Host-microbiota matching and epigenetic modulation drive Daphnia magna responses to cyanobacterial stress

Microbial communities are crucial in host adaptation to stressors, particularly in dynamic ecosystems. In aquatic environments, Daphnia magna is ideal for studying host-microbiome interactions due to its ecological importance and sensitivity. Adaptation to toxins, such as those produced by cyanobacteria, may involve both host and microbial gene repertoires. Yet, the influence of microbiota composition and function on host performance remains poorly understood. Because epigenetic mechanisms such as DNA methylation regulate gene expression and mediate adaptive responses, we also investigated whether these associations are reflected in DNA methylation levels. To address this, we conducted a fully factorial transplant experiment using microbiota-depleted Daphnia colonised with microbiota from the same or different genotype, previously exposed to toxic or nontoxic diets, or left uncolonised. We assessed life-history traits, microbial composition (16S rRNA genes), functional profiles (whole-genome-resequencing), and DNA methylation (colorimetric quantification). Daphnia fed nontoxic diets grew larger and reproduced more. Increased methylation occurred when microbiota donors differed from the host genotype and was strongest under toxic diet. Dysbiosis and reduced performance were noted in individuals colonised with toxic-diet microbiota from another genotype, where Limnohabitans spp. was reduced or absent. Signs of hormesis emerged when Daphnia received microbiota from their own genotype reared on nontoxic diets. DNA methylation of both host and microbiota was associated with functional pathways, including increased mitochondrial fatty acid biosynthesis. These findings highlight the importance of host-microbiota matching and microbial environmental history in shaping host performance and epigenetic responses, emphasizing the need to consider host-microbe-environment interactions in evolutionary and ecological studies.