Characterization of gill bacterial microbiota in wild Arctic char ( Salvelinus alpinus ) across lakes, rivers, and bays in the Canadian Arctic ecosystems

Abstract

ABSTRACT Teleost gill mucus has a highly diverse microbiota, which plays an essential role in the host’s fitness and is greatly influenced by the environment. Arctic char ( Salvelinus alpinus ), a salmonid well adapted to northern conditions, faces multiple stressors in the Arctic, including water chemistry modifications, that could negatively impact the gill microbiota dynamics related to the host’s health. In the context of increasing environmental disturbances, we aimed to characterize the taxonomic distribution of transcriptionally active taxa within the bacterial gill microbiota of Arctic char in the Canadian Arctic in order to identify active bacterial composition that correlates with environmental factors. For this purpose, a total of 140 adult anadromous individuals were collected from rivers, lakes, and bays belonging to five Inuit communities located in four distinct hydrologic basins in the Canadian Arctic (Nunavut and Nunavik) during spring (May) and autumn (August). Various environmental factors were collected, including latitudes, water and air temperatures, oxygen concentration, pH, dissolved organic carbon (DOC), salinity, and chlorophyll-a concentration. The taxonomic distribution of transcriptionally active taxa within the gill microbiota was quantified by 16S rRNA gene transcripts sequencing. The results showed differential bacterial activity between the different geographical locations, explained by latitude, salinity, and, to a lesser extent, air temperature. Network analysis allowed the detection of a potential dysbiosis signature (i.e., bacterial imbalance) in fish gill microbiota from Duquet Lake in the Hudson Strait and the system Five Mile Inlet connected to the Hudson Bay, both showing the lowest alpha diversity and connectivity between taxa. IMPORTANCE This paper aims to decipher the complex relationship between Arctic char ( Salvelinus alpinus ) and its symbiotic microbial consortium in gills. This salmonid is widespread in the Canadian Arctic and is the main protein and polyunsaturated fatty acids source for Inuit people. The influence of environmental parameters on gill microbiota in wild populations remains poorly understood. However, assessing the Arctic char’s active gill bacterial community is essential to look for potential pathogens or dysbiosis that could threaten wild populations. Here, we concluded that Arctic char gill microbiota was mainly influenced by latitude and air temperature, the latter being correlated with water temperature. In addition, a dysbiosis signature detected in gill microbiota was potentially associated with poor fish health status recorded in these disturbed environments. With those results, we hypothesized that rapid climate change and increasing anthropic activities in the Arctic might profoundly disturb Arctic char gill microbiota, affecting their survival.