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ABSTRACT A number of key factors can structure the gut microbiota of fish such as environment, diet, health state, and genotype. Mesonauta festivus, an Amazonian cichlid, is a relevant model organism to study the relative contribution of these factors on the community structure of fish gut microbiota. M. festivus has well-studied genetic populations and thrives in rivers with drastically divergent physicochemical characteristics. Here, we collected 167 fish from 12 study sites and used 16S and 18S rRNA metabarcoding approaches to characterize the gut microbiome structure of M. festivus. These data sets were analyzed in light of the host fish genotypes (genotyping-by-sequencing) and an extensive characterization of environmental physico-chemical parameters. We explored the relative contribution of environmental dissimilarity, the presence of parasitic taxa, and phylogenetic relatedness on structuring the gut microbiota. We documented occurrences of Nyctotherus sp. infecting a fish and linked its presence to a dysbiosis of the host gut microbiota. Moreover, we detected the presence of helminths which had a minor impact on the gut microbiota of their host. In addition, our results support a higher impact of the phylogenetic relatedness between fish rather than environmental similarity between sites of study on structuring the gut microbiota for this Amazonian cichlid. Our study in a heterogeneous riverscape integrates a wide range of factors known to structure fish gut microbiomes. It significantly improves understanding of the complex relationship between fish, their parasites, their microbiota, and the environment. IMPORTANCE The gut microbiota is known to play important roles in its host immunity, metabolism, and comportment. Its taxonomic composition is modulated by a complex interplay of factors that are hard to study simultaneously in natural systems. Mesonauta festivus, an Amazonian cichlid, is an interesting model to simultaneously study the influence of multiple variables on the gut microbiota. In this study, we explored the relative contribution of the environmental conditions, the presence of parasitic infections, and the genotype of the host on structuring the gut microbiota of M. festivus in Amazonia. Our results highlighted infections by a parasitic ciliate that caused a disruption of the gut microbiota and by parasitic worms that had a low impact on the microbiota. Finally, our results support a higher impact of the genotype than the environment on structuring the microbiota for this fish. These findings significantly improve understanding of the complex relationship among fish, their parasites, their microbiota, and the environment.

ABSTRACT The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear, and black waters. In black water, important loads of allochthonous humic dissolved organic matter (DOM) result from the bacterioplankton degradation of plant lignin. However, the bacterial taxa involved in this process remain unknown, since Amazonian bacterioplankton has been poorly studied. Its characterization could lead to a better understanding of the carbon cycle in one of the Earth’s most productive hydrological systems. Our study characterized the taxonomic structure and functions of Amazonian bacterioplankton to better understand the interplay between this community and humic DOM. We conducted a field sampling campaign comprising 15 sites distributed across the three main Amazonian water types (representing a gradient of humic DOM), and a 16S rRNA metabarcoding analysis based on bacterioplankton DNA and RNA extracts. Bacterioplankton functions were inferred using 16S rRNA data in combination with a tailored functional database from 90 Amazonian basin shotgun metagenomes from the literature. We discovered that the relative abundances of fluorescent DOM fractions (humic-, fulvic-, and protein-like) were major drivers of bacterioplankton structure. We identified 36 genera for which the relative abundance was significantly correlated with humic DOM. The strongest correlations were found in the Polynucleobacter, Methylobacterium, and Acinetobacter genera, three low abundant but omnipresent taxa that possessed several genes involved in the main steps of the β-aryl ether enzymatic degradation pathway of diaryl humic DOM residues. Overall, this study identified key taxa with DOM degradation genomic potential, the involvement of which in allochthonous Amazonian carbon transformation and sequestration merits further investigation. IMPORTANCE The Amazon basin discharge carries an important load of terrestrially derived dissolved organic matter (DOM) to the ocean. The bacterioplankton from this basin potentially plays important roles in transforming this allochthonous carbon, which has consequences on marine primary productivity and global carbon sequestration. However, the structure and function of Amazonian bacterioplanktonic communities remain poorly studied, and their interactions with DOM are unresolved. In this study, we (i) sampled bacterioplankton in all the main Amazon tributaries, (ii) combined information from the taxonomic structure and functional repertory of Amazonian bacterioplankton communities to understand their dynamics, (iii) identified the main physicochemical parameters shaping bacterioplanktonic communities among a set of >30 measured environmental parameters, and (iv) characterized how bacterioplankton structure varies according to the relative abundance of humic compounds, a by-product from the bacterial degradation process of allochthonous DOM.

ABSTRACT Fish bacterial communities provide functions critical for their host’s survival in contrasting environments. These communities are sensitive to environmental-specific factors (i.e., physicochemical parameters, bacterioplankton), and host-specific factors (i.e., host genetic background). The relative contribution of these factors shaping Amazonian fish bacterial communities is largely unknown. Here, we investigated this topic by analyzing the gill bacterial communities of 240 wild flag cichlids (Mesonauta festivus) from 4 different populations (genetic clusters) distributed across 12 sites in 2 contrasting water types (ion-poor/acidic black water and ion-rich/circumneutral white water). Transcriptionally active gill bacterial communities were characterized by a 16S rRNA metabarcoding approach carried on RNA extractions. They were analyzed using comprehensive data sets from the hosts genetic background (Genotyping-By-Sequencing), the bacterioplankton (16S rRNA) and a set of 34 environmental parameters. Results show that the taxonomic structure of 16S rRNA gene transcripts libraries were significantly different between the 4 genetic clusters and also between the 2 water types. However, results suggest that the contribution of the host’s genetic background was relatively weak in comparison to the environment-related factors in structuring the relative abundance of different active gill bacteria species. This finding was also confirmed by a mixed-effects modeling analysis, which indicated that the dissimilarity between the taxonomic structure of bacterioplanktonic communities possessed the best explicative power regarding the dissimilarity between gill bacterial communities’ structure, while pairwise fixation indexes (FST) from the hosts’ genetic data only had a weak explicative power. We discuss these results in terms of bacterial community assembly processes and flag cichlid fish ecology. IMPORTANCE Host-associated microbial communities respond to factors specific to the host physiology, genetic backgrounds, and life history. However, these communities also show different degrees of sensitivity to environment-dependent factors, such as abiotic physico-chemical parameters and ecological interactions. The relative importance of host- versus environment-associated factors in shaping teleost bacterial communities 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 bacterial communities 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 host’s genetic background was weak compared to environment-related bacterioplanktonic communities in shaping gill bacterial assemblages, 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.