Disruption of fish gut microbiota composition and holobiont’s metabolome by cyanobacterial blooms

Abstract

Background: Cyanobacterial blooms are one of the most common stress encountered by metazoans living in freshwater lentic systems such as lakes and ponds. Blooms reportedly impair fish health, notably through oxygen depletion and production of bioactive compounds including cyanotoxins. However, in the times of the microbiome revolution, it is surprising that so little is still known regarding the influence of blooms on fish microbiota. In this study, an experimental approach is used to demonstrate that blooms affect fish microbiome composition and functions, as well as the metabolome of holobionts. To this end, the model teleost Oryzias latipes is exposed to simulated Microcystis aeruginosa blooms of various intensities in a microcosm setting, and the response of bacterial gut communities is evaluated in terms of composition, metagenome-encoded functions and metabolome profiling. Results: The gut bacterial community of O. latipes exhibits marked responses to the presence of M. aeruginosa blooms in a dose-dependent manner. Notably, abundant gut-associated Firmicutes almost disappear, while potential opportunists increase. The holobiont gut metabolome displays major changes, while functions encoded in the metagenome of bacterial partners are more marginally affected. Bacterial communities tend to return to original composition after the end of the bloom suggesting post-bloom resilience, and remain sensitive in case of a second bloom, reflecting a highly reactive gut community. Conclusion: In the context of increasingly frequent and intense blooms worldwide, results point to the relevance of accounting for short- and long-term microbiome-related effects in fish ecology, with potential outcomes relevant to conservation biology as well as aquaculture.

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

“…In our study system, it is possible that direct interactions exist between both bacterial community types considered here: Bacterioplankton transcriptional activity could affect the activity of bacterial members from the gill microbiome. For example, recent investigations suggested that the production of bioactive compounds, such as cyanotoxins produced by planktonic cyanobacterial strains, can significantly perturb fish microbiomes (Gallet et al . 2021; Duperron et al .…”

“…Indeed, the selection of the bacterioplankton model based on Akaike scores gave a lot of weight to the parsimony criteria, thus advantaging simpler models (Bates et al 2015). Realistically, the global model was the one making the most sense biologically, as it included the influence of all the ecological, physico-chemical and geographical explicative variables considered in this study, which are known to affect the dynamics of host-associated microbiomes in many ecosystems (Goertz et al 2019;Sylvain et al 2020Sylvain et al , 2021Gallet et al 2021). It may seem surprising that the F ST values did not show a significant linear correlation with gill microbiome beta-diversity (Fig.…”

Gut microbiota and holobiont metabolome composition of the Medaka fish (Oryzias latipes) are affected by a short exposure to the cyanobacterium Microcystis aeruginosa

“…Fish were then exposed for 4 days to water, or water containing a strong but environmentally relevant density of the live non-axenic mono-clonal M. aeruginosa strain PMC 728.11 15 of the Paris Museum Collection 16 to simulate a bloom (100 µ g.L -1 Chl a ). The strain was cultured accordingly to anterior publication 11,14 (details in the supplementary information). M. aeruginosa concentrations were estimated after performing Chlorophyll a extractions and absorbance measurements as a proxy using a spectrophotometer 17 (Cary 60 UV-Vis, Agilent).…”

“…Mechanical extraction (GLH850 OMNI; 25 000 r.min -1 ; 30s) followed by sonication (Sonics Vibra-Cell VCX 13; 60% amplitude; 30s) were performed on weighted samples suspended in the extraction solvent (75-25% UHPLC methanol-water, 1 mL per 100 mg of tissue or per 10 mg of lyophilized culture, on ice). After centrifugation (10 min; 4 °C; 15,300 g), gut pellets were dried and used for subsequent DNA extraction 14 .…”

“…A recent study used microcosm-simulated M. aeruginosa blooms by exposing fish to high density of a cyanobacterial culture. Results revealed dose-dependent alterations of the composition of medaka gut bacterial communities and the holobiont metabolome, including a sharp decrease in abundance of a significant Firmicutes symbiont 14 . Altogether, these studies demonstrate that long exposures to cyanobacteria, together with their subsequent metabolites affect fish microbiota, and at least one of those studies also suggests an alteration of holobiont functions correlated with changes in microbiota composition 14 .…”