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Abstract:

Eutrophication and climate change have caused a widespread occurrence of cyanobacterial harmful algal blooms (cyanoHABs) in lakes, ponds and reservoirs worldwide. Due to the release of powerful toxins in the water, CyanoHABs pose severe threats on livestock and human health, causing diseases from gastrointestinal symptoms to liver cancer. In aquatic ecosystems, cyanoHABs have a strong negative impact on zooplankton grazers, and through the food web, disrupt the whole freshwater community. Deciphering the mechanisms underlying resistance to toxic cyanobacteria in these grazers is thus essential to predict how aquatic ecosystems can cope with cyanoHABs. In the freshwater crustacean Daphnia, resistance is influenced by both genotype and earlier exposure to cyanobacteria, but the underlying mechanisms remain unclear. Through gut microbiota transplants, we here show that gut microbiota plays a crucial role, and might mediate both genetic adaptation and acclimatization to cyanoHABs. Resistance to cyanobacteria in recipient Daphnia was not affected by the recipient genotype, but was strongly impacted by the donor genotype. Microbiota from resistant genotypes conferred a higher resistance to recipient Daphnia than microbiota from susceptible genotypes. This suggests that the Daphnia genotype acts indirectly on resistance to cyanobacteria, by shaping the gut microbiota. In addition, resistance was higher when donors were previously fed cyanobacteria, suggesting that gut microbiota responded to become more efficient in dealing with cyanobacteria after prior exposure. Analysis of 16S rDNA suggests that such response resulted from an alteration of the microbiota structure: cyanobacterial exposure favored bacterial taxa involved in digestion of cyanobacterial cells and detoxification of cyanobacterial toxins. Our results provide evidence that gut microbiota drives resistance to toxic cyanobacteria in Daphnia, and might thus act as an important mediator of the genetic mosaic of coevolution between toxic cyanobacteria and their grazers, as well as a key determinant of how freshwater ecosystems respond to climate warming