Topographical Mapping of the Rainbow Trout (Oncorhynchus mykiss) Microbiome Reveals a Diverse Bacterial Community with Antifungal Properties in the Skin

Abstract

The mucosal surfaces of wild and farmed aquatic vertebrates face the threat of many aquatic pathogens, including fungi. These surfaces are colonized by diverse symbiotic bacterial communities that may contribute to fight infection. Whereas the gut microbiome of teleosts has been extensively studied using pyrosequencing, this tool has rarely been employed to study the compositions of the bacterial communities present on other teleost mucosal surfaces. Here we provide a topographical map of the mucosal microbiome of an aquatic vertebrate, the rainbow trout (Oncorhynchus mykiss). Using 16S rRNA pyrosequencing, we revealed novel bacterial diversity at each of the five body sites sampled and showed that body site is a strong predictor of community composition. The skin exhibited the highest diversity, followed by the olfactory organ, gills, and gut. Flectobacillus was highly represented within skin and gill communities. Principal coordinate analysis and plots revealed clustering of external sites apart from internal sites. A highly diverse community was present within the epithelium, as demonstrated by confocal microscopy and pyrosequencing. Using in vitro assays, we demonstrated that two Arthrobacter sp. skin isolates, a Psychrobacter sp. strain, and a combined skin aerobic bacterial sample inhibit the growth of Saprolegnia australis and Mucor hiemalis, two important aquatic fungal pathogens. These results underscore the importance of symbiotic bacterial communities of fish and their potential role for the control of aquatic fungal diseases.T he mucosal surfaces of vertebrate animals are at the interface between the environment and the animal host. Mucosal epithelia form important mechanical and chemical barriers that prevent pathogen invasion but permit colonization by symbiotic microorganisms, the microbiota. The microbiota is crucial for the development, homeostasis, and immune function of an animal's mucosal epithelia (1, 2, 3).The associations between metazoans and commensal microorganisms are among the most ancient and successful associations found in nature (4, 5). The microbial communities of different organisms, such as plants, corals, annelids, gastropods, insects, and many vertebrates, are being characterized. In the particular case of vertebrates, mucosal surfaces have undergone drastic changes over the course of evolution due to the transition of vertebrate animals from water to land. These evolutionary pressures especially affected some mucosal barriers, such as the skin. While the skin of fish is a living cell layer that secretes a mucous layer and has imbricated scales for protection (6), amphibians have a cornified layer of skin that has developed into a more uniform epidermis (6). Finally, in birds and mammals, the presence of feathers, scales, hair, sweat glands, coats, or the leather-like thickening of the dermis represents unique adaptations to terrestrial environments. All these structures and appendages, in turn, provide unique niches within the skin for microbial colonization (6, 7).All verte...

An Economical Custom-Built Drone for Assessing Whale Health

“…It may be possible that bacteria found on whale skin also occur within the respiratory tract or epithelial cells. Tenacibaculum has been associated with the microbiome of other marine species such as southern bluefin tuna (Thunnus maccoyii castelnau) (Valdenegro-Vega et al, 2013), while Psychrobacter is part of the thresher shark and rainbow trout skin microbiome (Lowrey et al, 2015;Doane et al, 2017).…”

B cells and their role in the teleost gut

“…The composition of the microbiota is strongly correlated with a number of factors such as the environment, diet, and genetic backgrounds. Fish intestine harbors approximately 10 7 –10 8 bacteria per gram, represented by 500 species, consisting mainly of aerobic and facultative anaerobe organisms (Austin, 2006; Gomez and Balcazar, 2008; Lowrey et al, 2015; Pérez et al, 2010). As shown by studies in various species across the animal kingdom, the microbiota is essential for optimal host physiology (Sommer and Bäckhed, 2013; Wesemann, 2015).…”

“…Interestingly, very few bacteria were coated with both immunoglobulins, indicating a plausible selective binding of both immunoglobulins to different bacteria strains, or disparate epitopes. However, it is worth pointing out that the gut presents the lowest bacterial diversity among the four MALTs (GIALT, SIALT, GALT, NALT) in trout (Lowrey et al, 2015) and hence, this might be a factor influencing the aforementioned observations regarding immunoglobulin coating of the GALT microbiota. In contrast, the microbiota of both the trout GIALT and NALT present a significantly higher percentage of microbiota coated with more than one immunoglobulin isotype (Tacchi et al, 2014; Xu et al, 2016).…”

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“…Fish epidermis plays an important role in maintaining homeostasis. There is a close relationship between skin damage and microbial colonization (Weber, Chen, & Milton, 2010;Lowrey, Woodhams, Tacchi, & Salinas, 2015). The damage of epidermal layer provides access for infectious agents that enhance the osmotic stress and ultimately foster the mortality rate.…”

“…Thus, pathogens that are totally restricted to the epidermal layer (ectoparasites) are able to kill fish due to the result of osmotic shock related damage of the epidermal layer. Skin damage may affects fish in different ways such as increasing susceptibility to predation (Abbott & Dill, 1985;Lowrey et al, 2015) and reduces oxygen uptake from water (Whitear, 1986). Furthermore, epidermal damage and skin ulcers are also associated with the development of different diseases (Noga, 2000).…”