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

Blooms of toxic cyanobacteria are a common stress encountered by aquatic fauna. Evidence indicates that long-lasting blooms affect fauna-associated microbiota. Because of their multiple roles, host-associated microbes are nowadays considered relevant to ecotoxicology, yet the respective timing of microbiota versus functional changes in holobionts response needs to be clarified. The response of gut microbiota and holobionts metabolome to exposure to a dense culture of Microcystis aeruginosa was investigated as a microcosm-simulated bloom in the model fish species Oryzias latipes (medaka). Both gut microbiota and gut metabolome displayed significant composition changes after only 2 days of exposure. A dominant symbiont, member of the Firmicutes, plummeted whereas various genera of Proteobacteria and Actinobacteriota increased in relative abundance. Changes in microbiota composition occurred earlier and faster compared to metabolome composition, suggesting that the microbiota drives the holobionts response. Liver and muscle metabolome were much less affected than guts, supporting that gut and associated microbiota are in the front row upon exposure. This study highlights that even short cyanobacterial blooms, that are increasingly frequent, trigger changes in microbiota composition and holobiont metabolome. It emphasizes the relevance of multi-omics approaches to explore organisms response to an ecotoxicological stress. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=118 SRC="FIGDIR/small/499308v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@112a904org.highwire.dtl.DTLVardef@16589forg.highwire.dtl.DTLVardef@1146629org.highwire.dtl.DTLVardef@3f25e4_HPS_FORMAT_FIGEXP M_FIG C_FIG Highlights- A 2-day exposure to a simulated M. aeruginosa bloom is enough to sharply decrease the Firmicute/Proteobacteria ratio in the gut of Oryzias latipes fish. - The exposure induced changes in metabolome composition after 2 days in the gut and 4 days in the liver. - The gut bacterial microbiota response occurred faster than metabolomes; we hypothesize that changes in gut microbiota may drive the gut metabolome compositional changes.