Leroux, N. | bioRxiv Science

bioRxiv2022

Fish-microbe systems in the hostile but highly biodiverse Amazonian blackwaters

Amazonian blackwaters are extremely biodiverse systems containing some of the most naturally acidic, dissolved organic carbon-rich and ion-poor waters on Earth. Physiological adaptations of fish facing these ionoregulatory challenges are unresolved but could involve microbially-mediated processes. Here, we characterize the physiological response of 964 fish-microbe systems from four blackwater Teleost species along a natural hydrochemical gradient, using dual RNA-Seq and 16S rRNA of gill samples. We find that responses to blackwaters are host-species-specific, but occasionally include the overexpression of Toll-receptors and integrins associated to interkingdom communication. Blackwater gill microbiomes are characterized by a transcriptionally-active betaproteobacterial cluster potentially interfering with epithelial permeability. We explore further blackwater fish-microbe interactions by analyzing transcriptomes of 320 axenic zebrafish larvae exposed to sterile, non-sterile and inverted (non-native bacterioplankton) blackwater. We find that axenic zebrafish do not survive well when exposed to sterile/inverted blackwater, suggesting an essential role of endogenous symbionts in blackwater fish physiology.

ecology↗

bioRxiv2022

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.

ecology↗

bioRxiv2021

The Amazon River microbiome, a story of humic carbon.

The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear and black waters. Black waters contain important loads of allochthonous humic dissolved organic carbon (DOC), mostly coming from bacteria-mediated lignin degradation, a process that remains understudied. Here, we identified the main bacterial taxa and functions associated with contrasting Amazonian water types, and shed light on their potential implication in the lignin degradation process. We performed an extensive field bacterioplankton sampling campaign from the three Amazonian water types, and combined our observations to a meta-analysis of 90 Amazonian basin shotgun metagenomes used to build a tailored functional inference database. We showed that the overall quality of DOC is a major driver of bacterioplankton structure, transcriptional activity and functional repertory. We also showed that among the taxa mostly associated to differences between water types, Polynucleobacter sinensis particularly stood out, as its abundance and transcriptional activity was strongly correlated to black water environments, and specially to humic DOC concentration. Screening the reference genome of this bacteria, we found genes coding for enzymes implicated in all the main lignin degradation steps, suggesting that this bacteria may play key roles in the carbon cycle processes within the Amazon basin.

ecology↗