Salinity drives commensal and free-living bacterial community structures: Examination of the microbial communities of fish, water, and sediment along salinity gradients in two tributaries of the Chesapeake Bay
Wilkinson, Jeremy E.
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Fundulus is an ecologically and geographically diverse genus of small teleost fishes that inhabit coastal estuaries and salt marshes from New Brunswick to Florida along the Atlantic Ocean and from Florida to Texas along the Gulf of Mexico, including the connecting inland systems. Fish in this genus possess the ability to occupy a wide array of habitats that span extremes in salinity, temperature, pH, environmental contaminants, and dissolved oxygen. Some species of Fundulus are able to tolerate habitat extremes by exhibiting highly plastic physiologies, whereas other closely related species have much narrower tolerance ranges. Of particular interest, strong differences in salinity tolerance among species are very apparent. For example, Fundulus heteroclitus, an estuarine species, is capable of tolerating a range of salinities from fresh water to nearly four times the salinity of seawater, whereas F. majalis, a seawater species, can tolerate high marine-level salinities but not fresh water, and F. diaphanus, a freshwater species, can tolerate salinities from freshwater to brackish water but not seawater levels. Salt marshes and estuaries in which Fundulus are found can vary daily in salinity from near freshwater to seawater, depending on the position in the marsh and the time in the tidal cycle. At the mouth of a marsh, close to the ocean, salinity ranges from brackish to seawater depending on the current tidal cycle and the amount of freshwater input, whereas upstream at the headwaters and tributaries, salinities may remain near freshwater for much of the tidal cycle. These transitions between salinity levels in fresh water, brackish water, and seawater are rare in teleost fishes, and because of this, the genus Fundulus provides an excellent model to study the evolution of osmotic tolerances of fishes in response to differing salinities in the environment and their corresponding commensal microbes. Fundulus, sediment, and water were collected from multiple sites along two tributaries in the Chesapeake Bay that exhibit a large range of salinities from freshwater to brackish water to near seawater. Bacterial 16S rRNA gene sequencing was used to identify bacterial communities of Fundulus gill, foregut excreta and mucosa, and hindgut excreta and mucosa body sites and sediment and water samples from their surrounding environment. We found that differing salinity levels in the water in which F. heteroclitus reside alters the fish microbiome in the gills, foregut, and hindgut. These differences were observed in both alpha and beta diversity metrics as well as in community composition. We found functionally redundant taxa shifts within taxonomic levels such as class Gammaproteobacteria in the shift from Aeromonas to Vibrio from low to high salinity. Principle Coordinates Analyses (PCoA) depicted significant salinity based separation of the sites from which the fish were collected. Within the James River, all body site types (gill, foregut excreta, foregut mucosa, hindgut excreta, and hindgut mucosa) revealed separation at the same salinity level (~4 ppt), whereas in the Potomac River the level of separation changes with the body site types, other than in gill and foregut excreta samples where separation occurs at ~1 ppt. Likewise, we observed apparent bacterial differences along the salinity gradients within both tributaries in sediment and water. These differences were illustrated by changes in both alpha and beta diversity as well as community structure. A trend along the salinity gradients was depicted in the PCoAs, with one principal coordinate separating the salinity-based sites and the other principal coordinate separating sediment from water. Salinity-driven clusters were also formed as illustrated by heatmaps. Based on significant spearman correlations, environmental factors were also found to play a major role in the community structure of bacterial assemblages. We also found the gill, foregut, and hindgut microbiomes of F. heteroclitus to be distinctively different from F. diaphanus in freshwater sites within both the Potomac and James Rivers and from F. majalis in brackish water sites in both rivers in the Chesapeake Bay. This was apparent in alpha and beta diversity measures and in bacterial community composition. Each fish species pair maintained similar microbiomes with bacterial genera abundances differing in large amounts for some taxa. These abundance differences indicated fish species-specific dominance of certain bacterial taxa over others. This could stem from preferential commensalism to a host species by the bacteria or vice versa, could be indicative of what the Fundulus species diet is and how it differs from the co-habituating Fundulus species, or the specific bacteria that occur in the niche in which a respective Fundulus species resides. Since the fish in this study are wild-caught fish, their diets and niche-space can be variant and diverse.