Genomic and environmental factors shape gill microbiome activity in an Amazonian teleost holobiont

Fish microbiomes provide functions critical for their hosts survival in contrasting environments. These communities are sensitive to a range of environmental-specific factors (i.e. physicochemical parameters, free-living bacterioplankton) and host-specific factors (i.e. host genetic background). The relative contribution of these genomic and environmental factors shaping Amazonian fish microbiomes is still unknown. Here, we investigated this topic by analyzing the gill microbiomes of 240 wild flag cichlids (Mesonauta festivus) from four different populations (genetic clusters) distributed in 12 sites of two contrasting water types (ion-poor/acidic black water and ion-rich/circumneutral white water). The transcriptionally active gill microbiomes were characterized by a 16S rRNA metabarcoding approach carried on RNA extractions. They were analyzed in light of comprehensive datasets from the hosts genetic background (Genotyping-By-Sequencing), the bacterioplanktonic pool of bacteria (16S rRNA) and a set of 34 environmental parameters. Results show that the transcriptional activity of gill microbiome samples was significantly different between the genetic clusters and between water types. However, they suggest that the contribution of the hosts genetic background was relatively weak in comparison to the environment-related factors in structuring the relative abundance of different gill microbiome transcripts. This result was also confirmed by a mixed-effects modeling analysis, which suggested that the dissimilarity between the transcriptional activity of bacterioplanktonic communities possessed the best explicative power regarding the dissimilarity between gill microbiomes transcripts, while pairwise fixation indexes (FST) from the hosts genetic data only had a weak explicative power. We discuss these results in terms of microbiome assembly processes and flag cichlid fish ecology. ImportanceHost-associated microbial communities respond to a range of factors specific to the host physiology, genetic backgrounds and life history. However, these communities also show different degrees of sensitivity to environment-dependant factors such as abiotic physico-chemical parameters and ecological interactions. The relative importance of host-versus environment-associated factors in shaping teleost microbiomes is still understudied and is paramount for their conservation and aquaculture. Here, we studied the relative importance of host- and environment-associated factors structuring teleost microbiomes using gill samples from a wild Amazonian teleost model (Mesonauta festivus) sampled in contrasting habitats along a 1500 km section of the Amazonian basin, thus ensuring high genetic diversity. Results showed that the contribution of the hosts genetic background was weak compared to environment-related bacterioplanktonic communities in shaping gill microbiomes, thereby suggesting that our understanding of teleost microbiome assembly could benefit from further studies focused on the ecological interplay between host-associated and free-living communities.