatments (<32–4000 mg·L⁻¹) for 24 days to test effects on growth, survival, and waterborne CORT responses. Of those sampled, we also quantified waterborne ALDO from a subset. Using a glucocorticoid antagonist (RU486), we also experimentally suppressed CORT signaling of some larvae to determine if CORT mediates effects of salinity. There were no strong differences in survival among salinity treatments, but salinity reduced dry mass, snout–vent length, and body condition while increasing water content of larvae. High survival and sublethal effects demonstrated that salamanders were physiologically challenged but could tolerate the experimental concentrations. CORT signaling did not attenuate sublethal effects of salinity. Baseline and stress‐induced (after an acute stressor, shaking) CORT were not influenced by salinity. ALDO was correlated with baseline CORT, suggesting it could be difficult to decouple the roles of CORT and ALDO. Future studies comparing ALDO and CORT responses of adaptively tolerant and previously unexposed populations could be beneficial to understand the roles of these hormones in tolerance to salinity. Nevertheless, our study enhances our understanding of the roles of corticosteroid hormones in mediating effects of a prominent anthropogenic stressor. 

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